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Glycolytic enzymes in non-glycolytic web: functional analysis of the key players

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Abstract

To survive in the tumour microenvironment, cancer cells undergo rapid metabolic reprograming and adaptability. One of the key characteristics of cancer is increased glycolytic selectivity and decreased oxidative phosphorylation (OXPHOS). Apart from ATP synthesis, glycolysis is also responsible for NADH regeneration and macromolecular biosynthesis, such as amino acid biosynthesis and nucleotide biosynthesis. This allows cancer cells to survive and proliferate even in low-nutrient and oxygen conditions, making glycolytic enzymes a promising target for various anti-cancer agents. Oncogenic activation is also caused by the uncontrolled production and activity of glycolytic enzymes. Nevertheless, in addition to conventional glycolytic processes, some glycolytic enzymes are involved in non-canonical functions such as transcriptional regulation, autophagy, epigenetic changes, inflammation, various signaling cascades, redox regulation, oxidative stress, obesity and fatty acid metabolism, diabetes and neurodegenerative disorders, and hypoxia. The mechanisms underlying the non-canonical glycolytic enzyme activities are still not comprehensive. This review summarizes the current findings on the mechanisms fundamental to the non-glycolytic actions of glycolytic enzymes and their intermediates in maintaining the tumor microenvironment.

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Abbreviations

2-DG:

2-deoxy-D-glucose

5-TG:

5-thioglucose

6-PGDH:

6-Phosphogluconate dehydrogenase

6-PGL:

6-Phosphogluconolactonase

ACC:

Acetyl CoA Carboxylase

ACS 1:

Acetyl-CoA synthetase

AD:

Alzheimer’s disease

AKT S1:

AKT1 Substrate 1

ALS:

Amyotrophic lateral sclerosis

AMF:

Autocrine motility factor

AMFR:

Autocrine motility factor receptor

AMP:

Adenosine monophosphate

AMPK:

AMP-activated protein kinase

ANLS:

Astrocyte neuron lactate shuttle

APC:

Axin-Adenomatosis Polyposis Coli

APP:

Amyloid precursor protein

ARE:

Anti-oxidant responsive elements

ARNT:

Aryl hydrocarbon receptor nuclear translocator

ATM:

Ataxia- telangiectasia mutant

ATP:

Adenosine triphosphate

BECN1:

Beclin-1

c-AMP:

Cyclic AMP

CBP:

CREB-binding protein

CNS:

Central nervous system

CPT 1:

Carnitine palmitoyl transferase 1

Cyt c:

-Cytochrome c

DNA:

Deoxyribonucleic acid

DVL:

Dishevelled

EGF:

Epidermal growth factor

EGFR:

Epidermal growth factor receptor

ENO1:

Enolase 1

ER:

Endoplasmic reticulum

ERK:

Extracellular signal-regulated kinase

ETC:

Electron transport chain

FAS:

Fatty acid synthesis

FDG-PET:

Fluorodeoxyglucose positron emission tomography

FDH:

Fumarate dehydrogenase

FDH:

Folate dehydrogenase

FIH:

Factor inhibiting HIF

FZD:

Frizzled

G-3-P:

Glyceraldehyde-3-phosphate

GAPD:

Glyceraldehyde 3-phosphate dehydrogenase

GAPDH:

Glyceraldehyde 3-phosphate dehydrogenase

G-CSF:

Granulocyte colony stimulating factor

GFAP:

Glial fibrillary acidic protein

GLK:

Glucokinase

GLP 1:

Glucagon like peptide 1

GLUT 1:

Glucose transporter 1

GM CSF:

Granulocyte-macrophage colony-stimulating factor

GPI:

Glucose 6 phosphate isomerase

GR:

Glutathione reductase

Grx:

Glutaredoxin

GSH:

Glutathione (Reduced)

GSSG:

Glutathione (Oxidized)

GSK 3:

Glycogen synthase kinase 3

HDAC:

Histone deacetylases

HGP:

Hepatic glucose production

HIF:

Hypoxia-inducible factor

HRE:

Hypoxia-responsive elements

Hsp:

Heat shock protein

HXK:

Hexokinase

IDH:

Isocitrate dehydrogenase

IGF 1:

Insulin-like growth factor 1

IL:

Interleukin

JNK:

Jun N-terminal kinase

LAP:

LC3-associated phagocytosis

LC 3:

Microtubule-associated protein 1 A/1B-light chain 3

LDH:

Lactate dehydrogenase

LKB 1:

Liver kinase B1

MBP-1:

c-Myc binding protein 1

MCT 1:

Monocarboxylate transporter 1

ME:

Malic enzyme

MIP 2A:

Macrophage Inflammatory Protein 2

MLOC:

Mitochondrial lactate oxidation complex

mTORC:

Mammalian target of rapamycin

NAC:

N-Acetyl cystine

NAD:

Nicotinamide adenine dinucleotide

NADH:

Nicotinamide adenine dinucleotide (reduced)

NAFLD:

Non-alcoholic fatty liver disease

ND:

Neurodegenerative disease

NGF:

Nerve Growth Factor

NOX:

NADH oxidase

NRF-2:

Nuclear factor erythroid 2- related factor 2

OMM:

Outer mitochondrial membrane

OXPHOS:

Oxidative phosphorylation

PC:

Prostate cancer

PCAF:

p300/CBP associated Factor

PD:

Perkinson’s disease

PDC:

Pyruvate dehydrogenase complex

PDK 1:

Pyruvate dehydrogenase kinase 1

PEP:

Phosphoenolpyruvate

PFK:

Phosphofructokinase

PFKL:

Phosphofructokinase liver type

PGK:

Phosphoglycerate kinase

PHD:

Prolyl Hydroxylase Domain

PIKK:

Phosphatidylinositol-3- kinase

PKM 2:

Pyruvate kinase M2

PPP:

Pentose phosphate pathway

PYK 1:

Pyruvate Kinase

RBC:

Red blood corpuscles

RNA:

Ribonucleic acid

ROS:

Reactive oxygen species

SAICAR:

Succinyl-5-aminoimidazole-4-carboxamide-1-ribose-5’-phosphate

SAM:

S-Adenosyl methionine

SCD 1:

Stearoyl CoA desaturase 1

SDH:

Succinate dehydrogenase

SGLT:

Sodium glucose co-transporter

SOD:

Superoxide dismutase

STAT:

Signal transducer and activator of transcription

STZ:

Streptozotocin

T1DM/T2DM:

Type 1/2 diabetes mellitus

TAZ:

Yes-associated protein 1

TCA:

Tricarboxylic acid cycle

THF:

Tetrahydrofolic acid

TFAM:

Transcription factor A mitochondrial

TPA:

12-O -tetradecanoyl-phorbol-13- acetate

Trx:

Thioredoxin

TXNIP:

Thioredoxin interacting protein

ULK 1:

Unc-51 like autophagy activating kinase

UTR:

Untranslated region

VEGF:

Vascular endothelial growth factor

VHL:

Von-Hippel-Lindau

WNT:

Wingless-related integration site

YAP:

Yes-associated protein 1

References

  1. Yetkin-Arik, B., Vogels, I. M. C., Nowak-Sliwinska, P., Weiss, A., Houtkooper, R. H., Van Noorden, C. J. F., Klaassen, I., & Schlingemann, R. O. (2019). The role of glycolysis and mitochondrial respiration in the formation and functioning of endothelial tip cells during angiogenesis. Scientific Reports, 9(1), 12608. https://doi.org/10.1038/s41598-019-48676-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Lunt, S. Y., & Vander Heiden, M. G. (2011). Aerobic glycolysis: Meeting the metabolic requirements of cell proliferation. Annual Review of Cell and Developmental Biology, 27, 441–464. https://doi.org/10.1146/annurev-cellbio-092910-154237.

    Article  CAS  PubMed  Google Scholar 

  3. Lin, X., Xiao, Z., Chen, T., Liang, S. H., & Guo, H. (2020). Glucose metabolism on tumor plasticity, diagnosis, and treatment. Frontiers in Oncology, 10, 317. https://doi.org/10.3389/fonc.2020.00317.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Canback, B., Andersson, S. G., & Kurland, C. G. (2002). The global phylogeny of glycolytic enzymes. Proceedings of the National Academy of Sciences of the United States of America, 99(9), 6097–6102. https://doi.org/10.1073/pnas.082112499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Shiratori, R., Furuichi, K., Yamaguchi, M., Miyazaki, N., Aoki, H., Chibana, H., Ito, K., & Aoki, S. (2019). Glycolytic suppression dramatically changes the intracellular metabolic profile of multiple cancer cell lines in a mitochondrial metabolism-dependent manner. Scientific Reports, 9(1), 18699. https://doi.org/10.1038/s41598-019-55296-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ganapathy-Kanniappan, S., & Geschwind, J. F. (2013). Tumor glycolysis as a target for cancer therapy: Progress and prospects. Molecular Cancer, 12, 152. https://doi.org/10.1186/1476-4598-12-152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Poellinger, L., & Johnson, R. S. (2004). HIF-1 and hypoxic response: The plot thickens. Current Opinion in Genetics & Development, 14(1), 81–85. https://doi.org/10.1016/j.gde.2003.12.006.

    Article  CAS  Google Scholar 

  8. Schofield, C. J., & Ratcliffe, P. J. (2004). Oxygen sensing by HIF hydroxylases. Nature Reviews Molecular Cell Biology, 5(5), 343–354. https://doi.org/10.1038/nrm1366.

    Article  CAS  PubMed  Google Scholar 

  9. Ohh, M., Park, C. W., Ivan, M., Hoffman, M. A., Kim, T. Y., Huang, L. E., Pavletich, N., Chau, V., & Kaelin, W. G. (2000). Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nature Cell Biology, 2(7), 423–427. https://doi.org/10.1038/35017054.

    Article  CAS  PubMed  Google Scholar 

  10. Semenza, G. L., Jiang, B. H., Leung, S. W., Passantino, R., Concordet, J. P., Maire, P., & Giallongo, A. (1996). Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. The Journal of Biological Chemistry, 271(51), 32529–32537. https://doi.org/10.1074/jbc.271.51.32529.

    Article  CAS  PubMed  Google Scholar 

  11. Ashton, T. M., McKenna, W. G., Kunz-Schughart, L. A., & Higgins, G. S. (2018). Oxidative phosphorylation as an emerging target in cancer therapy. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 24(11), 2482–2490. https://doi.org/10.1158/1078-0432.CCR-17-3070.

    Article  CAS  PubMed  Google Scholar 

  12. Bardella, C., Pollard, P. J., & Tomlinson, I. (2011). SDH mutations in cancer. Biochimica et Biophysica Acta, 1807(11), 1432–1443. https://doi.org/10.1016/j.bbabio.2011.07.003.

    Article  CAS  PubMed  Google Scholar 

  13. Lehtonen, H. J., Kiuru, M., Ylisaukko-Oja, S. K., Salovaara, R., Herva, R., Koivisto, P. A., Vierimaa, O., Aittomäki, K., Pukkala, E., Launonen, V., & Aaltonen, L. A. (2006). Increased risk of cancer in patients with fumarate hydratase germline mutation. Journal of Medical Genetics, 43(6), 523–526. https://doi.org/10.1136/jmg.2005.036400.

    Article  CAS  PubMed  Google Scholar 

  14. Reitman, Z. J., & Yan, H. (2010). Isocitrate dehydrogenase 1 and 2 mutations in cancer: Alterations at a crossroads of cellular metabolism. Journal of the National Cancer Institute, 102(13), 932–941. https://doi.org/10.1093/jnci/djq187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Vander Heiden, M. G., Cantley, L. C., & Thompson, C. B. (2009). Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science (New York, N.Y.), 324(5930), 1029–1033. https://doi.org/10.1126/science.1160809.

    Article  CAS  Google Scholar 

  16. Dang, C. V., & Semenza, G. L. (1999). Oncogenic alterations of metabolism. Trends in Biochemical Sciences, 24(2), 68–72. https://doi.org/10.1016/s0968-0004(98)01344-9.

    Article  CAS  PubMed  Google Scholar 

  17. Muz, B., de la Puente, P., Azab, F., & Azab, A. K. (2015). The role of hypoxia in cancer progression, angiogenesis, metastasis, and resistance to therapy. Hypoxia (Auckland, N.Z.), 3, 83–92. https://doi.org/10.2147/HP.S93413.

    Article  PubMed  Google Scholar 

  18. Selak, M. A., Armour, S. M., MacKenzie, E. D., Boulahbel, H., Watson, D. G., Mansfield, K. D., Pan, Y., Simon, M. C., Thompson, C. B., & Gottlieb, E. (2005). Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell, 7(1), 77–85. https://doi.org/10.1016/j.ccr.2004.11.022.

