Skip to main content

Advertisement

Springer Nature Link
Log in

Regulation of cardiac long-chain fatty acid and glucose uptake by translocation of substrate transporters

  • Invited Review
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Cardiac uptake of long-chain fatty acids (FA) is mediated predominantly by two membrane-associated proteins, the 43-kDa plasma membrane fatty acid-binding protein (FABPpm) and the 88-kDa fatty acid translocase/CD36 (FAT/CD36). While FABPpm is present constitutively in the sarcolemma, FAT/CD36 is recycled between an intracellular membrane compartment and the sarcolemma. Since the amount of sarcolemmal FAT/CD36 is a major determinant of cellular FA uptake, understanding of the regulation of its recycling is likely to provide new insights into altering substrate preference of the heart. FAT/CD36 recycling displays a remarkable similarity with that of the two glucose transporters (GLUT) in the heart, GLUT1 and GLUT4. Translocation of all three transporters is induced by insulin and by contraction, which stimuli activate distinct signalling cascades. The insulin pathway involves phosphatidylinositol-3 kinase (PI3K) whilst the contraction pathway is dependent on AMP-activated protein kinase (AMPK). For the identification of additional protein components involved in the regulation of FAT/CD36 recycling, valuable lessons can be learned from GLUT1 and GLUT4 recycling. Especially GLUT4 recycling is an intensively studied process in which a number of signalling proteins, both upstream and downstream from PI3 K and AMPK, have been identified, as well as proteins that are part of the translocation machinery involving Rab GTPases and soluble N-ethylmaleimide attachment protein receptors (SNAREs). Comparison of the magnitude of the effects of insulin and contraction on substrate uptake and on transporter appearance in the sarcolemma have revealed that FAT/CD36 recycling resembles GLUT1 recycling more closely than that of GLUT4. This pinpoints the recycling compartment and excludes a pre-endosomal storage compartment as the intracellular storage site for FAT/CD36. Further research will probably establish whether FAT/CD36 translocation is (partly) coupled to that of one or both GLUTs or, alternatively, whether it is a distinct process that also can be induced independently of GLUT1 or GLUT4 movement. In the latter case, a unique set of proteins would be dedicated to FAT/CD36 recycling, which would then provide an attractive target for manipulating cardiac substrate preference.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AICAR :

5-aminoimidazole-4-carboxyamide-1-β-d-ribofuranoside, cell-permeable activator of AMPK

AMPK :

AMP-activated protein kinase

amrinone :

specific inhibitor of phosphodiesterase III

CPT-I :

carnitine palmitoyl transferase I

dibutyryl cyclic AMP :

cell-permeable analogue of cyclic AMP, mimics cyclic AMP-activated signalling

DNP :

2,4-dinitrophenol, mitochondrial uncoupling agent

ERK :

extracellular signal-regulated kinase

etomoxir :

specific inhibitor of CPT-I

FA :

long-chain fatty acid(s)

FABPpm :

plasma membrane fatty acid-binding protein

FAT/CD36 :

fatty acid translocase/CD36

GTPγS :

guanosine 5′-O-(3-thiotriphosphate), non-hydrolysable GTP analogue, locks Rab proteins in a persistently active state

IGF-II :

insulin-like growth factor II

5-iodotubercidin :

specific inhibitor of adenosine kinase, prevents conversion of AICAR into ZMP

IRAP :

insulin-responsive aminopeptidase

IRS :

insulin receptor substrate

isoproterenol :

potent β-agonist

myristoylated PKCζ pseudosubstrate :

cell-permeable, specific inhibitor of atypical PKCs

oligomycin :

potent inhibitor of mitochondrial F1F0-ATPase

PD98059 :

specific inhibitor of mitogen-activated protein kinase signalling

PI3K :

phosphatidylinositol-3 kinase

PKB (PKB/Akt):

protein kinase B

PKC :

protein kinase C

rotenone :

inhibitor of electron transfer in mitochondria

SCAMP :

secretory carrier membrane protein

SNAP23 :

synaptosomal-associated protein (23 kDa)

SNARE :

soluble N-ethylmaleimide attachment protein receptor

SSO :

sulpho-N-succinimidyloleate, specific inhibitor of transport function of FAT/CD36

VAMP2 (-3):

vesicle-associated membrane protein-2 (-3)

VAP33 :

vesicle-associated protein 33

wortmannin :

inhibitor of PI3K

ZMP :

