Abstract
Olfactory mucosa is well known for its lifelong ability for regeneration. Regeneration of neurons and regrowth of severed axons are the most common neural repair mechanisms in olfactory mucosa. Nonetheless, exposure to neurotoxic contaminants, such as copper nanoparticles (CuNPs) and copper ions (Cu2+), may alter the reparative capacity of olfactory mucosa. Here, using RNA-sequencing, we investigated the molecular basis of neural repair mechanisms that were affected by CuNPs and Cu2+ in rainbow trout olfactory mucosa. The transcript profile of olfactory mucosa suggested that regeneration of neurons was inhibited by CuNPs. Exposure to CuNPs reduced the transcript abundances of pro-inflammatory proteins which are required to initiate neuroregeneration. Moreover, the transcript of genes encoding regeneration promoters, including canonical Wnt/β-catenin signaling proteins and developmental transcription factors, were downregulated in the CuNP-treated fish. The mRNA levels of genes regulating axonal regrowth, including the growth-promoting signals secreted from olfactory ensheathing cells, were mainly increased in the CuNP treatment. However, the reduced transcript abundances of a few cell adhesion molecules and neural polarity genes may restrict axonogenesis in the CuNP-exposed olfactory mucosa. In the Cu2+-treated olfactory mucosa, both neural repair strategies were initiated at the transcript level. The stimulation of repair mechanisms can lead to the recovery of Cu2+-induced olfactory dysfunction. These results indicated CuNPs and Cu2+ differentially affected the neural repair mechanism in olfactory mucosa. Exposure to CuNP had greater effects on the expression of genes involved in olfactory repair mechanisms relative to Cu2+ and dysregulated the transcripts associated with stem cell proliferation and neural reconstitution.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Adeleye AS, Oranu EA, Tao M, Keller AA (2016) Release and detection of nanosized copper from a commercial antifouling paint. Water Res 102:374–382. https://doi.org/10.1016/j.watres.2016.06.056
Aegerter S, Jalabert B, Bobe J (2005) Large scale real-time PCR analysis of mRNA abundance in rainbow trout eggs in relationship with egg quality and post-ovulatory ageing. Mol Reprod Dev 72(3):377–385. https://doi.org/10.1002/mrd.20361
Agarwal H, Nakara A, Shanmugam VK (2019) Anti-inflammatory mechanism of various metal and metal oxide nanoparticles synthesized using plant extracts: a review. Biomed Pharmacother 109:2561–2572. https://doi.org/10.1016/j.biopha.2018.11.116
Andrews S (2020) FastQC: a quality control tool for high throughput sequence data.
Arimura N, Kaibuchi K (2007) Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat Rev Neurosci 8(3):194–205. https://doi.org/10.1038/nrn2056
Ashraf PM, Sasikala K, Thomas SN, Edwin L (2017) Biofouling resistant polyethylene cage aquaculture nettings: a new approach using polyaniline and nano copper oxide. Arab J Chem 13:875–882
Astic L, Pellier-Monnin V, Saucier D, Charrier C, Mehlen P (2002) Expression of netrin-1 and netrin-1 receptor, DCC, in the rat olfactory nerve pathway during development and axonal regeneration. Neuroscience 109(4):643–656. https://doi.org/10.1016/s0306-4522(01)00535-8
Atli G, Grosell M (2016) Characterization and response of antioxidant systems in the tissues of the freshwater pond snail (Lymnaea stagnalis) during acute copper exposure. Aquat Toxicol 176:38–44. https://doi.org/10.1016/j.aquatox.2016.04.007
Bengoa-Vergniory N, Kypta RM (2015) Canonical and noncanonical Wnt signaling in neural stem/progenitor cells. Cell Mol Life Sci 72(21):4157–4172. https://doi.org/10.1007/s00018-015-2028-6