    Article  CAS  PubMed  Google Scholar 

  19. Moreno, C., Santos, R. M., Burns, R., & Zhang, W. C. (2020). Succinate dehydrogenase and ribonucleic acid networks in cancer and other diseases. Cancers, 12(11), 3237. https://doi.org/10.3390/cancers12113237.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Abou Khouzam, R., Brodaczewska, K., Filipiak, A., Zeinelabdin, N. A., Buart, S., Szczylik, C., Kieda, C., & Chouaib, S. (2021). Tumor hypoxia regulates immune escape/invasion: Influence on angiogenesis and potential impact of hypoxic biomarkers on cancer therapies. Frontiers in Immunology, 11, 613114. https://doi.org/10.3389/fimmu.2020.613114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hompland, T., Fjeldbo, C. S., & Lyng, H. (2021). Tumor hypoxia as a barrier in cancer therapy: Why levels matter. Cancers, 13(3), 499. https://doi.org/10.3390/cancers13030499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Brown, J. M., & Wilson, W. R. (2004). Exploiting tumour hypoxia in cancer treatment. Nature Reviews Cancer, 4(6), 437–447. https://doi.org/10.1038/nrc1367.

    Article  CAS  PubMed  Google Scholar 

  23. Huangyang, P., & Simon, M. C. (2018). Hidden features: Exploring the non-canonical functions of metabolic enzymes. Disease Models & Mechanisms, 11(8), dmm033365. https://doi.org/10.1242/dmm.033365.

    Article  CAS  Google Scholar 

  24. Qvit, N., Joshi, A. U., Cunningham, A. D., Ferreira, J. C., & Mochly-Rosen, D. (2016). Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) protein-protein interaction inhibitor reveals a non-catalytic role for GAPDH oligomerization in cell death. The Journal of Biological Chemistry, 291(26), 13608–13621. https://doi.org/10.1074/jbc.M115.711630.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Snaebjornsson, M. T., & Schulze, A. (2018). Non-canonical functions of enzymes facilitate cross-talk between cell metabolic and regulatory pathways. Experimental & Molecular Medicine, 50(4), 1–16. https://doi.org/10.1038/s12276-018-0065-6.

    Article  CAS  Google Scholar 

  26. Lavik, A. R., McColl, K. S., Lemos, F. O., Kerkhofs, M., Zhong, F., Harr, M., Schlatzer, D., Hamada, K., Mikoshiba, K., Crea, F., Bultynck, G., Bootman, M. D., Parys, J. B., & Distelhorst, C. W. (2022). A non-canonical role for pyruvate kinase M2 as a functional modulator of Ca2+ signalling through IP3 receptors. Biochimica et Biophysica Acta Molecular Cell Research, 1869(4), 119206. https://doi.org/10.1016/j.bbamcr.2021.119206.

    Article  CAS  PubMed  Google Scholar 

  27. Xu, D., Shao, F., Bian, X., Meng, Y., Liang, T., & Lu, Z. (2021). The evolving landscape of noncanonical functions of metabolic enzymes in cancer and other pathologies. Cell Metabolism, 33(1), 33–50. https://doi.org/10.1016/j.cmet.2020.12.015.

    Article  CAS  PubMed  Google Scholar 

  28. Patra, K. C., Wang, Q., Bhaskar, P. T., Miller, L., Wang, Z., Wheaton, W., Chandel, N., Laakso, M., Muller, W. J., Allen, E. L., Jha, A. K., Smolen, G. A., Clasquin, M. F., Robey, B., & Hay, N. (2013). Hexokinase 2 is required for tumor initiation and maintenance and its systemic deletion is therapeutic in mouse models of cancer. Cancer Cell, 24(2), 213–228. https://doi.org/10.1016/j.ccr.2013.06.014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Rodríguez, A., De La Cera, T., Herrero, P., & Moreno, F. (2001). The hexokinase 2 protein regulates the expression of the GLK1, HXK1 and HXK2 genes of Saccharomyces cerevisiae. The Biochemical Journal, 355(Pt 3), 625–631. https://doi.org/10.1042/bj3550625.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Vega, M., Riera, A., Fernández-Cid, A., Herrero, P., & Moreno, F. (2016). Hexokinase 2 is an intracellular glucose sensor of yeast cells that maintains the structure and activity of Mig1 protein repressor complex. The Journal of Biological Chemistry, 291(14), 7267–7285. https://doi.org/10.1074/jbc.M115.711408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Papamichos-Chronakis, M., Gligoris, T., & Tzamarias, D. (2004). The Snf1 kinase controls glucose repression in yeast by modulating interactions between the Mig1 repressor and the Cyc8-Tup1 co-repressor. EMBO Reports, 5(4), 368–372. https://doi.org/10.1038/sj.embor.7400120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Crozet, P., Margalha, L., Confraria, A., Rodrigues, A., Martinho, C., Adamo, M., Elias, C. A., & Baena-González, E. (2014). Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases. Frontiers in Plant Science, 5, 190. https://doi.org/10.3389/fpls.2014.00190.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Adeva-Andany, M., López-Ojén, M., Funcasta-Calderón, R., Ameneiros-Rodríguez, E., Donapetry-García, C., Vila-Altesor, M., & Rodríguez-Seijas, J. (2014). Comprehensive review on lactate metabolism in human health. Mitochondrion, 17, 76–100. https://doi.org/10.1016/j.mito.2014.05.007.

    Article  CAS  PubMed  Google Scholar 

  34. Fiume, L., Vettraino, M., Carnicelli, D., Arfilli, V., Di Stefano, G., & Brigotti, M. (2013). Galloflavin prevents the binding of lactate dehydrogenase A to single stranded DNA and inhibits RNA synthesis in cultured cells. Biochemical and Biophysical Research Communications, 430(2), 466–469. https://doi.org/10.1016/j.bbrc.2012.12.013.

    Article  CAS  PubMed  Google Scholar 

  35. Williams, K. R., Reddigari, S., & Patel, G. L. (1985). Identification of a nucleic acid helix-destabilizing protein from rat liver as lactate dehydrogenase-5. Proceedings of the National Academy of Sciences of the United States of America, 82(16), 5260–5264. https://doi.org/10.1073/pnas.82.16.5260.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zheng, L., Roeder, R. G., & Luo, Y. (2003). S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell, 114(2), 255–266. https://doi.org/10.1016/s0092-8674(03)00552-x.

    Article  CAS  PubMed  Google Scholar 

  37. Fazioli, F., Minichiello, L., Matoska, V., Castagnino, P., Miki, T., Wong, W. T., & Di Fiore, P. P. (1993). Eps8, a substrate for the epidermal growth factor receptor kinase, enhances EGF-dependent mitogenic signals. The EMBO Journal, 12(10), 3799–3808. https://doi.org/10.1002/j.1460-2075.1993.tb06058.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Cattaneo, A., Biocca, S., Corvaja, N., & Calissano, P. (1985). Nuclear localization of a lactic dehydrogenase with single-stranded DNA-binding properties. Experimental Cell Research, 161(1), 130–140. https://doi.org/10.1016/0014-4827(85)90497-5.

    Article  CAS  PubMed  Google Scholar 

  39. Zhong, X. H., & Howard, B. D. (1990). Phosphotyrosine-containing lactate dehydrogenase is restricted to the nuclei of PC12 pheochromocytoma cells. Molecular and Cellular Biology, 10(2), 770–776. https://doi.org/10.1128/mcb.10.2.770-776.1990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Schultz, D. E., Hardin, C. C., & Lemon, S. M. (1996). Specific interaction of glyceraldehyde 3-phosphate dehydrogenase with the 5’-nontranslated RNA of hepatitis A virus. The Journal of Biological Chemistry, 271(24), 14134–14142. https://doi.org/10.1074/jbc.271.24.14134.

    Article  CAS  PubMed  Google Scholar 

  41. Pioli, P. A., Hamilton, B. J., Connolly, J. E., Brewer, G., & Rigby, W. F. (2002). Lactate dehydrogenase is an AU-rich element-binding protein that directly interacts with AUF1. The Journal of Biological Chemistry, 277(38), 35738–35745. https://doi.org/10.1074/jbc.M204002200.

    Article  CAS  PubMed  Google Scholar 

  42. Andrade, J., Pearce, S. T., Zhao, H., & Barroso, M. (2004). Interactions among p22, glyceraldehyde-3-phosphate dehydrogenase and microtubules. The Biochemical Journal, 384(Pt 2), 327–336. https://doi.org/10.1042/BJ20040622.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Cancemi, P., Buttacavoli, M., Roz, E., & Feo, S. (2019). Expression of alpha-enolase (ENO1), Myc promoter-binding protein-1 (MBP-1) and matrix metalloproteinases (MMP-2 and MMP-9) reflect the nature and aggressiveness of breast tumors. International Journal of Molecular Sciences, 20(16), 3952. https://doi.org/10.3390/ijms20163952.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Chaudhary, D., & Miller, D. M. (1995). The c-myc promoter binding protein (MBP-1) and TBP bind simultaneously in the minor groove of the c-myc P2 promoter. Biochemistry, 34(10), 3438–3445. https://doi.org/10.1021/bi00010a036.

    Article  CAS  PubMed  Google Scholar 

  45. Ghosh, A. K., Steele, R., & Ray, R. B. (1999). MBP-1 physically associates with histone deacetylase for transcriptional repression. Biochemical and Biophysical Research Communications, 260(2), 405–409. https://doi.org/10.1006/bbrc.1999.0921.

    Article  CAS  PubMed  Google Scholar 

  46. Ghosh, A. K., Majumder, M., Steele, R., White, R. A., & Ray, R. B. (2001). A novel 16-kilodalton cellular protein physically interacts with and antagonizes the functional activity of c-myc promoter-binding protein 1. Molecular and Cellular Biology, 21(2), 655–662. https://doi.org/10.1128/MCB.21.2.655-662.2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Ogino, T., Yamadera, T., Nonaka, T., Imajoh-Ohmi, S., & Mizumoto, K. (2001). Enolase, a cellular glycolytic enzyme, is required for efficient transcription of Sendai virus genome. Biochemical and Biophysical Research Communications, 285(2), 447–455. https://doi.org/10.1006/bbrc.2001.5160.

    Article  CAS  PubMed  Google Scholar 

  48. Zahra, K., Dey, T., Ashish, Mishra, S. P., & Pandey, U. (2020). Pyruvate kinase M2 and cancer: The role of PKM2 in promoting tumorigenesis. Frontiers in Oncology, 10, 159. https://doi.org/10.3389/fonc.2020.00159.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Azoitei, N., Becher, A., Steinestel, K., Rouhi, A., Diepold, K., Genze, F., Simmet, T., & Seufferlein, T. (2016). PKM2 promotes tumor angiogenesis by regulating HIF-1α through NF-κB activation. Molecular Cancer, 15, 3. https://doi.org/10.1186/s12943-015-0490-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Demaria, M., & Poli, V. (2012). PKM2, STAT3 and HIF-1α: The Warburg’s vicious circle. JAK-STAT, 1(3), 194–196. https://doi.org/10.4161/jkst.20662.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Li, X., Zheng, Y., & Lu, Z. (2016). PGK1 is a new member of the protein kinome. Cell Cycle (Georgetown, Tex.), 15(14), 1803–1804. https://doi.org/10.1080/15384101.2016.1179037.

    Article  CAS  PubMed  Google Scholar 

  52. Yi, W., Clark, P. M., Mason, D. E., Keenan, M. C., Hill, C., Goddard, 3rd, W. A., Peters, E. C., Driggers, E. M., & Hsieh-Wilson, L. C. (2012). Phosphofructokinase 1 glycosylation regulates cell growth and metabolism. Science (New York, N.Y.), 337(6097), 975–980. https://doi.org/10.1126/science.1222278.