5′-monophosphate of AICAR

References

  1. Abumrad NA, el-Maghrabi MR, Amri EZ, Lopez E, Grimaldi PA (1993) Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J Biol Chem 268:17665–17668

    CAS  PubMed  Google Scholar 

  2. Aledo JC, Lavoie L, Volchuk A, Keller SR, Klip A, Hundal HS (1997) Identification and characterization of two distinct intracellular GLUT4 pools in rat skeletal muscle: evidence for an endosomal and an insulin-sensitive GLUT4 compartment. Biochem J 325:727–732

    CAS  PubMed  Google Scholar 

  3. Baldini G, Hohman R, Charron MJ, Lodish HF (1991) Insulin and nonhydrolyzable GTP analogs induce translocation of GLUT 4 to the plasma membrane in alpha-toxin-permeabilized rat adipose cells. J Biol Chem 266:4037–4040

    CAS  PubMed  Google Scholar 

  4. Becker C, Sevilla L, Tomas E, Palacin M, Zorzano A, Fischer Y (2001) The endosomal compartment is an insulin-sensitive recruitment site for GLUT4 and GLUT1 glucose transporters in cardiac myocytes. Endocrinology 142:5267–5276

    CAS  PubMed  Google Scholar 

  5. Bergemann C, Loken C, Becker C, Graf B, Hamidizadeh M, Fischer Y (2001) Inhibition of glucose transport by cyclic GMP in cardiomyocytes. Life Sci 69:1391–1406

    Article  CAS  PubMed  Google Scholar 

  6. Bonen A, Luiken JJFP, Arumugam Y, Glatz JFC, Tandon NN (2000) Acute regulation of fatty acid uptake involves the cellular redistribution of fatty acid translocase. J Biol Chem 275:14501–14508

    Article  CAS  PubMed  Google Scholar 

  7. Bonen A, Luiken JJ, Glatz JFC (2002) Regulation of fatty acid transport and membrane transporters in health and disease. Mol Cell Biochem 239:181–192

    Article  CAS  PubMed  Google Scholar 

  8. Brooks CC, Scherer PE, Cleveland K, Whittemore JL, Lodish HF, Cheatham B (2000) Pantophysin is a phosphoprotein component of adipocyte transport vesicles and associates with GLUT4-containing vesicles. J Biol Chem 275:2029–2036

    Article  CAS  PubMed  Google Scholar 

  9. Bryant NJ, Govers R, James DE (2002) Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol 3:267–277

    Article  CAS  PubMed  Google Scholar 

  10. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70:715–728

    CAS  PubMed  Google Scholar 

  11. Calera MR, Martinez C, Liu H, Jack AK, Birnbaum MJ, Pilch PF (1998) Insulin increases the association of Akt-2 with Glut4-containing vesicles. J Biol Chem 273:7201–7204

    Article  CAS  PubMed  Google Scholar 

  12. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M (1990) Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62:317–329

    Google Scholar 

  13. Cheatham B (2000) GLUT4 and company: SNAREing roles in insulin-regulated glucose uptake. Trends Endocrinol Metab 11:356–361

    Article  CAS  PubMed  Google Scholar 

  14. Chen HC, Bandyopadhyay G, Sajan MP, Kanoh Y, Standaert M, Farese RV Jr, Farese RV (2002) Activation of the ERK pathway and atypical protein kinase C isoforms in exercise- and aminoimidazole-4-carboxamide-1-beta-d-riboside (AICAR)-stimulated glucose transport. J Biol Chem 277:23554–23562

    Article  CAS  PubMed  Google Scholar 

  15. Coderre L, Kandror KV, Vallega G, Pilch PF (1995) Identification and characterization of an exercise-sensitive pool of glucose transporters in skeletal muscle. J Biol Chem 270:27584–27588

    Article  CAS  PubMed  Google Scholar 

  16. Coe NR, Smith AJ, Frohnert BI, Watkins PA, Bernlohr DA (1999) The fatty acid transport protein (FATP1) is a very long chain acyl-CoA synthetase. J Biol Chem 274:36300–36304

    Article  CAS  PubMed  Google Scholar 

  17. Coort SLM, Willems J, Coumans WA, van der Vusse GJ, Bonen A, Glatz JFC, Luiken JJFP (????) Sulfo-N-succinimidyl esters of long chain fatty acids specifically inhibit fatty acid translocase (FAT/CD36)-mediated cellular fatty acid uptake. Mol Cell Biochem 239:213–219