Berghard A, Hägglund AC, Bohm S, Carlsson L (2012) Lhx2-dependent specification of olfactory sensory neurons is required for successful integration of olfactory, vomeronasal, and GnRH neurons. FASEB J 26(8):3464–3472
Bettini S, Ciani F, Franceschini V (2006) Recovery of the olfactory receptor neurons in the African Tilapia mariae following exposure to low copper level. Aquat Toxicol 76(3–4):321–328. https://doi.org/10.1016/j.aquatox.2005.10.009
Bols NC, Brubacher JL, Ganassin RC, Lee LE (2001) Ecotoxicology and innate immunity in fish. Dev Comp Immunol 25(8–9):853–873. https://doi.org/10.1016/s0145-305x(01)00040-4
Brann JH, Firestein SJ (2014) A lifetime of neurogenesis in the olfactory system. Front Neurosci 8:182. https://doi.org/10.3389/fnins.2014.00182
Chang SY, Glezer I (2018) The balance between efficient anti-inflammatory treatment and neuronal regeneration in the olfactory epithelium. Neural Regen Res 13(10):1711. https://doi.org/10.4103/1673-5374.238605
Chari N, Felix L, Davoodbasha M, Ali AS, Nooruddin T (2017) In vitro and in vivo antibiofilm effect of copper nanoparticles against aquaculture pathogens. Biocatal Agric Biotechnol 10:336–341. https://doi.org/10.1016/j.bcab.2017.04.013
Chen M, Tian S, Yang X, Lane AP, Reed RR, Liu H (2014) Wnt-responsive Lgr5+ globose basal cells function as multipotent olfactory epithelium progenitor cells. J Neurosci 34(24):8268–8276. https://doi.org/10.1523/Jneurosci.0240-14.2014
Chen M, Reed RR, Lane AP (2017) Acute inflammation regulates neuroregeneration through the NF-κB pathway in olfactory epithelium. Proc Natl Acad Sci 114(30):8089–8094
Chen M, Reed RR, Lane AP (2019) Chronic inflammation directs an olfactory stem cell functional switch from neuroregeneration to immune defense. Cell Stem Cell 25(4):501–513. https://doi.org/10.1016/j.stem.2019.08.011
Chio C-P, Chen W-Y, Chou W-C, Hsieh N-H, Ling M-P, Liao C-M (2012) Assessing the potential risks to zebrafish posed by environmentally relevant copper and silver nanoparticles. Sci Total Environ 420:111–118. https://doi.org/10.1016/j.scitotenv.2012.01.023
Cho JH, Lépine M, Andrews W, Parnavelas J, Cloutier J-F (2007) Requirement for Slit-1 and Robo-2 in zonal segregation of olfactory sensory neuron axons in the main olfactory bulb. J Neurosci 27(34):9094–9104. https://doi.org/10.1523/JNEUROSCI.2217-07.2007
Choi R, Goldstein BJ (2018) Olfactory epithelium: cells, clinical disorders, and insights from an adult stem cell niche. Laryngoscope Investig Otolaryngol 3(1):35–42. https://doi.org/10.1002/lio2.135
Chuykin I, Ossipova O, Sokol SY (2018) Par3 interacts with Prickle3 to generate apical PCP complexes in the vertebrate neural plate. Elife 7:e37881. https://doi.org/10.7554/eLife.37881
Collinson JM, Quinn JC, Hill RE, West JD (2003) The roles of Pax6 in the cornea, retina, and olfactory epithelium of the developing mouse embryo. Dev Biol 255(2):303–312. https://doi.org/10.1016/s0012-1606(02)00095-7
Crisafulli U, Xavier AM, dos Santos FB et al (2018) Topical dexamethasone administration impairs protein synthesis and neuronal regeneration in the olfactory epithelium. Front Mol Neurosci 11:50. https://doi.org/10.3389/fnmol.2018.00050
Davis JA, Reed RR (1996) Role of Olf-1 and Pax-6 transcription factors in neurodevelopment. J Neurosci 16(16):5082–5094
de Rivero Vaccari JP, Dietrich WD, Keane RW (2014) Activation and regulation of cellular inflammasomes: gaps in our knowledge for central nervous system injury. J Cereb Blood Flow Metab 34(3):369–375