    Article  CAS  PubMed  Google Scholar 

  53. Simula, L., Alifano, M., & Icard, P. (2022). How phosphofructokinase-1 promotes PI3K and YAP/TAZ in cancer: Therapeutic perspectives. Cancers, 14(10), 2478. https://doi.org/10.3390/cancers14102478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Miller, J. L., & Grant, P. A. (2013). The role of DNA methylation and histone modifications in transcriptional regulation in humans. Sub-Cellular Biochemistry, 61, 289–317. https://doi.org/10.1007/978-94-007-4525-4_13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Meier, J. L. (2013). Metabolic mechanisms of epigenetic regulation. ACS Chemical Biology, 8(12), 2607–2621. https://doi.org/10.1021/cb400689r.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Fan, J., Krautkramer, K. A., Feldman, J. L., & Denu, J. M. (2015). Metabolic regulation of histone post-translational modifications. ACS Chemical Biology, 10(1), 95–108. https://doi.org/10.1021/cb500846u.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Boon, R. (2021). Metabolic fuel for epigenetic: Nuclear production meets local consumption. Frontiers in Genetics, 12, 768996. https://doi.org/10.3389/fgene.2021.768996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Sivanand, S., Viney, I., & Wellen, K. E. (2018). Spatiotemporal control of acetyl-CoA metabolism in chromatin regulation. Trends in Biochemical Sciences, 43(1), 61–74. https://doi.org/10.1016/j.tibs.2017.11.004.

    Article  CAS  PubMed  Google Scholar 

  59. Kornacki, J. R., Stuparu, A. D., & Mrksich, M. (2015). Acetyltransferase p300/CBP associated Factor (PCAF) regulates crosstalk-dependent acetylation of histone H3 by distal site recognition. ACS Chemical Biology, 10(1), 157–164. https://doi.org/10.1021/cb5004527.

    Article  CAS  PubMed  Google Scholar 

  60. Evans, C. G., Chang, L., & Gestwicki, J. E. (2010). Heat shock protein 70 (hsp70) as an emerging drug target. Journal of Medicinal Chemistry, 53(12), 4585–4602. https://doi.org/10.1021/jm100054f.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Zhao, Z., & Shilatifard, A. (2019). Epigenetic modifications of histones in cancer. Genome Biology, 20(1), 245. https://doi.org/10.1186/s13059-019-1870-5.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Friis, R. M., Wu, B. P., Reinke, S. N., Hockman, D. J., Sykes, B. D., & Schultz, M. C. (2009). A glycolytic burst drives glucose induction of global histone acetylation by picNuA4 and SAGA. Nucleic Acids Research, 37(12), 3969–3980. https://doi.org/10.1093/nar/gkp270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Hellemann, E., Walker, J. L., Lesko, M. A., Chandrashekarappa, D. G., Schmidt, M. C., O’Donnell, A. F., & Durrant, J. D. (2022). Novel mutation in hexokinase 2 confers resistance to 2-deoxyglucose by altering protein dynamics. PLoS Computational Biology, 18(3), e1009929. https://doi.org/10.1371/journal.pcbi.1009929.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Cheng, T., Sudderth, J., Yang, C., Mullen, A. R., Jin, E. S., Matés, J. M., & DeBerardinis, R. J. (2011). Pyruvate carboxylase is required for glutamine-independent growth of tumor cells. Proceedings of the National Academy of Sciences of the United States of America, 108(21), 8674–8679. https://doi.org/10.1073/pnas.1016627108.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Ucar, D., Hu, Q., & Tan, K. (2011). Combinatorial chromatin modification patterns in the human genome revealed by subspace clustering. Nucleic Acids Research, 39(10), 4063–4075. https://doi.org/10.1093/nar/gkr016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Matsuda, S., Adachi, J., Ihara, M., Tanuma, N., Shima, H., Kakizuka, A., Ikura, M., Ikura, T., & Matsuda, T. (2016). Nuclear pyruvate kinase M2 complex serves as a transcriptional coactivator of arylhydrocarbon receptor. Nucleic Acids Research, 44(2), 636–647. https://doi.org/10.1093/nar/gkv967.

    Article  CAS  PubMed  Google Scholar 

  67. Latham, T., Mackay, L., Sproul, D., Karim, M., Culley, J., Harrison, D. J., Hayward, L., Langridge-Smith, P., Gilbert, N., & Ramsahoye, B. H. (2012). Lactate, a product of glycolytic metabolism, inhibits histone deacetylase activity and promotes changes in gene expression. Nucleic Acids Research, 40(11), 4794–4803. https://doi.org/10.1093/nar/gks066.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Watanabe, H., Inaba, Y., Kimura, K., Matsumoto, M., Kaneko, S., Kasuga, M., & Inoue, H. (2018). Sirt2 facilitates hepatic glucose uptake by deacetylating glucokinase regulatory protein. Nature Communications, 9(1), 30. https://doi.org/10.1038/s41467-017-02537-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Cantó, C., Gerhart-Hines, Z., Feige, J. N., Lagouge, M., Noriega, L., Milne, J. C., Elliott, P. J., Puigserver, P., & Auwerx, J. (2009). AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature, 458(7241), 1056–1060. https://doi.org/10.1038/nature07813.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Yang, W., Xia, Y., Hawke, D., Li, X., Liang, J., Xing, D., Aldape, K., Hunter, T., Alfred Yung, W. K., & Lu, Z. (2012). PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis. Cell, 150(4), 685–696. https://doi.org/10.1016/j.cell.2012.07.018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Yu, Q., Tong, C., Luo, M., Xue, X., Mei, Q., Ma, L., Yu, X., Mao, W., Kong, L., Yu, X., & Li, S. (2017). Regulation of SESAME-mediated H3T11 phosphorylation by glycolytic enzymes and metabolites. PloS One, 12(4), e0175576. https://doi.org/10.1371/journal.pone.0175576.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. He, H., Lee, M. C., Zheng, L. L., Zheng, L., & Luo, Y. (2013). Integration of the metabolic/redox state, histone gene switching, DNA replication and S-phase progression by moonlighting metabolic enzymes. Bioscience Reports, 33(2), e00018. https://doi.org/10.1042/BSR20120059.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Cai, L., Sutter, B. M., Li, B., & Tu, B. P. (2011). Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Molecular Cell, 42(4), 426–437. https://doi.org/10.1016/j.molcel.2011.05.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Lozoya, O. A., Wang, T., Grenet, D., Wolfgang, T. C., Sobhany, M., Ganini da Silva, D., Riadi, G., Chandel, N., Woychik, R. P., & Santos, J. H. (2019). Mitochondrial acetyl-CoA reversibly regulates locus-specific histone acetylation and gene expression. Life Science Alliance, 2(1), e201800228. https://doi.org/10.26508/lsa.201800228.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Ma, R., Wu, Y., Li, S., & Yu, X. (2021). Interplay between glucose metabolism and chromatin modifications in cancer. Frontiers in Cell and Developmental Biology, 9, 654337. https://doi.org/10.3389/fcell.2021.654337.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Keller, K. E., Doctor, Z. M., Dwyer, Z. W., & Lee, Y. S. (2014). SAICAR induces protein kinase activity of PKM2 that is necessary for sustained proliferative signaling of cancer cells. Molecular Cell, 53(5), 700–709. https://doi.org/10.1016/j.molcel.2014.02.015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Rosa, F., & Osorio, J. S. (2020). Quantitative determination of histone methylation via fluorescence resonance energy transfer (FRET) technology in immortalized bovine mammary alveolar epithelial cells supplemented with methionine. PloS One, 15(12), e0244135. https://doi.org/10.1371/journal.pone.0244135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Amelio, I., Cutruzzolá, F., Antonov, A., Agostini, M., & Melino, G. (2014). Serine and glycine metabolism in cancer. Trends in Biochemical Sciences, 39(4), 191–198. https://doi.org/10.1016/j.tibs.2014.02.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Ghergurovich, J. M., Xu, X., Wang, J. Z., Yang, L., Ryseck, R. P., Wang, L., & Rabinowitz, J. D. (2021). Methionine synthase supports tumour tetrahydrofolate pools. Nature Metabolism, 3(11), 1512–1520. https://doi.org/10.1038/s42255-021-00465-w.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Liu, M., Saha, N., Gajan, A., Saadat, N., Gupta, S. V., & Pile, L. A. (2020). A complex interplay between SAM synthetase and the epigenetic regulator SIN3 controls metabolism and transcription. The Journal of Biological Chemistry, 295(2), 375–389. https://doi.org/10.1074/jbc.RA119.010032.

    Article  CAS  PubMed  Google Scholar 

  81. Wong, C. C., Qian, Y., & Yu, J. (2017). Interplay between epigenetics and metabolism in oncogenesis: Mechanisms and therapeutic approaches. Oncogene, 36(24), 3359–3374. https://doi.org/10.1038/onc.2016.485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Gatla, H. R., Muniraj, N., Thevkar, P., Yavvari, S., Sukhavasi, S., & Makena, M. R. (2019). Regulation of chemokines and cytokines by histone deacetylases and an update on histone decetylase inhibitors in human diseases. International Journal of Molecular Sciences, 20(5), 1110. https://doi.org/10.3390/ijms20051110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Das, P., & Taube, J. H. (2020). Regulating methylation at H3K27: A trick or treat for cancer cell plasticity. Cancers, 12(10), 2792. https://doi.org/10.3390/cancers12102792.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Soto-Heredero, G., Gómez de Las Heras, M. M., Gabandé-Rodríguez, E., Oller, J., & Mittelbrunn, M. (2020). Glycolysis - a key player in the inflammatory response. The FEBS Journal, 287(16), 3350–3369. https://doi.org/10.1111/febs.15327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Dinarello, C. A. (2018). Overview of the IL-1 family in innate inflammation and acquired immunity. Immunological Reviews, 281(1), 8–27. https://doi.org/10.1111/imr.12621.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Sutinen, E. M., Pirttilä, T., Anderson, G., Salminen, A., & Ojala, J. O. (2012). Pro-inflammatory interleukin-18 increases Alzheimer’s disease-associated amyloid-β production in human neuron-like cells. Journal of Neuroinflammation, 9, 199. https://doi.org/10.1186/1742-2094-9-199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Missiroli, S., Genovese, I., Perrone, M., Vezzani, B., Vitto, V. A. M., & Giorgi, C. (2020). The role of mitochondria in inflammation: From cancer to neurodegenerative disorders. Journal of Clinical Medicine, 9(3), 740. https://doi.org/10.3390/jcm9030740.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Bhattacharya, S., Ploplis, V. A., & Castellino, F. J. (2012). Bacterial plasminogen receptors utilize host plasminogen system for effective invasion and dissemination. Journal of Biomedicine & Biotechnology, 2012, 482096. https://doi.org/10.1155/2012/482096.

    Article  CAS  Google Scholar 

  89. Yatsenko, T., Skrypnyk, M., Troyanovska, O., Tobita, M., Osada, T., Takahashi, S., Hattori, K., & Heissig, B. (2023). The role of the plasminogen/plasmin system in inflammation of the oral cavity. Cells, 12(3), 445. https://doi.org/10.3390/cells12030445.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Tristan, C., Shahani, N., Sedlak, T. W., & Sawa, A. (2011). The diverse functions of GAPDH: Views from different subcellular compartments. Cellular Signalling, 23(2), 317–323. https://doi.org/10.1016/j.cellsig.2010.08.003.

    Article  CAS  PubMed  Google Scholar 

  91. Liao, S. T., Han, C., Xu, D. Q., Fu, X. W., Wang, J. S., & Kong, L. Y. (2019). 4-Octyl itaconate inhibits aerobic glycolysis by targeting GAPDH to exert anti-inflammatory effects. Nature Communications, 10(1), 5091. https://doi.org/10.1038/s41467-019-13078-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Millet, P., Vachharajani, V., McPhail, L., Yoza, B., & McCall, C. E. (2016). GAPDH Binding to TNF-α mRNA Contributes to Posttranscriptional Repression in Monocytes: A Novel Mechanism of Communication between Inflammation and Metabolism. Journal of Immunology (Baltimore, Md.: 1950), 196(6), 2541–2551. https://doi.org/10.4049/jimmunol.1501345.

    Article  CAS  PubMed  Google Scholar 

  93. Lo Presti, M., Ferro, A., Contino, F., Mazzarella, C., Sbacchi, S., Roz, E., Lupo, C., Perconti, G., Giallongo, A., Migliorini, P., Marrazzo, A., & Feo, S. (2010). Myc promoter-binding protein-1 (MBP-1) is a novel potential prognostic marker in invasive ductal breast carcinoma. PloS One, 5(9), e12961. https://doi.org/10.1371/journal.pone.0012961.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Miller, D. M., Thomas, S. D., Islam, A., Muench, D., & Sedoris, K. (2012). c-Myc and cancer metabolism. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 18(20), 5546–5553. https://doi.org/10.1158/1078-0432.CCR-12-0977.