    Google Scholar 

  18. Cormont M, Tanti JF, Zahraoui A, Van Obberghen E, Tavitian A, Le Marchand-Brustel Y (1993) Insulin and okadaic acid induce Rab4 redistribution in adipocytes. J Biol Chem 268:19491–19497

    CAS  PubMed  Google Scholar 

  19. Derave W, Ai H, Ihlemann J, Witters LA, Kristiansen S, Richter EA, Ploug T (2000) Dissociation of AMP-activated protein kinase activation and glucose transport in contracting slow-twitch muscle. Diabetes 49:1281–1287

    Google Scholar 

  20. Donthi RV, Huisamen B, Lochner A (2000) Effect of vanadate and insulin on glucose transport in isolated adult rat cardiomyocytes. Cardiovasc Drugs Ther 14:463–470

    Google Scholar 

  21. Dransfeld O, Uphues I, Sasson S, Schurmann A, Joost HG, Eckel J (2000) Regulation of subcellular distribution of GLUT4 in cardiomyocytes: Rab4A reduces basal glucose transport and augments insulin responsiveness. Exp Clin Endocrinol Diabetes 108:26–36

    Google Scholar 

  22. Dyck DJ, Steinberg G, Bonen A (????) Insulin increases FA uptake and esterification but reduces lipid utilization in isolated contracting muscle. Am J Physiol 281:E600–E607

    Google Scholar 

  23. Egert S, Nguyen N, Schwaiger M (1999) Myocardial glucose transporter GLUT1: translocation induced by insulin and ischemia. J Mol Cell Cardiol 31:1337–1344

    Article  CAS  PubMed  Google Scholar 

  24. Elsing C, Kassner A, Gajdzik L, Graf J, Stremmel W (1998) Electrogenicity of hepatocellular fatty acid uptake. Eur J Med Res 3:393–396

    CAS  PubMed  Google Scholar 

  25. Farese RV (2002) Function and dysfunction of aPKC isoforms for glucose transport in insulin-sensitive and insulin-resistant states. Am J Physiol 283:E1–E11

    CAS  Google Scholar 

  26. Feron O, Zhao YY, Kelly RA (1999) The ins and outs of caveolar signaling. m2 muscarinic cholinergic receptors and eNOS activation versus neuregulin and ErbB4 signaling in cardiac myocytes. Ann NY Acad Sci 874:11–19

    CAS  PubMed  Google Scholar 

  27. Fischer Y, Rose H, Kammermeier H (1991) Highly insulin-responsive isolated rat heart muscle cells yielded by a modified isolation method. Life Sci 49:1679–1688

    Article  CAS  PubMed  Google Scholar 

  28. Fischer Y, Kamp J, Thomas J, Popping S, Rose H, Carpene C, Kammermeier H (1996) Signals mediating stimulation of cardiomyocyte glucose transport by the alpha-adrenergic agonist phenylephrine. Am J Physiol 270:C1211–C1220

    CAS  PubMed  Google Scholar 

  29. Fischer Y, Thomas J, Sevilla L, Munoz P, Becker C, Holman G, Kozka IJ, Palacin M, Testar X, Kammermeier H, Zorzano A (1997) Insulin-induced recruitment of glucose transporter 4 (GLUT4) and GLUT1 in isolated rat cardiac myocytes. Evidence of the existence of different intracellular GLUT4 vesicle populations. J Biol Chem 272:7085–7092

    Article  CAS  PubMed  Google Scholar 

  30. Foster LJ, Weir ML, Lim DY, Liu Z, Trimble WS, Klip A (2000) A functional role for VAP-33 in insulin-stimulated GLUT4 traffic. Traffic 1:512–521

    Article  CAS  PubMed  Google Scholar 

  31. Fryer LG, Hajduch E, Rencurel F, Salt IP, Hundal HS, Hardie DG, Carling D (2000) Activation of glucose transport by AMP-activated protein kinase via stimulation of nitric oxide synthase. Diabetes 49:1978–1985

    Google Scholar 

  32. Gao J, Ren J, Gulve EA, Holloszy JO (1994) Additive effect of contractions and insulin on GLUT-4 translocation into the sarcolemma. J Appl Physiol 77:1597–1601