Dobin A, Davis CA, Schlesinger F et al (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29(1):15–21. https://doi.org/10.1093/bioinformatics/bts635
El Basuini M, El-Hais A, Dawood M et al (2017) Effects of dietary copper nanoparticles and vitamin C supplementations on growth performance, immune response and stress resistance of red sea bream Pagrus Major. Aquac Nutr 23(6):1329–1340
Fletcher RB, Das D, Gadye L et al (2017) Deconstructing olfactory stem cell trajectories at single-cell resolution. Cell stem cell 20(6):817–830. https://doi.org/10.1016/j.stem.2017.04.003
Gadye L, Das D, Sanchez MA et al (2017) Injury activates transient olfactory stem cell states with diverse lineage capacities. Cell Stem Cell 21(6):775–790. https://doi.org/10.1016/j.stem.2017.10.014
Gan Q, Lee A, Suzuki R et al (2014) Pax6 mediates ss-catenin signaling for self-renewal and neurogenesis by neocortical radial glial stem cells. Stem Cells 32(1):45–58. https://doi.org/10.1002/stem.1561
Gharagozloo M, Mahvelati TM, Imbeault E et al (2015) The nod-like receptor, Nlrp12, plays an anti-inflammatory role in experimental autoimmune encephalomyelitis. J Neuroinflammation 12(1):1–13. https://doi.org/10.1186/s12974-015-0414-5
Ghiani C, Starcevic M, Rodriguez-Fernandez I et al (2010) The dysbindin-containing complex (BLOC-1) in brain: developmental regulation, interaction with SNARE proteins and role in neurite outgrowth. Mol Psychiatry 15(2):204–215. https://doi.org/10.1038/mp.2009.58
Götz S, García-Gómez JM, Terol J et al (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36(10):3420–3435. https://doi.org/10.1093/nar/gkn176
Graziadei GM, Graziadei PPC (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy. J Neurocytol 8(2):197–213. https://doi.org/10.1007/BF01175561
Grebbin BM, Schulte D (2017) PBX1 as pioneer factor: a case still open. Front Cell and Dev Biol 5:9. https://doi.org/10.3389/fcell.2017.00009
Guo Z, Packard A, Krolewski RC, Harris MT, Manglapus GL, Schwob JE (2010) Expression of pax6 and sox2 in adult olfactory epithelium. J Comp Neurol 518(21):4395–4418. https://doi.org/10.1002/cne.22463
Halpain S, Dehmelt L (2006) The MAP1 family of microtubule-associated proteins. Genome Biol 7(6):224. https://doi.org/10.1186/gb-2006-7-6-224
Hasegawa T, Hall CJ, Crosier PS et al (2017) Transient inflammatory response mediated by interleukin-1β is required for proper regeneration in zebrafish fin fold. Elife 6:e22716
He Z, Jin Y (2016) Intrinsic control of axon regeneration. Neuron 90(3):437–451. https://doi.org/10.1016/j.neuron.2016.04.022
Hegg CC, Irwin M, Lucero MT (2009) Calcium store-mediated signaling in sustentacular cells of the mouse olfactory epithelium. Glia 57(6):634–644. https://doi.org/10.1002/glia.20792
Henion TR, Raitcheva D, Grosholz R et al (2005) β1, 3-N-acetylglucosaminyltransferase 1 glycosylation is required for axon pathfinding by olfactory sensory neurons. J Neurosci 25(8):1894–1903
Heron PM, Stromberg AJ, Breheny P, McClintock TS (2013) Molecular events in the cell types of the olfactory epithelium during adult neurogenesis. Mol Brain 6(1):49. https://doi.org/10.1186/1756-6606-6-49
Hirai S-i, Banba Y, Satake T, Ohno S (2011) Axon formation in neocortical neurons depends on stage-specific regulation of microtubule stability by the dual leucine zipper kinase–c-Jun N-Terminal Kinase pathway. J Neurosci 31(17):6468–6480. https://doi.org/10.1523/JNEUROSCI.5038-10.2011
Imura T, Wang X, Noda T, Sofroniew MV, Fushiki S (2010) Adenomatous polyposis coli is essential for both neuronal differentiation and maintenance of adult neural stem cells in subventricular zone and hippocampus. Stem Cells 28(11):2053–2064. https://doi.org/10.1002/stem.524