    Article  CAS  PubMed  Google Scholar 

  95. Sedoris, K. C., Thomas, S. D., & Miller, D. M. (2010). Hypoxia induces differential translation of enolase/MBP-1. BMC Cancer, 10, 157. https://doi.org/10.1186/1471-2407-10-157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Goverman, J. (2009). Autoimmune T cell responses in the central nervous system. Nature Reviews Immunology, 9(6), 393–407. https://doi.org/10.1038/nri2550.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Liu, Z., Zhang, A., Zheng, L., Johnathan, A. F., Zhang, J., & Zhang, G. (2018). The biological significance and regulatory mechanism of c-Myc binding protein 1 (MBP-1). International Journal of Molecular Sciences, 19(12), 3868. https://doi.org/10.3390/ijms19123868.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Huang, C. K., Sun, Y., Lv, L., & Ping, Y. (2022). ENO1 and cancer. Molecular Therapy Oncolytics, 24, 288–298. https://doi.org/10.1016/j.omto.2021.12.026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Su, Q., Tao, T., Tang, L., Deng, J., Darko, K. O., Zhou, S., Peng, M., He, S., Zeng, Q., Chen, A. F., & Yang, X. (2018). Down-regulation of PKM2 enhances anticancer efficiency of THP on bladder cancer. Journal of Cellular and Molecular Medicine, 22(5), 2774–2790. https://doi.org/10.1111/jcmm.13571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Gupta, V., & Bamezai, R. N. (2010). Human pyruvate kinase M2: A multifunctional protein. Protein Science: A Publication of the Protein Society, 19(11), 2031–2044. https://doi.org/10.1002/pro.505.

    Article  CAS  PubMed  Google Scholar 

  101. Corcoran, S. E., & O’Neill, L. A. (2016). HIF1α and metabolic reprogramming in inflammation. The Journal of Clinical Investigation, 126(10), 3699–3707. https://doi.org/10.1172/JCI84431.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Dietrich, C., & Kaina, B. (2010). The aryl hydrocarbon receptor (AhR) in the regulation of cell-cell contact and tumor growth. Carcinogenesis, 31(8), 1319–1328. https://doi.org/10.1093/carcin/bgq028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Israelsen, W. J., & Vander Heiden, M. G. (2015). Pyruvate kinase: Function, regulation and role in cancer. Seminars in Cell & Developmental Biology, 43, 43–51. https://doi.org/10.1016/j.semcdb.2015.08.004.

    Article  CAS  Google Scholar 

  104. Tang, Y., Gu, S., Zhu, L., Wu, Y., Zhang, W., & Zhao, C. (2022). LDHA: The Obstacle to T cell responses against tumor. Frontiers in Oncology, 12, 1036477. https://doi.org/10.3389/fonc.2022.1036477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Van Wilpe, S., Koornstra, R., Den Brok, M., De Groot, J. W., Blank, C., De Vries, J., Gerritsen, W., & Mehra, N. (2020). Lactate dehydrogenase: A marker of diminished antitumor immunity. Oncoimmunology, 9(1), 1731942. https://doi.org/10.1080/2162402X.2020.1731942.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Serra, M., Di Matteo, M., Serneels, J., Pal, R., Cafarello, S. T., Lanza, M., Sanchez-Martin, C., Evert, M., Castegna, A., Calvisi, D. F., Mazzone, M., & Columbano, A. (2022). Deletion of lactate dehydrogenase-A impairs oncogene-induced mouse hepatocellular carcinoma development. Cellular and Molecular Gastroenterology and Hepatology, 14(3), 609–624. https://doi.org/10.1016/j.jcmgh.2022.06.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Chen, J., Adamiak, W., Huang, G., Atasoy, U., Rostami, A., & Yu, S. (2017). Interaction of RNA-binding protein HuR and miR-466i regulates GM-CSF expression. Scientific Reports, 7(1), 17233. https://doi.org/10.1038/s41598-017-17371-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Elmore, S. (2007). Apoptosis: A review of programmed cell death. Toxicologic Pathology, 35(4), 495–516. https://doi.org/10.1080/01926230701320337.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Mason, E. F., & Rathmell, J. C. (2011). Cell metabolism: An essential link between cell growth and apoptosis. Biochimica et Biophysica Acta, 1813(4), 645–654. https://doi.org/10.1016/j.bbamcr.2010.08.011.

    Article  CAS  PubMed  Google Scholar 

  110. Schoeniger, A., Wolf, P., & Edlich, F. (2022). How do hexokinases inhibit receptor-mediated apoptosis? Biology, 11(3), 412. https://doi.org/10.3390/biology11030412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Garrido, C., Galluzzi, L., Brunet, M., Puig, P. E., Didelot, C., & Kroemer, G. (2006). Mechanisms of cytochrome c release from mitochondria. Cell Death and Differentiation, 13(9), 1423–1433. https://doi.org/10.1038/sj.cdd.4401950.

    Article  CAS  PubMed  Google Scholar 

  112. Szlyk, B., Braun, C. R., Ljubicic, S., Patton, E., Bird, G. H., Osundiji, M. A., Matschinsky, F. M., Walensky, L. D., & Danial, N. N. (2014). A phospho-BAD BH3 helix activates glucokinase by a mechanism distinct from that of allosteric activators. Nature Structural & Molecular Biology, 21(1), 36–42. https://doi.org/10.1038/nsmb.2717.

    Article  CAS  Google Scholar 

  113. Jahan, I., Corbin, K. L., Bogart, A. M., Whitticar, N. B., Waters, C. D., Schildmeyer, C., Vann, N. W., West, H. L., Law, N. C., Wiseman, J. S., & Nunemaker, C. S. (2018). Reducing glucokinase activity restores endogenous pulsatility and enhances insulin secretion in Islets From db/db mice. Endocrinology, 159(11), 3747–3760. https://doi.org/10.1210/en.2018-00589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. White, M. R., & Garcin, E. D. (2016). The sweet side of RNA regulation: Glyceraldehyde-3-phosphate dehydrogenase as a noncanonical RNA-binding protein. Wiley interdisciplinary reviews. RNA, 7(1), 53–70. https://doi.org/10.1002/wrna.1315.

    Article  CAS  PubMed  Google Scholar 

  115. Chuang, D. M., Hough, C., & Senatorov, V. V. (2005). Glyceraldehyde-3-phosphate dehydrogenase, apoptosis, and neurodegenerative diseases. Annual Review of Pharmacology and Toxicology, 45, 269–290. https://doi.org/10.1146/annurev.pharmtox.45.120403.095902.

    Article  CAS  PubMed  Google Scholar 

  116. Shashidharan, P., Chalmers-Redman, R. M., Carlile, G. W., Rodic, V., Gurvich, N., Yuen, T., Tatton, W. G., & Sealfon, S. C. (1999). Nuclear translocation of GAPDH-GFP fusion protein during apoptosis. Neuroreport, 10(5), 1149–1153. https://doi.org/10.1097/00001756-199904060-00045.

    Article  CAS  PubMed  Google Scholar 

  117. Gibson, R. M. (2001). Does apoptosis have a role in neurodegeneration? BMJ (Clinical research ed.), 322(7301), 1539–1540. https://doi.org/10.1136/bmj.322.7301.1539.

    Article  CAS  PubMed  Google Scholar 

  118. El Kadmiri, N., Slassi, I., El Moutawakil, B., Nadifi, S., Tadevosyan, A., Hachem, A., & Soukri, A. (2014). Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and Alzheimer’s disease. Pathologie-Biologie, 62(6), 333–336. https://doi.org/10.1016/j.patbio.2014.08.002.

    Article  CAS  PubMed  Google Scholar 

  119. Mikhaylova, E. R., Lazarev, V. F., Nikotina, A. D., Margulis, B. A., & Guzhova, I. V. (2016). Glyceraldehyde 3-phosphate dehydrogenase augments the intercellular transmission and toxicity of polyglutamine aggregates in a cell model of Huntington disease. Journal of Neurochemistry, 136(5), 1052–1063. https://doi.org/10.1111/jnc.13463.

    Article  CAS  PubMed  Google Scholar 

  120. Schulz, L. C., & Bahr, J. M. (2003). Glucose-6-phosphate isomerase is necessary for embryo implantation in the domestic ferret. Proceedings of the National Academy of Sciences of the United States of America, 100(14), 8561–8566. https://doi.org/10.1073/pnas.1531024100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Coulam, C. B., Kaider, B. D., Kaider, A. S., Janowicz, P., & Roussev, R. G. (1997). Antiphospholipid antibodies associated with implantation failure after IVF/ET. Journal of Assisted Reproduction and Genetics, 14(10), 603–608. https://doi.org/10.1023/a:1022588903620.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Li, Y., Jia, Y., Che, Q., Zhou, Q., Wang, K., & Wan, X. P. (2015). AMF/PGI-mediated tumorigenesis through MAPK-ERK signaling in endometrial carcinoma. Oncotarget, 6(28), 26373–26387. https://doi.org/10.18632/oncotarget.4708.

    Article  PubMed  PubMed Central  Google Scholar 

  123. Nakajima, K., & Raz, A. (2020). Autocrine motility factor and its receptor expression in musculoskeletal tumors. Journal of Bone Oncology, 24, 100318. https://doi.org/10.1016/j.jbo.2020.100318.

    Article  PubMed  PubMed Central  Google Scholar 

  124. Lucarelli, G., Rutigliano, M., Sanguedolce, F., Galleggiante, V., Giglio, A., Cagiano, S., Bufo, P., Maiorano, E., Ribatti, D., Ranieri, E., Gigante, M., Gesualdo, L., Ferro, M., de Cobelli, O., Buonerba, C., Di Lorenzo, G., De Placido, S., Palazzo, S., Bettocchi, C., Ditonno, P., & Battaglia, M. (2015). Increased expression of the autocrine motility factor is associated with poor prognosis in patients with clear cell-renal cell carcinoma. Medicine, 94(46), e2117. https://doi.org/10.1097/MD.0000000000002117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Khajah, M. A., Khushaish, S., & Luqmani, Y. A. (2021). Lactate dehydrogenase A or B knockdown reduces lactate production and inhibits breast cancer cell motility in vitro. Frontiers in Pharmacology, 12, 747001. https://doi.org/10.3389/fphar.2021.747001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Parzych, K. R., & Klionsky, D. J. (2014). An overview of autophagy: Morphology, mechanism, and regulation. Antioxidants & Redox Signaling, 20(3), 460–473. https://doi.org/10.1089/ars.2013.5371.

    Article  CAS  Google Scholar 

  127. Kroemer, G., Mariño, G., & Levine, B. (2010). Autophagy and the integrated stress response. Molecular Cell, 40(2), 280–293. https://doi.org/10.1016/j.molcel.2010.09.023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Khandia, R., Dadar, M., Munjal, A., Dhama, K., Karthik, K., Tiwari, R., Yatoo, M. I., Iqbal, H. M. N., Singh, K. P., Joshi, S. K., & Chaicumpa, W. (2019). A comprehensive review of autophagy and its various roles in infectious, non-infectious, and lifestyle diseases: Current knowledge and prospects for disease prevention, novel drug design, and therapy. Cells, 8(7), 674. https://doi.org/10.3390/cells8070674.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Yun, C. W., & Lee, S. H. (2018). The roles of autophagy in cancer. International Journal of Molecular Sciences, 19(11), 3466. https://doi.org/10.3390/ijms19113466.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Srinivas, U. S., Tan, B. W. Q., Vellayappan, B. A., & Jeyasekharan, A. D. (2019). ROS and the DNA damage response in cancer. Redox Biology, 25, 101084. https://doi.org/10.1016/j.redox.2018.101084.

    Article  CAS  PubMed  Google Scholar 

  131. Zheng, J. (2012). Energy metabolism of cancer: Glycolysis versus oxidative phosphorylation (Review). Oncology Letters, 4(6), 1151–1157. https://doi.org/10.3892/ol.2012.928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Wang, X., Lu, S., He, C., Wang, C., Wang, L., Piao, M., Chi, G., Luo, Y., & Ge, P. (2019). RSL3 induced autophagic death in glioma cells via causing glycolysis dysfunction. Biochemical and Biophysical Research Communications, 518(3), 590–597. https://doi.org/10.1016/j.bbrc.2019.08.096.

    Article  CAS  PubMed  Google Scholar 

  133. Kim, J. H., Nam, B., Choi, Y. J., Kim, S. Y., Lee, J. E., Sung, K. J., Kim, W. S., Choi, C. M., Chang, E. J., Koh, J. S., Song, J. S., Yoon, S., Lee, J. C., Rho, J. K., & Son, J. (2018). Enhanced glycolysis supports cell survival in EGFR-mutant lung adenocarcinoma by inhibiting autophagy-mediated EGFR degradation. Cancer Research, 78(16), 4482–4496. https://doi.org/10.1158/0008-5472.CAN-18-0117.