    Google Scholar 

  33. Gervois P, Torra IP, Fruchart JC, Staels B (2000) Regulation of lipid and lipoprotein metabolism by PPAR activators. Clin Chem Lab Med 38:3–11

    CAS  PubMed  Google Scholar 

  34. Gimeno RE, Ortegon AM, Patel S, Punreddy S, Ge P, Sun Y, Lodish HF, Stahl A (2003) Characterization of a heart-specific fatty acid transport protein. J Biol Chem 278:16039–16044

    Article  CAS  PubMed  Google Scholar 

  35. Glatz JF, van der Vusse GJ (1989) Intracellular transport of lipids. Mol Cell Biochem 88:37–44

    CAS  PubMed  Google Scholar 

  36. Glatz JF, Luiken JJ, Bonen A (2001) Involvement of membrane-associated proteins in the acute regulation of cellular fatty acid uptake. J Mol Neurosci 16:123–132

    CAS  PubMed  Google Scholar 

  37. Groen AK, Wanders RJ, Westerhoff HV, van der Meer R, Tager JM (1982) Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem 257:2754–2757

    CAS  PubMed  Google Scholar 

  38. Hamilton JA (1998) Fatty acid transport: difficult or easy? J Lipid Res 39:467–481

    CAS  PubMed  Google Scholar 

  39. Hamilton JA, Kamp F (1999) How are free fatty acids transported in membranes? Is it by proteins or by free diffusion through the lipids? Diabetes 48:2255–2269

    Google Scholar 

  40. Hardie DG, Carling D (1997) The AMP-activated protein kinase--fuel gauge of the mammalian cell? Eur J Biochem 246:259–273

    CAS  PubMed  Google Scholar 

  41. Hayashi T, Wojtaszewski JF, Goodyear LJ (1997) Exercise regulation of glucose transport in skeletal muscle. Am J Physiol 273:E1039–E1051

    CAS  Google Scholar 

  42. Hayashi T, Hirshman MF, Kurth EJ, Winder WW, Goodyear LJ (1998) Evidence for 5’ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 47:1369–1373

    Google Scholar 

  43. Heller-Harrison RA, Morin M, Guilherme A, Czech MP (1996) Insulin-mediated targeting of phosphatidylinositol 3-kinase to GLUT4-containing vesicles. J Biol Chem 271:10200–10204

    Article  CAS  PubMed  Google Scholar 

  44. Holman GD, Lo Leggio L, Cushman SW (1994) Insulin-stimulated GLUT4 glucose transporter recycling. A problem in membrane protein subcellular trafficking through multiple pools. J Biol Chem 269:17516–17524

    CAS  PubMed  Google Scholar 

  45. Huang J, Imamura T, Olefsky JM (2001) Insulin can regulate GLUT4 internalization by signaling to Rab5 and the motor protein dynein. Proc Natl Acad Sci USA 98:13084–13089

    Article  CAS  PubMed  Google Scholar 

  46. Hyde R, Peyrollier K, Hundal HS (2002) Insulin promotes the cell surface recruitment of the SAT2/ATA2 system A amino acid transporter from an endosomal compartment in skeletal muscle cells. J Biol Chem 277:13628–13634

    Article  PubMed  Google Scholar 

  47. Ibrahimi A, Sfeir Z, Magharaie H, Amri EZ, Grimaldi P, Abumrad NA (1996) Expression of the CD36 homolog (FAT) in fibroblast cells: effects on fatty acid transport. Proc Natl Acad Sci USA 93:2646–2651

    Article  CAS  PubMed  Google Scholar 

  48. Isola LM, Zhou SL, Kiang CL, Stump DD, Bradbury MW, Berk PD (1995) 3T3 fibroblasts transfected with a cDNA for mitochondrial aspartate aminotransferase express plasma membrane fatty acid-binding protein and saturable fatty acid uptake. Proc Natl Acad Sci USA 92:9866–9870

    CAS  PubMed  Google Scholar 

  49. Jiang H, Li J, Katz EB, Charron MJ (2001) GLUT4 ablation in mice results in redistribution of IRAP to the plasma membrane. Biochem Biophys Res Commun 284:519–525

    Article  CAS  PubMed  Google Scholar 

  50. Johannsson E, Nagelhus EA, McCullagh KJ, Sejersted OM, Blackstad TW, Bonen A, Ottersen OP (1997) Cellular and subcellular expression of the monocarboxylate transporter MCT1 in rat heart. A high-resolution immunogold analysis. Circ Res 80:400–407