John JAS, Pasquale EB, Key B (2002) EphA receptors and ephrin-A ligands exhibit highly regulated spatial and temporal expression patterns in the developing olfactory system. Dev Brain Res 138(1):1–14
Kasberg AD, Brunskill EW, Potter SS (2013) SP8 regulates signaling centers during craniofacial development. Dev Biol 381(2):312–323. https://doi.org/10.1016/j.ydbio.2013.07.007
Kawasaki A, Okada M, Tamada A et al (2018) Growth cone phosphoproteomics reveals that GAP-43 phosphorylated by JNK is a marker of axon growth and regeneration. Iscience 4:190–203. https://doi.org/10.1016/j.isci.2018.05.019
Kermen F, Franco LM, Wyatt C, Yaksi E (2013) Neural circuits mediating olfactory-driven behavior in fish. Frontiers in Neural Circuits 7:62. https://doi.org/10.3389/fncir.2013.00062
Kizil C, Kyritsis N, Dudczig S et al (2012) Regenerative neurogenesis from neural progenitor cells requires injury-induced expression of Gata3. Dev Cell 23(6):1230–1237. https://doi.org/10.1016/j.devcel.2012.10.014
Kolterud Å, Alenius M, Carlsson L, Bohm S (2004) The Lim homeobox gene Lhx2 is required for olfactory sensory neuron identity. Development 131(21):5319–5326. https://doi.org/10.1242/dev.01416
Kyritsis N, Kizil C, Zocher S et al (2012) Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 338(6112):1353–1356. https://doi.org/10.1126/science.1228773
Laberge F, Hara TJ (2001) Neurobiology of fish olfaction: a review. Brain Res Rev 36(1):46–59. https://doi.org/10.1016/s0165-0173(01)00064-9
Lakhina V, Marcaccio CL, Shao X et al (2012) Netrin/DCC signaling guides olfactory sensory axons to their correct location in the olfactory bulb. J Neurosci 32(13):4440–4456. https://doi.org/10.1523/Jneurosci.4442-11.2012
Lin N, Dong XJ, Wang TY et al (2019) Characteristics of olfactory ensheathing cells and microarray analysis in Tupaia belangeri (Wagner, 1841). Mol Med Rep 20(2):1819–1825. https://doi.org/10.3892/mmr.2019.10422
Liu T, Zhang L, Joo D, Sun S-C (2017) NF-κB signaling in inflammation. Signal Transduct Target Ther 2(1):1–9
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550. https://doi.org/10.1186/s13059-014-0550-8
Ma EY, Heffern K, Cheresh J, Gallagher EP (2018) Differential copper-induced death and regeneration of olfactory sensory neuron populations and neurobehavioral function in larval zebrafish. Neurotoxicology 69:141–151. https://doi.org/10.1016/j.neuro.2018.10.002
Mahar M, Cavalli V (2018) Intrinsic mechanisms of neuronal axon regeneration. Nat Rev Neurosci 19(6):323–337. https://doi.org/10.1038/s41583-018-0001-8
Malhotra N, Ger T-R, Uapipatanakul B, Huang J-C, Chen KH-C, Hsiao C-D (2020) Review of copper and copper nanoparticle toxicity in Fish. Nanomaterials 10(6):1126. https://doi.org/10.3390/nano10061126
McCormick LE, Gupton SL (2020) Mechanistic advances in axon pathfinding. Curr Opin Cell Biol 63:11–19. https://doi.org/10.1016/j.ceb.2019.12.003
McIntyre JC, Titlow WB, McClintock TS (2010) Axon growth and guidance genes identify nascent, immature, and mature olfactory sensory neurons. J Neurosci Res 88(15):3243–3256. https://doi.org/10.1002/jnr.22497
Miyasaka N, Sato Y, Yeo S-Y et al (2005) Robo2 is required for establishment of a precise glomerular map in the zebrafish olfactory system. Development 132(6):1283–1293. https://doi.org/10.1242/dev.01698
Montenegro-Venegas C, Tortosa E, Rosso S et al (2010) MAP1B regulates axonal development by modulating Rho-GTPase Rac1 activity. Mol Biol Cell 21(20):3518–3528. https://doi.org/10.1091/mbc.E09-08-0709
Moore FB (1823) Baleja JD (2012) Molecular remodeling mechanisms of the neural somatodendritic compartment. Biochim et Biophys Acta Mol Cell Res 10:1720–1730. https://doi.org/10.1016/j.bbamcr.2012.06.006