    Article  CAS  PubMed  Google Scholar 

  134. Chu, Y., Chang, Y., Lu, W., Sheng, X., Wang, S., Xu, H., & Ma, J. (2020). Regulation of autophagy by glycolysis in cancer. Cancer Management and Research, 12, 13259–13271. https://doi.org/10.2147/CMAR.S279672.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Kothari, S. S., Abrahamsen, M. S., Cole, T., & Hammond, W. P. (1995). Expression of granulocyte colony stimulating factor (G-CSF) and granulocyte/macrophage colony stimulating factor (GM-CSF) mRNA upon stimulation with phorbol ester. Blood Cells, Molecules & Diseases, 21(3), 192–200. https://doi.org/10.1006/bcmd.1995.0022.

    Article  CAS  Google Scholar 

  136. Zhang, X. Y., Zhang, M., Cong, Q., Zhang, M. X., Zhang, M. Y., Lu, Y. Y., & Xu, C. J. (2018). Hexokinase 2 confers resistance to cisplatin in ovarian cancer cells by enhancing cisplatin-induced autophagy. The International Journal of Biochemistry & Cell Biology, 95, 9–16. https://doi.org/10.1016/j.biocel.2017.12.010.

    Article  CAS  Google Scholar 

  137. Tan, W. X., Xu, T. M., Zhou, Z. L., Lv, X. J., Liu, J., Zhang, W. J., & Cui, M. H. (2019). TRP14 promotes resistance to cisplatin by inducing autophagy in ovarian cancer. Oncology Reports, 42(4), 1343–1354. https://doi.org/10.3892/or.2019.7258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Pajak, B., Siwiak, E., Sołtyka, M., Priebe, A., Zieliński, R., Fokt, I., Ziemniak, M., Jaśkiewicz, A., Borowski, R., Domoradzki, T., & Priebe, W. (2019). 2-Deoxy-d-Glucose and its analogs: From diagnostic to therapeutic agents. International Journal of Molecular Sciences, 21(1), 234. https://doi.org/10.3390/ijms21010234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Brohée, L., Peulen, O., Nusgens, B., Castronovo, V., Thiry, M., Colige, A. C., & Deroanne, C. F. (2018). Propranolol sensitizes prostate cancer cells to glucose metabolism inhibition and prevents cancer progression. Scientific Reports, 8(1), 7050. https://doi.org/10.1038/s41598-018-25340-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Ye, M., Wang, S., Wan, T., Jiang, R., Qiu, Y., Pei, L., Pang, N., Huang, Y., Huang, Y., Zhang, Z., & Yang, L. (2017). Combined inhibitions of glycolysis and AKT/autophagy can overcome resistance to EGFR-targeted therapy of lung cancer. Journal of Cancer, 8(18), 3774–3784. https://doi.org/10.7150/jca.21035.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Herzig, S., & Shaw, R. J. (2018). AMPK: Guardian of metabolism and mitochondrial homeostasis. Nature Reviews Molecular Cell Biology, 19(2), 121–135. https://doi.org/10.1038/nrm.2017.95.

    Article  CAS  PubMed  Google Scholar 

  142. Chang, C., Su, H., Zhang, D., Wang, Y., Shen, Q., Liu, B., Huang, R., Zhou, T., Peng, C., Wong, C. C., Shen, H. M., Lippincott-Schwartz, J., & Liu, W. (2015). AMPK-dependent phosphorylation of GAPDH Triggers Sirt1 activation and is necessary for autophagy upon glucose starvation. Molecular Cell, 60(6), 930–940. https://doi.org/10.1016/j.molcel.2015.10.037.

    Article  CAS  PubMed  Google Scholar 

  143. Butera, G., Mullappilly, N., Masetto, F., Palmieri, M., Scupoli, M. T., Pacchiana, R., & Donadelli, M. (2019). Regulation of autophagy by nuclear GAPDH and its aggregates in cancer and neurodegenerative disorders. International Journal of Molecular Sciences, 20(9), 2062. https://doi.org/10.3390/ijms20092062.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Chambers, A., Tsang, J. S., Stanway, C., Kingsman, A. J., & Kingsman, S. M. (1989). Transcriptional control of the Saccharomyces cerevisiae PGK gene by RAP1. Molecular and Cellular Biology, 9(12), 5516–5524. https://doi.org/10.1128/mcb.9.12.5516-5524.1989.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Park, J. M., Seo, M., Jung, C. H., Grunwald, D., Stone, M., Otto, N. M., Toso, E., Ahn, Y., Kyba, M., Griffin, T. J., Higgins, L., & Kim, D. H. (2018). ULK1 phosphorylates Ser30 of BECN1 in association with ATG14 to stimulate autophagy induction. Autophagy, 14(4), 584–597. https://doi.org/10.1080/15548627.2017.1422851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Das, C. K., Parekh, A., Parida, P. K., Bhutia, S. K., & Mandal, M. (2019). Lactate dehydrogenase A regulates autophagy and tamoxifen resistance in breast cancer. Biochimica et Biophysica Acta. Molecular Cell Research, 1866(6), 1004–1018. https://doi.org/10.1016/j.bbamcr.2019.03.004.

    Article  CAS  PubMed  Google Scholar 

  147. Urbańska, K., & Orzechowski, A. (2019). Unappreciated role of LDHA and LDHB to control apoptosis and autophagy in tumor cells. International Journal Of Molecular Sciences, 20(9), 2085. https://doi.org/10.3390/ijms20092085.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Shi, L., Yan, H., An, S., Shen, M., Jia, W., Zhang, R., Zhao, L., Huang, G., & Liu, J. (2019). SIRT5-mediated deacetylation of LDHB promotes autophagy and tumorigenesis in colorectal cancer. Molecular Oncology, 13(2), 358–375. https://doi.org/10.1002/1878-0261.12408.

    Article  CAS  PubMed  Google Scholar 

  149. Kim, L. C., Cook, R. S., & Chen, J. (2017). mTORC1 and mTORC2 in cancer and the tumor microenvironment. Oncogene, 36(16), 2191–2201. https://doi.org/10.1038/onc.2016.363.

    Article  CAS  PubMed  Google Scholar 

  150. Lv, D., Guo, L., Zhang, T., & Huang, L. (2017). PRAS40 signaling in tumor. Oncotarget, 8(40), 69076–69085. https://doi.org/10.18632/oncotarget.17299.

    Article  PubMed  PubMed Central  Google Scholar 

  151. He, X., Du, S., Lei, T., Li, X., Liu, Y., Wang, H., Tong, R., & Wang, Y. (2017). PKM2 in carcinogenesis and oncotherapy. Oncotarget, 8(66), 110656–110670. https://doi.org/10.18632/oncotarget.22529.

    Article  PubMed  PubMed Central  Google Scholar 

  152. Magaway, C., Kim, E., & Jacinto, E. (2019). Targeting mTOR and metabolism in cancer: Lessons and innovations. Cells, 8(12), 1584. https://doi.org/10.3390/cells8121584.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Batlle, E., & Massagué, J. (2019). Transforming growth Factor-β signaling in immunity and cancer. Immunity, 50(4), 924–940. https://doi.org/10.1016/j.immuni.2019.03.024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Parker, T. W., & Neufeld, K. L. (2020). APC controls Wnt-induced β-catenin destruction complex recruitment in human colonocytes. Scientific Reports, 10(1), 2957. https://doi.org/10.1038/s41598-020-59899-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Vallée, A., Lecarpentier, Y., & Vallée, J. N. (2021). The key role of the WNT/β-Catenin pathway in metabolic reprogramming in cancers under normoxic conditions. Cancers, 13(21), 5557. https://doi.org/10.3390/cancers13215557.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Pate, K. T., Stringari, C., Sprowl-Tanio, S., Wang, K., TeSlaa, T., Hoverter, N. P., McQuade, M. M., Garner, C., Digman, M. A., Teitell, M. A., Edwards, R. A., Gratton, E., & Waterman, M. L. (2014). Wnt signaling directs a metabolic program of glycolysis and angiogenesis in colon cancer. The EMBO Journal, 33(13), 1454–1473. https://doi.org/10.15252/embj.201488598.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Pérez-Tomás, R., & Pérez-Guillén, I. (2020). Lactate in the tumor microenvironment: An essential molecule in cancer progression and treatment. Cancers, 12(11), 3244. https://doi.org/10.3390/cancers12113244.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Mo, Y., Wang, Y., Zhang, L., Yang, L., Zhou, M., Li, X., Li, Y., Li, G., Zeng, Z., Xiong, W., Xiong, F., & Guo, C. (2019). The role of Wnt signaling pathway in tumor metabolic reprogramming. Journal of Cancer, 10(16), 3789–3797. https://doi.org/10.7150/jca.31166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Yoo, H. C., Yu, Y. C., Sung, Y., & Han, J. M. (2020). Glutamine reliance in cell metabolism. Experimental & Molecular Medicine, 52(9), 1496–1516. https://doi.org/10.1038/s12276-020-00504-8.

    Article  CAS  Google Scholar 

  160. Li, S., Liu, F., Xu, L., Li, C., Yang, X., Guo, B., Gu, J., & Wang, L. (2020). Wnt/β-catenin signaling axis is required for TFEB-mediated gastric cancer metastasis and epithelial-mesenchymal transition. Molecular Cancer Research: MCR, 18(11), 1650–1659. https://doi.org/10.1158/1541-7786.MCR-20-0180.

    Article  CAS  PubMed  Google Scholar 

  161. Shang, S., Hua, F., & Hu, Z. W. (2017). The regulation of β-catenin activity and function in cancer: Therapeutic opportunities. Oncotarget, 8(20), 33972–33989. https://doi.org/10.18632/oncotarget.15687.

    Article  PubMed  PubMed Central  Google Scholar 

  162. Long, Y. C., & Zierath, J. R. (2006). AMP-activated protein kinase signaling in metabolic regulation. The Journal of Clinical Investigation, 116(7), 1776–1783. https://doi.org/10.1172/JCI29044.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Panieri, E., & Santoro, M. M. (2016). ROS homeostasis and metabolism: A dangerous liason in cancer cells. Cell Death & Disease, 7(6), e2253. https://doi.org/10.1038/cddis.2016.105.

    Article  CAS  Google Scholar 

  164. Gorrini, C., Harris, I. S., & Mak, T. W. (2013). Modulation of oxidative stress as an anticancer strategy. Nature Reviews Drug Discovery, 12(12), 931–947. https://doi.org/10.1038/nrd4002.

    Article  CAS  PubMed  Google Scholar 

  165. Weinberg, F., Hamanaka, R., Wheaton, W. W., Weinberg, S., Joseph, J., Lopez, M., Kalyanaraman, B., Mutlu, G. M., Budinger, G. R., & Chandel, N. S. (2010). Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proceedings of the National Academy of Sciences of the United States of America, 107(19), 8788–8793. https://doi.org/10.1073/pnas.1003428107.

    Article  PubMed  PubMed Central  Google Scholar 

  166. Zu, X. L., & Guppy, M. (2004). Cancer metabolism: Facts, fantasy, and fiction. Biochemical and Biophysical Research Communications, 313(3), 459–465. https://doi.org/10.1016/j.bbrc.2003.11.136.

    Article  CAS  PubMed  Google Scholar 

  167. Liberti, M. V., & Locasale, J. W. (2016). The Warburg effect: How does it benefit cancer cells? Trends in Biochemical Sciences, 41(3), 211–218. https://doi.org/10.1016/j.tibs.2015.12.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Patra, K. C., & Hay, N. (2014). The pentose phosphate pathway and cancer. Trends in Biochemical Sciences, 39(8), 347–354. https://doi.org/10.1016/j.tibs.2014.06.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Hardie, D. G. (2011). AMP-activated protein kinase: An energy sensor that regulates all aspects of cell function. Genes & Development, 25(18), 1895–1908. https://doi.org/10.1101/gad.17420111.

    Article  CAS  Google Scholar 

  170. Garcia, D., & Shaw, R. J. (2017). AMPK: Mechanisms of cellular energy sensing and restoration of metabolic balance. Molecular Cell, 66(6), 789–800. https://doi.org/10.1016/j.molcel.2017.05.032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Shackelford, D. B., & Shaw, R. J. (2009). The LKB1-AMPK pathway: Metabolism and growth control in tumour suppression. Nature Reviews Cancer, 9(8), 563–575. https://doi.org/10.1038/nrc2676.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Sun, S. Y. (2010). N-acetylcysteine, reactive oxygen species and beyond. Cancer Biology & Therapy, 9(2), 109–110. https://doi.org/10.4161/cbt.9.2.10583.