    CAS  PubMed  Google Scholar 

  51. Joost HG, Bell GI, Best JD, Birnbaum MJ, Charron MJ, Chen YT, Doege H, James DE, Lodish HF, Moley KH, Moley JF, Mueckler M, Rogers S, Schurmann A, Seino S, Thorens B (2002) Nomenclature of the GLUT/SLC2A family of sugar/polyol transport facilitators. Am J Physiol 282:E974–E976

    CAS  Google Scholar 

  52. Kagaya Y, Kanno Y, Takeyama D, Ishide N, Maruyama Y, Takahashi T, Ido T, Takishima T (1990) Effects of long-term pressure overload on regional myocardial glucose and free fatty acid uptake in rats. A quantitative autoradiographic study. Circulation 81:1353–1361

    CAS  PubMed  Google Scholar 

  53. Kandror KV, Pilch PF (1994) gp160, a tissue-specific marker for insulin-activated glucose transport. Proc Natl Acad Sci USA 91:8017–8021

    CAS  PubMed  Google Scholar 

  54. Kandror KV, Pilch PF (1996) Compartmentalization of protein traffic in insulin-sensitive cells. Am J Physiol 271:E1–E14

    CAS  PubMed  Google Scholar 

  55. Karlsson M, Thorn H, Parpal S, Stralfors P, Gustavsson J (2002) Insulin induces translocation of glucose transporter GLUT4 to plasma membrane caveolae in adipocytes. FASEB J 16:249–251

    CAS  PubMed  Google Scholar 

  56. Karnieli E, Hissin PJ, Simpson IA, Salans LB, Cushman SW (1981) A possible mechanism of insulin resistance in the rat adipose cell in streptozotocin-induced diabetes mellitus. Depletion of intracellular glucose transport systems. J Clin Invest 68:811–814

    CAS  PubMed  Google Scholar 

  57. Kessler A, Tomas E, Immler D, Meyer HE, Zorzano A, Eckel J (2000) Rab11 is associated with GLUT4-containing vesicles and redistributes in response to insulin. Diabetologia 43:1518–1527

    Google Scholar 

  58. Kessler A, Uphues I, Ouwens DM, Till M, Eckel J (2001) Diversification of cardiac insulin signaling involves the p85 alpha/beta subunits of phosphatidylinositol 3-kinase. Am J Physiol 280:E65–E74

    CAS  Google Scholar 

  59. Khan AH, Pessin JE (2002) Insulin regulation of glucose uptake: a complex interplay of intracellular signalling pathways. Diabetologia 45:1475–1483

    Google Scholar 

  60. Kono T (1982) Recycling of the insulin-sensitive glucose transport mechanism in fat-cells. Biochem Soc Trans 10:9–10

    CAS  PubMed  Google Scholar 

  61. Koonen DPY, Coumans WA, Arumugam Y, Bonen A, Glatz JFC, Luiken JJFP (2002) Giant membrane vesicles as a model to study cellular substrate uptake dissected from metabolism. Mol Cell Biochem 239:121–130

    Article  CAS  PubMed  Google Scholar 

  62. Kupriyanova TA, Kandror KV (1999) Akt-2 binds to Glut4-containing vesicles and phosphorylates their component proteins in response to insulin. J Biol Chem 274:1458–1464

    Article  CAS  PubMed  Google Scholar 

  63. Lango R, Smolenski RT, Narkiewicz M, Suchorzewska J, Lysiak-Szydlowska W (2001) Influence of L-carnitine and its derivatives on myocardial metabolism and function in ischemic heart disease and during cardiopulmonary bypass. Cardiovasc Res 51:21–29

    Google Scholar 

  64. Lasley RD, Smart EJ (2001) Cardiac myocyte adenosine receptors and caveolae. Trends Cardiovasc Med 11:259–263

    Article  CAS  PubMed  Google Scholar 

  65. Lopaschuk GD (2001) Malonyl CoA control of fatty acid oxidation in the diabetic rat heart. Adv Exp Med Biol 498:155–165

    CAS  PubMed  Google Scholar 

  66. Lopaschuk GD (2002) Metabolic abnormalities in the diabetic heart. Heart Fail Rev 7:149–159

    Article  CAS  PubMed  Google Scholar 

  67. Luiken JJFP, van Nieuwenhoven FA, America G, van der Vusse GJ, Glatz JFC (1997) Uptake and metabolism of palmitate by isolated cardiac myocytes from adult rats: involvement of sarcolemmal proteins. J Lipid Res 38:745–758