Nicolay DJ, Doucette JR, Nazarali AJ (2006) Transcriptional regulation of neurogenesis in the olfactory epithelium. Cell Mol Neurobiol 26(4–6):801–819. https://doi.org/10.1007/s10571-006-9058-4
Pasparakis M (2009) Regulation of tissue homeostasis by NF-κB signalling: implications for inflammatory diseases. Nat Rev Immunol 9(11):778–788. https://doi.org/10.1038/nri2655
Pavlos NJ, Grønborg M, Riedel D et al (2010) Quantitative analysis of synaptic vesicle Rabs uncovers distinct yet overlapping roles for Rab3a and Rab27b in Ca2+-triggered exocytosis. J Neurosci 30(40):13441–13453. https://doi.org/10.1523/JNEUROSCI.0907-10.2010
Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33(3):290–295. https://doi.org/10.1038/nbt.3122
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29(9):e45–e45. https://doi.org/10.1093/nar/29.9.e45
Pirrone C, Chiaravalli AM, Marando A et al (2017) OTX1 and OTX2 as possible molecular markers of sinonasal carcinomas and olfactory neuroblastomas. Eur J Histochem EJH. https://doi.org/10.4081/ejh.2017.2730
Polakof S, Médale F, Skiba-Cassy S, Corraze G, Panserat S (2010) Molecular regulation of lipid metabolism in liver and muscle of rainbow trout subjected to acute and chronic insulin treatments. Domest Anim Endocrinol 39(1):26–33. https://doi.org/10.1016/j.domaniend.2010.01.003
Pu Y, Liu H, Xu H et al (2018) IL-1β promotes the migration of olfactory epithelium neural stem cells through activating matrix metalloproteinase expressions. Pathol Res Pract 214(8):1210–1217
R Core Team (2019) A language and environment for statistical computing. In: Team RC (ed) R foundation for statistical computing. R Core Team, Vienna
Rao AN, Patil A, Black MM et al (2017) Cytoplasmic dynein transports axonal microtubules in a polarity-sorting manner. Cell Rep 19(11):2210–2219. https://doi.org/10.1016/j.celrep.2017.05.064
Razmara P, Pyle GG (2022) Recovery of rainbow trout olfactory function following exposure to copper nanoparticles and copper ions. Aquat Toxicol 245:106109. https://doi.org/10.1016/j.aquatox.2022.106109
Razmara P, Lari E, Mohaddes E, Zhang Y, Goss GG, Pyle GG (2019) The effect of copper nanoparticles on olfaction in rainbow trout (Oncorhynchus mykiss). Environ Sci Nano 6(7):2094–2104. https://doi.org/10.1039/c9en00360f
Razmara P, Imbery JJ, Koide E et al (2021) Mechanism of copper nanoparticle toxicity in rainbow trout olfactory mucosa. Environ Pollut 284:117141. https://doi.org/10.1016/j.envpol.2021.117141
Rigby MJ, Gomez TM, Puglielli L (2020) Glial cell-axonal growth cone interactions in neurodevelopment and regeneration. Front Neurosci 14:203. https://doi.org/10.3389/fnins.2020.00203
Roet KC, Verhaagen J (2014) Understanding the neural repair-promoting properties of olfactory ensheathing cells. Exp Neurol 261:594–609. https://doi.org/10.1016/j.expneurol.2014.05.007
Roet KC, Franssen EH, de Bree FM et al (2013) A multilevel screening strategy defines a molecular fingerprint of proregenerative olfactory ensheathing cells and identifies SCARB2, a protein that improves regenerative sprouting of injured sensory spinal axons. J Neurosci 33(27):11116–11135. https://doi.org/10.1523/Jneurosci.1002-13.2013
Rossner P, Vrbova K, Rossnerova A et al (2020) Gene expression and epigenetic changes in mice following inhalation of copper (II) oxide nanoparticles. Nanomaterials 10(3):550. https://doi.org/10.3390/nano10030550
Roy D, Ghosh D, Mandal DK (2013) Cadmium induced histopathology in the olfactory epithelium of a snakehead fish, Channa punctatus (Bloch). Inter J Aquat Biol 1(5):221–227