    Article  Google Scholar 

  173. Jeon, S. M., Chandel, N. S., & Hay, N. (2012). AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress. Nature, 485(7400), 661–665. https://doi.org/10.1038/nature11066.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Houten, S. M., & Wanders, R. J. (2010). A general introduction to the biochemistry of mitochondrial fatty acid β-oxidation. Journal of Inherited Metabolic Disease, 33(5), 469–477. https://doi.org/10.1007/s10545-010-9061-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Rabinovitch, R. C., Samborska, B., Faubert, B., Ma, E. H., Gravel, S. P., Andrzejewski, S., Raissi, T. C., Pause, A., St-Pierre, J., & Jones, R. G. (2017). AMPK Maintains cellular metabolic homeostasis through regulation of mitochondrial reactive oxygen species. Cell Reports, 21(1), 1–9. https://doi.org/10.1016/j.celrep.2017.09.026.

    Article  CAS  PubMed  Google Scholar 

  176. Marin, T. L., Gongol, B., Zhang, F., Martin, M., Johnson, D. A., Xiao, H., Wang, Y., Subramaniam, S., Chien, S., & Shyy, J. Y. (2017). AMPK promotes mitochondrial biogenesis and function by phosphorylating the epigenetic factors DNMT1, RBBP7, and HAT1. Science Signaling, 10(464), eaaf7478. https://doi.org/10.1126/scisignal.aaf7478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Zimmermann, K., Baldinger, J., Mayerhofer, B., Atanasov, A. G., Dirsch, V. M., & Heiss, E. H. (2015). Activated AMPK boosts the Nrf2/HO-1 signaling axis-A role for the unfolded protein response. Free Radical Biology & Medicine, 88(Pt B), 417–426. https://doi.org/10.1016/j.freeradbiomed.2015.03.030.

    Article  CAS  Google Scholar 

  178. Kobayashi, A., Kang, M. I., Okawa, H., Ohtsuji, M., Zenke, Y., Chiba, T., Igarashi, K., & Yamamoto, M. (2004). Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Molecular and Cellular Biology, 24(16), 7130–7139. https://doi.org/10.1128/MCB.24.16.7130-7139.2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Ma, Q. (2013). Role of nrf2 in oxidative stress and toxicity. Annual Review of Pharmacology and Toxicology, 53, 401–426. https://doi.org/10.1146/annurev-pharmtox-011112-140320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Zambrano, A., Molt, M., Uribe, E., & Salas, M. (2019). Glut 1 in cancer cells and the inhibitory action of resveratrol as a potential therapeutic strategy. International Journal of Molecular Sciences, 20(13), 3374. https://doi.org/10.3390/ijms20133374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Ancey, P. B., Contat, C., & Meylan, E. (2018). Glucose transporters in cancer - from tumor cells to the tumor microenvironment. The FEBS Journal, 285(16), 2926–2943. https://doi.org/10.1111/febs.14577.

    Article  CAS  PubMed  Google Scholar 

  182. Lee, E. E., Ma, J., Sacharidou, A., Mi, W., Salato, V. K., Nguyen, N., Jiang, Y., Pascual, J. M., North, P. E., Shaul, P. W., Mettlen, M., & Wang, R. C. (2015). A protein kinase C phosphorylation motif in GLUT1 affects glucose transport and is mutated in GLUT1 deficiency syndrome. Molecular Cell, 58(5), 845–853. https://doi.org/10.1016/j.molcel.2015.04.015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Romero-Garcia, S., Lopez-Gonzalez, J. S., Báez-Viveros, J. L., Aguilar-Cazares, D., & Prado-Garcia, H. (2011). Tumor cell metabolism: An integral view. Cancer Biology & Therapy, 12(11), 939–948. https://doi.org/10.4161/cbt.12.11.18140.

    Article  CAS  Google Scholar 

  184. Stincone, A., Prigione, A., Cramer, T., Wamelink, M. M., Campbell, K., Cheung, E., Olin-Sandoval, V., Grüning, N. M., Krüger, A., Tauqeer Alam, M., Keller, M. A., Breitenbach, M., Brindle, K. M., Rabinowitz, J. D., & Ralser, M. (2015). The return of metabolism: Biochemistry and physiology of the pentose phosphate pathway. Biological Reviews of the Cambridge Philosophical Society, 90(3), 927–963. https://doi.org/10.1111/brv.12140.

    Article  PubMed  Google Scholar 

  185. Shibuya, M. (2011). Vascular endothelial growth factor (VEGF) and its receptor (VEGFR) signaling in angiogenesis: A crucial target for anti- and pro-angiogenic therapies. Genes & Cancer, 2(12), 1097–1105. https://doi.org/10.1177/1947601911423031.

    Article  CAS  Google Scholar 

  186. Estrella, V., Chen, T., Lloyd, M., Wojtkowiak, J., Cornnell, H. H., Ibrahim-Hashim, A., Bailey, K., Balagurunathan, Y., Rothberg, J. M., Sloane, B. F., Johnson, J., Gatenby, R. A., & Gillies, R. J. (2013). Acidity generated by the tumor microenvironment drives local invasion. Cancer Research, 73(5), 1524–1535. https://doi.org/10.1158/0008-5472.CAN-12-2796.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Brooks, G. A., Dubouchaud, H., Brown, M., Sicurello, J. P., & Butz, C. E. (1999). Role of mitochondrial lactate dehydrogenase and lactate oxidation in the intracellular lactate shuttle. Proceedings of the National Academy of Sciences of the United States of America, 96(3), 1129–1134. https://doi.org/10.1073/pnas.96.3.1129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Lagarde, D., Jeanson, Y., Portais, J. C., Galinier, A., Ader, I., Casteilla, L., & Carrière, A. (2021). Lactate fluxes and plasticity of adipose tissues: A redox perspective. Frontiers in Physiology, 12, 689747. https://doi.org/10.3389/fphys.2021.689747.

    Article  PubMed  PubMed Central  Google Scholar 

  189. Xie, N., Zhang, L., Gao, W., Huang, C., Huber, P. E., Zhou, X., Li, C., Shen, G., & Zou, B. (2020). NAD+ metabolism: Pathophysiologic mechanisms and therapeutic potential. Signal Transduction and Targeted Therapy, 5(1), 227. https://doi.org/10.1038/s41392-020-00311-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Go, S., Kramer, T. T., Verhoeven, A. J., Oude Elferink, R. P. J., & Chang, J. C. (2021). The extracellular lactate-to-pyruvate ratio modulates the sensitivity to oxidative stress-induced apoptosis via the cytosolic NADH/NAD+ redox state. Apoptosis: An International Journal on Programmed Cell Death, 26(1-2), 38–51. https://doi.org/10.1007/s10495-020-01648-8.

    Article  CAS  PubMed  Google Scholar 

  191. Svedružić, Ž. M., Odorčić, I., Chang, C. H., & Svedružić, D. (2020). Substrate channeling via a transient protein-protein complex: The case of D-Glyceraldehyde-3-phosphate dehydrogenase and L-lactate dehydrogenase. Scientific Reports, 10(1), 10404. https://doi.org/10.1038/s41598-020-67079-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Vijay, N., & Morris, M. E. (2014). Role of monocarboxylate transporters in drug delivery to the brain. Current Pharmaceutical Design, 20(10), 1487–1498. https://doi.org/10.2174/13816128113199990462.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Rabinowitz, J. D., & Enerbäck, S. (2020). Lactate: The ugly duckling of energy metabolism. Nature Metabolism, 2(7), 566–571. https://doi.org/10.1038/s42255-020-0243-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Brooks, G. A. (2018). The science and translation of lactate shuttle theory. Cell Metabolism, 27(4), 757–785. https://doi.org/10.1016/j.cmet.2018.03.008.

    Article  CAS  PubMed  Google Scholar 

  195. Martínez-Reyes, I., & Chandel, N. S. (2020). Mitochondrial TCA cycle metabolites control physiology and disease. Nature Communications, 11(1), 102. https://doi.org/10.1038/s41467-019-13668-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Hashimoto, T., Hussien, R., Cho, H. S., Kaufer, D., & Brooks, G. A. (2008). Evidence for the mitochondrial lactate oxidation complex in rat neurons: Demonstration of an essential component of brain lactate shuttles. PloS One, 3(8), e2915. https://doi.org/10.1371/journal.pone.0002915.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Lin, Y., Wang, Y., & Li, P. F. (2022). Mutual regulation of lactate dehydrogenase and redox robustness. Frontiers in Physiology, 13, 1038421. https://doi.org/10.3389/fphys.2022.1038421.

    Article  PubMed  PubMed Central  Google Scholar 

  198. Li, X., Yang, Y., Zhang, B., Lin, X., Fu, X., An, Y., Zou, Y., Wang, J. X., Wang, Z., & Yu, T. (2022). Lactate metabolism in human health and disease. Signal Transduction and Targeted Therapy, 7(1), 305. https://doi.org/10.1038/s41392-022-01151-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Kane, D. A. (2014). Lactate oxidation at the mitochondria: A lactate-malate-aspartate shuttle at work. Frontiers in Neuroscience, 8, 366. https://doi.org/10.3389/fnins.2014.00366.

    Article  PubMed  PubMed Central  Google Scholar 

  200. Peters, A. L., & Van Noorden, C. J. (2009). Glucose-6-phosphate dehydrogenase deficiency and malaria: Cytochemical detection of heterozygous G6PD deficiency in women. The Journal of Histochemistry and Cytochemistry: Official Journal of the Histochemistry Society, 57(11), 1003–1011. https://doi.org/10.1369/jhc.2009.953828.

    Article  CAS  PubMed  Google Scholar 

  201. Dey, S., Sidor, A., & O’Rourke, B. (2016). Compartment-specific control of reactive oxygen species scavenging by antioxidant pathway enzymes. The Journal of Biological Chemistry, 291(21), 11185–11197. https://doi.org/10.1074/jbc.M116.726968.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Polat, I. H., Tarrado-Castellarnau, M., Bharat, R., Perarnau, J., Benito, A., Cortés, R., Sabatier, P., & Cascante, M. (2021). Oxidative pentose phosphate pathway enzyme 6-phosphogluconate dehydrogenase plays a key role in breast cancer metabolism. Biology, 10(2), 85. https://doi.org/10.3390/biology10020085.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  203. Szablewski, L. (2022). Glucose transporters as markers of diagnosis and prognosis in cancer diseases. Oncology Reviews, 16(1), 561. https://doi.org/10.4081/oncol.2022.561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  204. Stanirowski, P. J., Szukiewicz, D., Majewska, A., Wątroba, M., Pyzlak, M., Bomba-Opoń, D., & Wielgoś, M. (2022). Placental expression of glucose transporters GLUT-1, GLUT-3, GLUT-8 and GLUT-12 in pregnancies complicated by gestational and type 1 diabetes mellitus. Journal of Diabetes Investigation, 13(3), 560–570. https://doi.org/10.1111/jdi.13680.

    Article  CAS  PubMed  Google Scholar 

  205. Wu, N., Zheng, B., Shaywitz, A., Dagon, Y., Tower, C., Bellinger, G., Shen, C. H., Wen, J., Asara, J., McGraw, T. E., Kahn, B. B., & Cantley, L. C. (2013). AMPK-dependent degradation of TXNIP upon energy stress leads to enhanced glucose uptake via GLUT1. Molecular Cell, 49(6), 1167–1175. https://doi.org/10.1016/j.molcel.2013.01.035.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Dahl, E. S., & Aird, K. M. (2017). Ataxia-Telangiectasia mutated modulation of carbon metabolism in cancer. Frontiers in Oncology, 7, 291. https://doi.org/10.3389/fonc.2017.00291.

    Article  PubMed  PubMed Central  Google Scholar 

  207. Maréchal, A., & Zou, L. (2013). DNA damage sensing by the ATM and ATR kinases. Cold Spring Harbor Perspectives in Biology, 5(9), a012716. https://doi.org/10.1101/cshperspect.a012716.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  208. Xie, X., Zhang, Y., Wang, Z., Wang, S., Jiang, X., Cui, H., Zhou, T., He, Z., Feng, H., Guo, Q., Song, X., & Cao, L. (2021). ATM at the crossroads of reactive oxygen species and autophagy. International Journal of Biological Sciences, 17(12), 3080–3090. https://doi.org/10.7150/ijbs.63963.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. Kurz, E. U., Douglas, P., & Lees-Miller, S. P. (2004). Doxorubicin activates ATM-dependent phosphorylation of multiple downstream targets in part through the generation of reactive oxygen species. The Journal of Biological Chemistry, 279(51), 53272–53281. https://doi.org/10.1074/jbc.M406879200.