    CAS  PubMed  Google Scholar 

  68. Luiken JJFP, Turcotte LP, Bonen A (1999) Protein-mediated palmitate uptake and expression of fatty acid transport proteins in heart giant vesicles. J Lipid Res 40:1007–1016

    CAS  PubMed  Google Scholar 

  69. Luiken JJFP, Arumugam Y, Dyck DJ, Bell RC, Pelsers MM, Turcotte LP, Tandon NN, Glatz JFC, Bonen A (2001) Increased rates of fatty acid uptake and plasmalemmal fatty acid transporters in obese Zucker rats. J Biol Chem 276:40567–40573

    Article  CAS  PubMed  Google Scholar 

  70. Luiken JJFP, Willems J, van der Vusse GJ, Glatz JFC (2001) Electrostimulation enhances FAT/CD36-mediated long-chain fatty acid uptake by isolated rat cardiac myocytes. Am J Physiol 281:E704–E712

    CAS  Google Scholar 

  71. Luiken JJFP, Dyck DJ, Han XX, Tandon NN, Arumugam Y, Glatz JFC, Bonen A (2002) Insulin induces the translocation of the fatty acid transporter FAT/CD36 to the plasma membrane. Am J Physiol 282:E491–E495

    CAS  Google Scholar 

  72. Luiken JJFP, Koonen DP, Willems J, Zorzano A, Becker C, Fischer Y, Tandon NN, Van Der Vusse GJ, Bonen A, Glatz JFC (2002) Insulin stimulates long-chain fatty acid utilization by rat cardiac myocytes through cellular redistribution of FAT/CD36. Diabetes 51:3113–3119

    Google Scholar 

  73. Luiken JJFP, Willems J, Coort SLM, Coumans WA, Bonen A, Van Der Vusse GJ, Glatz JFC (2002) Effects of cAMP modulators on long-chain fatty-acid uptake and utilization by electrically stimulated rat cardiac myocytes. Biochem J 367:881–887

    Article  CAS  PubMed  Google Scholar 

  74. Luiken JJFP, Coort SLM, Willems J, Coumans WA, Bonen A, van der Vusse GJ, Glatz JFC (2003) Contraction-induced FAT/CD36 translocation in rat cardiac myocytes is mediated through AMP-activated protein kinase signaling. Diabetes 52:1627–1634

    Google Scholar 

  75. Lund S, Holman GD, Schmitz O, Pedersen O (1995) Contraction stimulates translocation of glucose transporter GLUT4 in skeletal muscle through a mechanism distinct from that of insulin. Proc Natl Acad Sci USA 92:5817–5821

    CAS  PubMed  Google Scholar 

  76. Malide D, Ramm G, Cushman SW, Slot JW (2000) Immunoelectron microscopic evidence that GLUT4 translocation explains the stimulation of glucose transport in isolated rat white adipose cells. J Cell Sci 113:4203–4210

    CAS  PubMed  Google Scholar 

  77. Martin LB, Shewan A, Millar CA, Gould GW, James DE (1998) Vesicle-associated membrane protein 2 plays a specific role in the insulin-dependent trafficking of the facilitative glucose transporter GLUT4 in 3T3-L1 adipocytes. J Biol Chem 273:1444–1452

    Article  CAS  PubMed  Google Scholar 

  78. Martinez O, Antony C, Pehau-Arnaudet G, Berger EG, Salamero J, Goud B (1997) GTP-bound forms of rab6 induce the redistribution of Golgi proteins into the endoplasmic reticulum. Proc Natl Acad Sci USA 94:1828–1833

    Article  CAS  PubMed  Google Scholar 

  79. Merrill GF, Kurth EJ, Hardie DG, Winder WW (1997) AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol 273:E1107–E1112

    CAS  PubMed  Google Scholar 

  80. Min J, Okada S, Kanzaki M, Elmendorf JS, Coker KJ, Ceresa BP, Syu LJ, Noda Y, Saltiel AR, Pessin JE (1999) Synip: a novel insulin-regulated syntaxin 4-binding protein mediating GLUT4 translocation in adipocytes. Mol Cell 3:751–760

    Article  CAS  PubMed  Google Scholar 

  81. Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ (2001) A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7:1085–1094