Sharma D, Malik A, Guy C, Vogel P, Kanneganti T-D (2019) TNF/TNFR axis promotes pyrin inflammasome activation and distinctly modulates pyrin inflammasomopathy. J Clin Investig 129(1):150–162. https://doi.org/10.1172/JCI121372
Shetty RS, Bose SC, Nickell MD et al (2005) Transcriptional changes during neuronal death and replacement in the olfactory epithelium. Mol Cell Neurosci 30(1):90–107
Shimizu N, Kawakami K, Ishitani T (2012) Visualization and exploration of Tcf/Lef function using a highly responsive Wnt/β-catenin signaling-reporter transgenic zebrafish. Dev Biol 370(1):71–85
Sokpor G, Abbas E, Rosenbusch J, Staiger JF, Tuoc T (2018) Transcriptional and epigenetic control of mammalian olfactory epithelium development. Mol Neurobiol 55(11):8306–8327. https://doi.org/10.1007/s12035-018-0987-y
Stone MC, Nguyen MM, Tao J, Allender DL, Rolls MM (2010) Global up-regulation of microtubule dynamics and polarity reversal during regeneration of an axon from a dendrite. Mol Biol Cell 21(5):767–777. https://doi.org/10.1091/mbc.E09-11-0967
Su Z, He C (2010) Olfactory ensheathing cells: biology in neural development and regeneration. Prog Neurobiol 92(4):517–532. https://doi.org/10.1016/j.pneurobio.2010.08.008
Sun S-C (2011) Non-canonical NF-κB signaling pathway. Cell Res 21(1):71–85. https://doi.org/10.1038/cr.2010.177
Sun S-C (2017) The non-canonical NF-κB pathway in immunity and inflammation. Nat Rev Immunol 17(9):545. https://doi.org/10.1038/nri.2017.52
Suzuki J, Sakurai K, Yamazaki M et al (2015) Horizontal basal cell-specific deletion of Pax6 impedes recovery of the olfactory neuroepithelium following severe injury. Stem Cells Dev 24(16):1923–1933. https://doi.org/10.1089/scd.2015.0011
Szymkowicz DB, Sims KC, Schwendinger KL et al (2019) Exposure to arsenic during embryogenesis impairs olfactory sensory neuron differentiation and function into adulthood. Toxicology 420:73–84. https://doi.org/10.1016/j.tox.2019.04.005
Tabesh E, Salimijazi H, Kharaziha M, Hejazi M (2018) Antibacterial chitosan-copper nanocomposite coatings for biomedical applications. Mater Today Proc 5(7):15806–15812. https://doi.org/10.1016/j.matpr.2018.05.078
Takei Y, Teng J, Harada A, Hirokawa N (2000) Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes. J Cell Biol 150(5):989–1000. https://doi.org/10.1083/jcb.150.5.989
Thiruvengadam M, Chung I-M, Gomathi T et al (2019) Synthesis, characterization and pharmacological potential of green synthesized copper nanoparticles. Bioprocess Biosyst Eng 42(11):1769–1777. https://doi.org/10.1007/s00449-019-02173-y
Tilton F, Tilton SC, Bammler TK et al (2008) Transcriptional biomarkers and mechanisms of copper-induced olfactory injury in zebrafish. Environ Sci Technol 42(24):9404–9411. https://doi.org/10.1021/es801636v
Tsarouchas TM, Wehner D, Cavone L et al (2018) Dynamic control of proinflammatory cytokines Il-1β and Tnf-α by macrophages in zebrafish spinal cord regeneration. Nat Commun 9(1):1–17. https://doi.org/10.1038/s41467-018-07036-w
Tuncer S, Fiorillo MT, Sorrentino R (2014) The multifaceted nature of NLRP12. J Leukoc Biol 96(6):991–1000. https://doi.org/10.1189/jlb.3RU0514-265RR
Valiño-Rivas L, Gonzalez-Lafuente L, Sanz AB, Ruiz-Ortega M, Ortiz A, Sanchez-Niño MD (2016) Non-canonical NFκB activation promotes chemokine expression in podocytes. Sci Rep 6:28857. https://doi.org/10.1038/srep28857
Vanti GL, Masaphy S, Kurjogi M, Chakrasali S, Nargund VB (2020) Synthesis and application of chitosan-copper nanoparticles on damping off causing plant pathogenic fungi. Int J Biol Macromol 156:1387–1395. https://doi.org/10.1016/j.ijbiomac.2019.11.179