    Article  CAS  PubMed  Google Scholar 

  210. Park, J., Kim, J., & Mikami, T. (2021). Exercise-induced lactate release mediates mitochondrial biogenesis in the hippocampus of mice via monocarboxylate transporters. Frontiers in Physiology, 12, 736905. https://doi.org/10.3389/fphys.2021.736905.

    Article  PubMed  PubMed Central  Google Scholar 

  211. Bhatti, M. S., & Frostig, R. D. (2023). Astrocyte-neuron lactate shuttle plays a pivotal role in sensory-based neuroprotection in a rat model of permanent middle cerebral artery occlusion. Scientific Reports, 13(1), 12799. https://doi.org/10.1038/s41598-023-39574-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  212. Zorov, D. B., Juhaszova, M., & Sollott, S. J. (2014). Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiological Reviews, 94(3), 909–950. https://doi.org/10.1152/physrev.00026.2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Johri, A., & Beal, M. F. (2012). Mitochondrial dysfunction in neurodegenerative diseases. The Journal of Pharmacology and Experimental Therapeutics, 342(3), 619–630. https://doi.org/10.1124/jpet.112.192138.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. Höhn, A., Tramutola, A., & Cascella, R. (2020). Proteostasis failure in neurodegenerative diseases: Focus on oxidative stress. Oxidative Medicine and Cellular Longevity, 2020, 5497046. https://doi.org/10.1155/2020/5497046.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Tauffenberger, A., Fiumelli, H., Almustafa, S., & Magistretti, P. J. (2019). Lactate and pyruvate promote oxidative stress resistance through hormetic ROS signaling. Cell Death & Disease, 10(9), 653. https://doi.org/10.1038/s41419-019-1877-6.

    Article  CAS  Google Scholar 

  216. Zou, G. P., Wang, T., Xiao, J. X., Wang, X. Y., Jiang, L. P., Tou, F. F., Chen, Z. P., Qu, X. H., & Han, X. J. (2023). Lactate protects against oxidative stress-induced retinal degeneration by activating autophagy. Free Radical Biology & Medicine, 194, 209–219. https://doi.org/10.1016/j.freeradbiomed.2022.12.004.

    Article  CAS  Google Scholar 

  217. Schiliro, C., & Firestein, B. L. (2021). Mechanisms of metabolic reprogramming in cancer cells supporting enhanced growth and proliferation. Cells, 10(5), 1056. https://doi.org/10.3390/cells10051056.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Cho, E. S., Cha, Y. H., Kim, H. S., Kim, N. H., & Yook, J. I. (2018). The pentose phosphate pathway as a potential target for cancer therapy. Biomolecules & Therapeutics, 26(1), 29–38. https://doi.org/10.4062/biomolther.2017.179.

    Article  CAS  Google Scholar 

  219. Lubos, E., Loscalzo, J., & Handy, D. E. (2011). Glutathione peroxidase-1 in health and disease: From molecular mechanisms to therapeutic opportunities. Antioxidants & Redox Signaling, 15(7), 1957–1997. https://doi.org/10.1089/ars.2010.3586.

    Article  CAS  Google Scholar 

  220. Nita, M., & Grzybowski, A. (2016). The role of the reactive oxygen species and oxidative stress in the pathomechanism of the age-related ocular diseases and other pathologies of the anterior and posterior eye segments in adults. Oxidative Medicine and Cellular Longevity, 2016, 3164734. https://doi.org/10.1155/2016/3164734.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  221. Read, A. D., Bentley, R. E., Archer, S. L., & Dunham-Snary, K. J. (2021). Mitochondrial iron-sulfur clusters: Structure, function, and an emerging role in vascular biology. Redox Biology, 47, 102164. https://doi.org/10.1016/j.redox.2021.102164.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  222. Fukai, T., & Ushio-Fukai, M. (2011). Superoxide dismutases: Role in redox signaling, vascular function, and diseases. Antioxidants & Redox Signaling, 15(6), 1583–1606. https://doi.org/10.1089/ars.2011.3999.

    Article  CAS  Google Scholar 

  223. Ren, X., Zou, L., Zhang, X., Branco, V., Wang, J., Carvalho, C., Holmgren, A., & Lu, J. (2017). Redox signaling mediated by thioredoxin and glutathione systems in the central nervous system. Antioxidants & Redox Signaling, 27(13), 989–1010. https://doi.org/10.1089/ars.2016.6925.

    Article  CAS  Google Scholar 

  224. Schieber, M., & Chandel, N. S. (2014). ROS function in redox signaling and oxidative stress. Current Biology: CB, 24(10), R453–R462. https://doi.org/10.1016/j.cub.2014.03.034.

    Article  CAS  PubMed  Google Scholar 

  225. Zhao, Z. (2019). Iron and oxidizing species in oxidative stress and Alzheimer’s disease. Aging Medicine (Milton (N.S.W)), 2(2), 82–87. https://doi.org/10.1002/agm2.12074.

    Article  Google Scholar 

  226. Hill, J. O., Wyatt, H. R., & Peters, J. C. (2012). Energy balance and obesity. Circulation, 126(1), 126–132. https://doi.org/10.1161/CIRCULATIONAHA.111.087213.

    Article  PubMed  PubMed Central  Google Scholar 

  227. Czech, M. P. (2017). Insulin action and resistance in obesity and type 2 diabetes. Nature Medicine, 23(7), 804–814. https://doi.org/10.1038/nm.4350.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  228. Dobrzyn, P., Dobrzyn, A., Miyazaki, M., Cohen, P., Asilmaz, E., Hardie, D. G., Friedman, J. M., & Ntambi, J. M. (2004). Stearoyl-CoA desaturase 1 deficiency increases fatty acid oxidation by activating AMP-activated protein kinase in liver. Proceedings of the National Academy of Sciences of the United States of America, 101(17), 6409–6414. https://doi.org/10.1073/pnas.0401627101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  229. Larsen, P. J., Fledelius, C., Knudsen, L. B., & Tang-Christensen, M. (2001). Systemic administration of the long-acting GLP-1 derivative NN2211 induces lasting and reversible weight loss in both normal and obese rats. Diabetes, 50(11), 2530–2539. https://doi.org/10.2337/diabetes.50.11.2530.

    Article  CAS  PubMed  Google Scholar 

  230. Farr, O. M., Li, C. R., & Mantzoros, C. S. (2016). Central nervous system regulation of eating: Insights from human brain imaging. Metabolism: Clinical and Experimental, 65(5), 699–713. https://doi.org/10.1016/j.metabol.2016.02.002.

    Article  CAS  PubMed  Google Scholar 

  231. Wu, C., Kang, J. E., Peng, L. J., Li, H., Khan, S. A., Hillard, C. J., Okar, D. A., & Lange, A. J. (2005). Enhancing hepatic glycolysis reduces obesity: Differential effects on lipogenesis depend on site of glycolytic modulation. Cell Metabolism, 2(2), 131–140. https://doi.org/10.1016/j.cmet.2005.07.003.

    Article  CAS  PubMed  Google Scholar 

  232. Foretz, M., Even, P. C., & Viollet, B. (2018). AMPK activation reduces hepatic lipid content by increasing fat oxidation in vivo. International Journal of Molecular Sciences, 19(9), 2826. https://doi.org/10.3390/ijms19092826.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  233. Liangpunsakul, S., Ross, R. A., & Crabb, D. W. (2013). Activation of carbohydrate response element-binding protein by ethanol. Journal of Investigative Medicine: The Official Publication of the American Federation for Clinical Research, 61(2), 270–277. https://doi.org/10.2310/JIM.0b013e31827c2795.

    Article  CAS  PubMed  Google Scholar 

  234. Iizuka, K., Takao, K., & Yabe, D. (2020). ChREBP-mediated regulation of lipid metabolism: Involvement of the gut microbiota, liver, and adipose tissue. Frontiers in Endocrinology, 11, 587189. https://doi.org/10.3389/fendo.2020.587189.

    Article  PubMed  PubMed Central  Google Scholar 

  235. Li, Y., Xu, S., Mihaylova, M. M., Zheng, B., Hou, X., Jiang, B., Park, O., Luo, Z., Lefai, E., Shyy, J. Y., Gao, B., Wierzbicki, M., Verbeuren, T. J., Shaw, R. J., Cohen, R. A., & Zang, M. (2011). AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metabolism, 13(4), 376–388. https://doi.org/10.1016/j.cmet.2011.03.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  236. Guo, K., Tian, Q., Yang, L., & Zhou, Z. (2021). The role of glucagon in glycemic variability in type 1 diabetes: A narrative review. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy, 14, 4865–4873. https://doi.org/10.2147/DMSO.S343514.

    Article  CAS  PubMed  Google Scholar 

  237. Jiang, S., Young, J. L., Wang, K., Qian, Y., & Cai, L. (2020). Diabetic‑induced alterations in hepatic glucose and lipid metabolism: The role of type 1 and type 2 diabetes mellitus (Review). Molecular medicine reports, 22(2), 603–611. https://doi.org/10.3892/mmr.2020.11175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  238. Sharabi, K., Tavares, C. D., Rines, A. K., & Puigserver, P. (2015). Molecular pathophysiology of hepatic glucose production. Molecular Aspects of Medicine, 46, 21–33. https://doi.org/10.1016/j.mam.2015.09.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  239. Zhang, D., Wei, Y., Huang, Q., Chen, Y., Zeng, K., Yang, W., Chen, J., & Chen, J. (2022). Important hormones regulating lipid metabolism. Molecules (Basel, Switzerland), 27(20), 7052. https://doi.org/10.3390/molecules27207052.

    Article  CAS  PubMed  Google Scholar 

  240. Henly, D. C., Phillips, J. W., & Berry, M. N. (1996). Suppression of glycolysis is associated with an increase in glucose cycling in hepatocytes from diabetic rats. The Journal of Biological Chemistry, 271(19), 11268–11271. https://doi.org/10.1074/jbc.271.19.11268.

    Article  CAS  PubMed  Google Scholar 

  241. Giacco, F., & Brownlee, M. (2010). Oxidative stress and diabetic complications. Circulation Research, 107(9), 1058–1070. https://doi.org/10.1161/CIRCRESAHA.110.223545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  242. Li, Y. G., Ji, D. F., Zhong, S., Lv, Z. Q., & Lin, T. B. (2013). Cooperative anti-diabetic effects of deoxynojirimycin-polysaccharide by inhibiting glucose absorption and modulating glucose metabolism in streptozotocin-induced diabetic mice. PloS One, 8(6), e65892. https://doi.org/10.1371/journal.pone.0065892.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  243. Bence, K. K., & Birnbaum, M. J. (2021). Metabolic drivers of non-alcoholic fatty liver disease. Molecular Metabolism, 50, 101143. https://doi.org/10.1016/j.molmet.2020.101143.

    Article  CAS  PubMed  Google Scholar 

  244. Onyango, A. N. (2022). Excessive gluconeogenesis causes the hepatic insulin resistance paradox and its sequelae. Heliyon, 8(12), e12294. https://doi.org/10.1016/j.heliyon.2022.e12294.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  245. Go, Y., Jeong, J. Y., Jeoung, N. H., Jeon, J. H., Park, B. Y., Kang, H. J., Ha, C. M., Choi, Y. K., Lee, S. J., Ham, H. J., Kim, B. G., Park, K. G., Park, S. Y., Lee, C. H., Choi, C. S., Park, T. S., Lee, W. N., Harris, R. A., & Lee, I. K. (2016). Inhibition of pyruvate dehydrogenase kinase 2 protects against hepatic steatosis through modulation of tricarboxylic acid cycle anaplerosis and ketogenesis. Diabetes, 65(10), 2876–2887. https://doi.org/10.2337/db16-0223.