    Article  CAS  PubMed  Google Scholar 

  82. Mueckler M (1994) Facilitative glucose transporters. Eur J Biochem 219:713–725

    CAS  PubMed  Google Scholar 

  83. Muller H, Deckers K, Eckel J (2002) The fatty acid translocase (FAT)/CD36 and the glucose transporter GLUT4 are localized in different cellular compartments in rat cardiac muscle. Biochem Biophys Res Commun 293:665–669

    Article  CAS  PubMed  Google Scholar 

  84. Munoz P, Mora S, Sevilla L, Kaliman P, Tomas E, Guma A, Testar X, Palacin M, Zorzano A (1996) Expression and insulin-regulated distribution of caveolin in skeletal muscle. Caveolin does not colocalize with GLUT4 in intracellular membranes. J Biol Chem 271:8133–8139

    Article  CAS  PubMed  Google Scholar 

  85. Muoio DM, Dohm GL, Tapscott EB, Coleman RA (1999) Leptin opposes insulin’s effects on fatty acid partitioning in muscles isolated from obese ob/ob mice. Am J Physiol 276:E913–E921

    CAS  PubMed  Google Scholar 

  86. Oram JF, Wenger JI, Neely JR (1975) Regulation of long chain fatty acid activation in heart muscle. J Biol Chem 250:73–78

    CAS  PubMed  Google Scholar 

  87. Pearce SF, Wu J, Silverstein RL (1994) A carboxyl terminal truncation mutant of CD36 is secreted and binds thrombospondin: evidence for a single transmembrane domain. Blood 84:384–389

    CAS  PubMed  Google Scholar 

  88. Ploug T, van Deurs B, Ai H, Cushman SW, Ralston E (1998) Analysis of GLUT4 distribution in whole skeletal muscle fibers: identification of distinct storage compartments that are recruited by insulin and muscle contractions. J Cell Biol 142:1429–1446

    CAS  PubMed  Google Scholar 

  89. Plutner H, Cox AD, Pind S, Khosravi-Far R, Bourne JR, Schwaninger R, Der CJ, Balch WE (1991) Rab1b regulates vesicular transport between the endoplasmic reticulum and successive Golgi compartments. J Cell Biol 115:31–43

    CAS  PubMed  Google Scholar 

  90. Pohl J, Ring A, Stremmel W (2002) Uptake of long-chain fatty acids in HepG2 cells involves caveolae: analysis of a novel pathway. J Lipid Res 43:1390–1399

    Article  CAS  PubMed  Google Scholar 

  91. Ponticos M, Lu QL, Morgan JE, Hardie DG, Partridge TA, Carling D (1998) Dual regulation of the AMP-activated protein kinase provides a novel mechanism for the control of creatine kinase in skeletal muscle. EMBO J 17:1688–1699

    Article  CAS  PubMed  Google Scholar 

  92. Ralston E, Ploug T (1999) Caveolin-3 is associated with the T-tubules of mature skeletal muscle fibers. Exp Cell Res 246:510–515

    Article  CAS  PubMed  Google Scholar 

  93. Ramrath S, Tritschler HJ, Eckel J (1999) Stimulation of cardiac glucose transport by thioctic acid and insulin. Horm Metab Res 31:632–635

    CAS  PubMed  Google Scholar 

  94. Randle PJ, Garland PB, Newsholme EA, Hales CN (1965) The glucose fatty acid cycle in obesity and maturity onset diabetes mellitus. Ann NY Acad Sci 131:324–333

    CAS  PubMed  Google Scholar 

  95. Rett K, Wicklmayr M, Dietze GJ, Haring HU (1996) Insulin-induced glucose transporter (GLUT1 and GLUT4) translocation in cardiac muscle tissue is mimicked by bradykinin. Diabetes 45:S66–S69

    Google Scholar 

  96. Rodrigues B, Cam MC, McNeill JH (1998) Metabolic disturbances in diabetic cardiomyopathy. Mol Cell Biochem 180:53–57

    Article  CAS  PubMed  Google Scholar 

  97. Ros-Baro A, Lopez-Iglesias C, Peiro S, Bellido D, Palacin M, Zorzano A, Camps M (2001) Lipid rafts are required for GLUT4 internalization in adipose cells. Proc Natl Acad Sci USA 98:12050–12055