Waclaw RR, Allen ZJ II, Bell SM et al (2006) The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron 49(4):503–516. https://doi.org/10.1016/j.neuron.2006.01.018
Wang Y-Z, Yamagami T, Gan Q et al (2011) Canonical Wnt signaling promotes the proliferation and neurogenesis of peripheral olfactory stem cells during postnatal development and adult regeneration. J Cell Sci 124(9):1553–1563. https://doi.org/10.1242/jcs.080580
Wang L, Bammler TK, Beyer RP, Gallagher EP (2013) Copper-induced deregulation of microRNA expression in the zebrafish olfactory system. Environ Sci Technol 47(13):7466–7474. https://doi.org/10.1021/es400615q
Wang H, Engstrom AK, Xia Z (2017a) Cadmium impairs the survival and proliferation of cultured adult subventricular neural stem cells through activation of the JNK and p38 MAP kinases. Toxicology 380:30–37. https://doi.org/10.1016/j.tox.2017.01.013
Wang Y, Yang Q-W, Yang Q et al (2017b) Cuprous oxide nanoparticles inhibit prostate cancer by attenuating the stemness of cancer cells via inhibition of the Wnt signaling pathway. Int J Nanomed 12:2569. https://doi.org/10.2147/IJN.S130537
Winter CG, Wang B, Ballew A et al (2001) Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105(1):81–91. https://doi.org/10.1016/s0092-8674(01)00298-7
Xu J, Zhang Q, Li X, Zhan S, Wang L, Chen D (2017) The effects of copper oxide nanoparticles on dorsoventral patterning, convergent extension, and neural and cardiac development of zebrafish. Aquat Toxicol 188:130–137. https://doi.org/10.1016/j.aquatox.2017.05.002
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13(1):134. https://doi.org/10.1186/1471-2105-13-134
Zhang H, Macara IG (2006) The polarity protein PAR-3 and TIAM1 cooperate in dendritic spine morphogenesis. Nat Cell Biol 8(3):227–237. https://doi.org/10.1038/ncb1368
Zhang Y, Liu J, Yao S et al (2012) Nuclear factor kappa B signaling initiates early differentiation of neural stem cells. Stem Cells 30(3):510–524. https://doi.org/10.1002/stem.1006
Zhou Y, Wu S, Liu F (2019) High-performance polyimide nanocomposites with polydopamine-coated copper nanoparticles and nanowires for electronic applications. Mater Lett 237:19–21. https://doi.org/10.1016/j.matlet.2018.11.067
Zou Y (2020) Breaking symmetry–cell polarity signaling pathways in growth cone guidance and synapse formation. Curr Opin Neurobiol 63:77–86. https://doi.org/10.1016/j.conb.2020.03.010
Zou Y (2012) Does planar cell polarity signaling steer growth cones. Curr top Dev Biol 101:141–160
Acknowledgements
The authors would like to thank the University of Lethbridge Aquatic Research facility staff Dr. Shamsuddin Mamun and Holly Shepherd for taking care of study fish.
Funding
The current study was supported by an NSERC Discovery Grant (# RGPIN-2015–04492) and a Campus Alberta Innovation Program (CAIP) research chair to GGP.
Author information
Authors and Affiliations
Contributions
Both authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by PR. The first draft of the manuscript was written by PR, and both authors commented on previous versions of the manuscript. Both authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interests
The authors have no relevant financial or non-financial interests to disclose.
Rights and permissions
About this article
Cite this article
Razmara, P., Pyle, G.G. Impact of Copper Nanoparticles and Copper Ions on Transcripts Involved in Neural Repair Mechanisms in Rainbow Trout Olfactory Mucosa. Arch Environ Contam Toxicol 84, 18–31 (2023). https://doi.org/10.1007/s00244-022-00969-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-022-00969-w