    Article  CAS  PubMed  Google Scholar 

  246. Ahmad, W., Ijaz, B., Shabbiri, K., Ahmed, F., & Rehman, S. (2017). Oxidative toxicity in diabetes and Alzheimer’s disease: Mechanisms behind ROS/ RNS generation. Journal of Biomedical Science, 24(1), 76. https://doi.org/10.1186/s12929-017-0379-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  247. Talwar, D., Miller, C. G., Grossmann, J., Szyrwiel, L., Schwecke, T., Demichev, V., Mikecin Drazic, A. M., Mayakonda, A., Lutsik, P., Veith, C., Milsom, M. D., Müller-Decker, K., Mülleder, M., Ralser, M., & Dick, T. P. (2023). The GAPDH redox switch safeguards reductive capacity and enables survival of stressed tumour cells. Nature Metabolism, 5(4), 660–676. https://doi.org/10.1038/s42255-023-00781-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  248. Jellinger, K. A. (2010). Basic mechanisms of neurodegeneration: A critical update. Journal of Cellular and Molecular Medicine, 14(3), 457–487. https://doi.org/10.1111/j.1582-4934.2010.01010.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  249. Bouter, C., Henniges, P., Franke, T. N., Irwin, C., Sahlmann, C. O., Sichler, M. E., Beindorff, N., Bayer, T. A., & Bouter, Y. (2019). 18F-FDG-PET detects drastic changes in brain metabolism in the Tg4-42 model of Alzheimer’s disease. Frontiers in Aging Neuroscience, 10, 425. https://doi.org/10.3389/fnagi.2018.00425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  250. Murphy, M. P., & LeVine, 3rd, H. (2010). Alzheimer’s disease and the amyloid-beta peptide. Journal of Alzheimer’s Disease: JAD, 19(1), 311–323. https://doi.org/10.3233/JAD-2010-1221.

    Article  CAS  PubMed  Google Scholar 

  251. Lau, A., Beheshti, I., Modirrousta, M., Kolesar, T. A., Goertzen, A. L., & Ko, J. H. (2021). Alzheimer’s disease-related metabolic pattern in diverse forms of neurodegenerative diseases. Diagnostics (Basel, Switzerland), 11(11), 2023. https://doi.org/10.3390/diagnostics11112023.

    Article  PubMed  PubMed Central  Google Scholar 

  252. Duffy, P. E., Rapport, M., & Graf, L. (1980). Glial fibrillary acidic protein and Alzheimer-type senile dementia. Neurology, 30(7 Pt 1), 778–782. https://doi.org/10.1212/wnl.30.7.778.

    Article  CAS  PubMed  Google Scholar 

  253. Butterfield, D. A., Favia, M., Spera, I., Campanella, A., Lanza, M., & Castegna, A. (2022). Metabolic features of brain function with relevance to clinical features of Alzheimer and Parkinson diseases. Molecules (Basel, Switzerland), 27(3), 951. https://doi.org/10.3390/molecules27030951.

    Article  CAS  PubMed  Google Scholar 

  254. Demetrius, L. A., Magistretti, P. J., & Pellerin, L. (2015). Alzheimer’s disease: The amyloid hypothesis and the Inverse Warburg effect. Frontiers in Physiology, 5, 522. https://doi.org/10.3389/fphys.2014.00522.

    Article  PubMed  PubMed Central  Google Scholar 

  255. Zhang, X., Alshakhshir, N., & Zhao, L. (2021). Glycolytic metabolism, brain resilience, and Alzheimer’s disease. Frontiers in Neuroscience, 15, 662242. https://doi.org/10.3389/fnins.2021.662242.

    Article  PubMed  PubMed Central  Google Scholar 

  256. Bell, S. M., Burgess, T., Lee, J., Blackburn, D. J., Allen, S. P., & Mortiboys, H. (2020). Peripheral glycolysis in neurodegenerative diseases. International Journal of Molecular Sciences, 21(23), 8924. https://doi.org/10.3390/ijms21238924.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  257. Kaminsky, Y. G., Reddy, V. P., Ashraf, G. M., Ahmad, A., Benberin, V. V., Kosenko, E. A., & Aliev, G. (2013). Age-related defects in erythrocyte 2,3-diphosphoglycerate metabolism in dementia. Aging and Disease, 4(5), 244–255. https://doi.org/10.14336/AD.2013.0400244.

    Article  PubMed  PubMed Central  Google Scholar 

  258. Griffin, J. W., & Bradshaw, P. C. (2017). Amino acid catabolism in Alzheimer’s disease brain: Friend or foe? Oxidative Medicine and Cellular Longevity, 2017, 5472792. https://doi.org/10.1155/2017/5472792.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  259. Cai, R., Zhang, Y., Simmering, J. E., Schultz, J. L., Li, Y., Fernandez-Carasa, I., Consiglio, A., Raya, A., Polgreen, P. M., Narayanan, N. S., Yuan, Y., Chen, Z., Su, W., Han, Y., Zhao, C., Gao, L., Ji, X., Welsh, M. J., & Liu, L. (2019). Enhancing glycolysis attenuates Parkinson’s disease progression in models and clinical databases. The Journal of Clinical Investigation, 129(10), 4539–4549. https://doi.org/10.1172/JCI129987.

    Article  PubMed  PubMed Central  Google Scholar 

  260. Mazzio, E. A., Reams, R. R., & Soliman, K. F. (2004). The role of oxidative stress, impaired glycolysis and mitochondrial respiratory redox failure in the cytotoxic effects of 6-hydroxydopamine in vitro. Brain Research, 1004(1-2), 29–44. https://doi.org/10.1016/j.brainres.2003.12.034.

    Article  CAS  PubMed  Google Scholar 

  261. Tian, Q., Tang, H. L., Tang, Y. Y., Zhang, P., Kang, X., Zou, W., & Tang, X. Q. (2022). Hydrogen sulfide attenuates the cognitive dysfunction in Parkinson’s disease rats via promoting hippocampal microglia M2 polarization by enhancement of hippocampal Warburg effect. Oxidative Medicine and Cellular Longevity, 2022, 2792348. https://doi.org/10.1155/2022/2792348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  262. Guo, C., Sun, L., Chen, X., & Zhang, D. (2013). Oxidative stress, mitochondrial damage and neurodegenerative diseases. Neural Regeneration Research, 8(21), 2003–2014. https://doi.org/10.3969/j.issn.1673-5374.2013.21.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  263. Kierans, S. J., & Taylor, C. T. (2021). Regulation of glycolysis by the hypoxia-inducible factor (HIF): Implications for cellular physiology. The Journal of Physiology, 599(1), 23–37. https://doi.org/10.1113/JP280572.

    Article  CAS  PubMed  Google Scholar 

  264. Bonora, M., Patergnani, S., Rimessi, A., De Marchi, E., Suski, J. M., Bononi, A., Giorgi, C., Marchi, S., Missiroli, S., Poletti, F., Wieckowski, M. R., & Pinton, P. (2012). ATP synthesis and storage. Purinergic Signalling, 8(3), 343–357. https://doi.org/10.1007/s11302-012-9305-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  265. Abhishek, S., Deeksha, W., Nethravathi, K. R., Davari, M. D., & Rajakumara, E. (2023). Allosteric crosstalk in modular proteins: Function fine-tuning and drug design. Computational and Structural Biotechnology Journal, 21, 5003–5015. https://doi.org/10.1016/j.csbj.2023.10.013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  266. Wei, X., Hou, Y., Long, M., Jiang, L., & Du, Y. (2022). Molecular mechanisms underlying the role of hypoxia-inducible factor-1 α in metabolic reprogramming in renal fibrosis. Frontiers in Endocrinology, 13, 927329. https://doi.org/10.3389/fendo.2022.927329.

    Article  PubMed  PubMed Central  Google Scholar 

  267. Hoxhaj, G., & Manning, B. D. (2020). The PI3K-AKT network at the interface of oncogenic signalling and cancer metabolism. Nature Reviews Cancer, 20(2), 74–88. https://doi.org/10.1038/s41568-019-0216-7.

    Article  CAS  PubMed  Google Scholar 

  268. Hu, C. J., Wang, L. Y., Chodosh, L. A., Keith, B., & Simon, M. C. (2003). Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Molecular and Cellular Biology, 23(24), 9361–9374. https://doi.org/10.1128/MCB.23.24.9361-9374.2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  269. He, W., Batty-Stuart, S., Lee, J. E., & Ohh, M. (2021). HIF-1α hydroxyprolines modulate oxygen-dependent protein stability via single VHL interface with comparable effect on ubiquitination rate. Journal of Molecular Biology, 433(22), 167244. https://doi.org/10.1016/j.jmb.2021.167244.

    Article  CAS  PubMed  Google Scholar 

  270. Strowitzki, M. J., Cummins, E. P., & Taylor, C. T. (2019). Protein hydroxylation by hypoxia-inducible factor (HIF) hydroxylases: Unique or ubiquitous? Cells, 8(5), 384. https://doi.org/10.3390/cells8050384.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  271. Lancaster, D. E., McNeill, L. A., McDonough, M. A., Aplin, R. T., Hewitson, K. S., Pugh, C. W., Ratcliffe, P. J., & Schofield, C. J. (2004). Disruption of dimerization and substrate phosphorylation inhibit factor inhibiting hypoxia-inducible factor (FIH) activity. The Biochemical Journal, 383(Pt. 3), 429–437. https://doi.org/10.1042/BJ20040735.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  272. Ziello, J. E., Jovin, I. S., & Huang, Y. (2007). Hypoxia-Inducible Factor (HIF)-1 regulatory pathway and its potential for therapeutic intervention in malignancy and ischemia. Yale Journal of Biology and Medicine, 80(2), 51–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  273. Yfantis, A., Mylonis, I., Chachami, G., Nikolaidis, M., Amoutzias, G. D., Paraskeva, E., & Simos, G. (2023). Transcriptional response to hypoxia: The role of HIF-1-associated co-regulators. Cells, 12(5), 798. https://doi.org/10.3390/cells12050798.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  274. Nagao, A., Kobayashi, M., Koyasu, S., Chow, C. C. T., & Harada, H. (2019). HIF-1-dependent reprogramming of glucose metabolic pathway of cancer cells and its therapeutic significance. International Journal of Molecular Sciences, 20(2), 238. https://doi.org/10.3390/ijms20020238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  275. Gao, S., Zhou, J., Zhao, Y., Toselli, P., & Li, W. (2013). Hypoxia-response element (HRE)-directed transcriptional regulation of the rat lysyl oxidase gene in response to cobalt and cadmium. Toxicological Sciences: An Official Journal of the Society of Toxicology, 132(2), 379–389. https://doi.org/10.1093/toxsci/kfs327.

    Article  CAS  PubMed  Google Scholar 

  276. Kim, J. W., Tchernyshyov, I., Semenza, G. L., & Dang, C. V. (2006). HIF-1-mediated expression of pyruvate dehydrogenase kinase: A metabolic switch required for cellular adaptation to hypoxia. Cell Metabolism, 3(3), 177–185. https://doi.org/10.1016/j.cmet.2006.02.002.

    Article  CAS  PubMed  Google Scholar 

  277. Cui, X. G., Han, Z. T., He, S. H., Wu, X. D., Chen, T. R., Shao, C. H., Chen, D. L., Su, N., Chen, Y. M., Wang, T., Wang, J., Song, D. W., Yan, W. J., Yang, X. H., Liu, T., Wei, H. F., & Xiao, J. (2017). HIF1/2α mediates hypoxia-induced LDHA expression in human pancreatic cancer cells. Oncotarget, 8(15), 24840–24852. https://doi.org/10.18632/oncotarget.15266.

    Article  PubMed  PubMed Central  Google Scholar 

  278. Pérez-Escuredo, J., Van Hée, V. F., Sboarina, M., Falces, J., Payen, V. L., Pellerin, L., & Sonveaux, P. (2016). Monocarboxylate transporters in the brain and in cancer. Biochimica et Biophysica Acta, 1863(10), 2481–2497. https://doi.org/10.1016/j.bbamcr.2016.03.013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  279. Zhang, H., Bosch-Marce, M., Shimoda, L. A., Tan, Y. S., Baek, J. H., Wesley, J. B., Gonzalez, F. J., & Semenza, G. L. (2008). Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. The Journal of Biological Chemistry, 283(16), 10892–10903. https://doi.org/10.1074/jbc.M800102200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  280. Hirota, K. (2021). HIF-α prolyl hydroxylase inhibitors and their implications for biomedicine: A comprehensive review. Biomedicines, 9(5), 468. https://doi.org/10.3390/biomedicines9050468.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank the Council of Scientific and Industrial Research [CSIR File no-09/028(1112)/2019-EMR-I] for funding AM’s fellowship.

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  1. Department of Biophysics, Molecular Biology and Bioinformatics, University of Calcutta, Kolkata, India

    Avirup Malla & Runa Sur

  2. Department of Aquaculture Management, Khejuri college, West Bengal, Baratala, India

    Suvroma Gupta

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Conceptualization of the project was done by S.G., R.S. and A.M. A.M. prepared the original draft, which was edited by S.G. and R.S. S.G. and R.S. are corresponding authors of this manuscript. All approve the final version of the submitted manuscript.

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Malla, A., Gupta, S. & Sur, R. Glycolytic enzymes in non-glycolytic web: functional analysis of the key players. Cell Biochem Biophys 82, 351–378 (2024). https://doi.org/10.1007/s12013-023-01213-5

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