    CAS  PubMed  Google Scholar 

  98. Rose H, Hennecke T, Kammermeier H (1990) Sarcolemmal fatty acid transfer in isolated cardiomyocytes governed by albumin/membrane-lipid partition. J Mol Cell Cardiol 22:883–892

    CAS  PubMed  Google Scholar 

  99. Saltis J, Habberfield AD, Egan JJ, Londos C, Simpson IA, Cushman SW (1991) Role of protein kinase C in the regulation of glucose transport in the rat adipose cell. Translocation of glucose transporters without stimulation of glucose transport activity. J Biol Chem 266:261–267

    CAS  PubMed  Google Scholar 

  100. Schaffer JE, Lodish HF (1994) Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 79:427–436

    CAS  PubMed  Google Scholar 

  101. Sevilla L, Tomas E, Munoz P, Guma A, Fischer Y, Thomas J, Ruiz-Montasell B, Testar X, Palacin M, Blasi J, Zorzano A (1997) Characterization of two distinct intracellular GLUT4 membrane populations in muscle fiber. Differential protein composition and sensitivity to insulin. Endocrinology 138:3006–3015

    CAS  PubMed  Google Scholar 

  102. Shulman GI (2000) Cellular mechanisms of insulin resistance. J Clin Invest 106:171–176

    CAS  PubMed  Google Scholar 

  103. Slot JW, Geuze HJ, Gigengack S, James DE, Lienhard GE (1991) Translocation of the glucose transporter GLUT4 in cardiac myocytes of the rat. Proc Natl Acad Sci USA 88:7815–7819

    CAS  PubMed  Google Scholar 

  104. Sogaard M, Tani K, Ye RR, Geromanos S, Tempst P, Kirchhausen T, Rothman JE, Sollner T (1994) A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles. Cell 78:937–948

    CAS  PubMed  Google Scholar 

  105. Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, Lisanti MP (1996) Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem 271:15160–15165

    CAS  PubMed  Google Scholar 

  106. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149:901–914

    PubMed  Google Scholar 

  107. St.Denis JF, Cushman SW (1998) Role of SNAREs in the GLUT4 translocation response to insulin in adipose cells and muscle. J Basic Clin Physiol Pharmacol 9:153–165

    CAS  PubMed  Google Scholar 

  108. Stagsted J, Olsson L, Holman GD, Cushman SW, Satoh S (1993) Inhibition of internalization of glucose transporters and IGF-II receptors. Mechanism of action of MHC class I-derived peptides which augment the insulin response in rat adipose cells. J Biol Chem 268:22809–22813

    CAS  PubMed  Google Scholar 

  109. Stahl A, Evans JG, Pattel S, Hirsch D, Lodish HF (2002) Insulin causes fatty acid transport protein translocation and enhanced fatty acid uptake in adipocytes. Dev Cell 2:477–488

    CAS  PubMed  Google Scholar 

  110. Stremmel W (1988) Fatty acid uptake by isolated rat heart myocytes represents a carrier-mediated transport process. J Clin Invest 81:844–852

    CAS  PubMed  Google Scholar 

  111. Stuart Wood I, Trayhurn P (2003) Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. Br J Nutr 89:3–9

    CAS  PubMed  Google Scholar 

  112. Stump DD, Zhou SL, Berk PD (1993) Comparison of plasma membrane FABP and mitochondrial isoform of aspartate aminotransferase from rat liver. Am J Physiol 265:G894–G902

    CAS  PubMed  Google Scholar 

  113. Taegtmeyer H, Goodwin GW, Doenst T, Frazier OH (1997) Substrate metabolism as a determinant for postischemic functional recovery of the heart. Am J Cardiol 80:3A–10A

    Article  CAS  PubMed  Google Scholar 

  114. Tomas E, Sevilla L, Palacin M, Zorzano A (2001) The insulin-sensitive GLUT4 storage compartment is a postendocytic and heterogeneous population recruited by acute exercise. Biochem Biophys Res Commun 284:490–495

    Article  CAS  PubMed  Google Scholar 

  115. Trischler M, Stoorvogel W, Ullrich O (1999) Biochemical analysis of distinct Rab5- and Rab11-positive endosomes along the transferrin pathway. J Cell Sci112:4773–4783

    Google Scholar 

  116. Tsakiridis T, Vranic M, Klip A (1995) Phosphatidylinositol 3-kinase and the actin network are not required for the stimulation of glucose transport caused by mitochondrial uncoupling: comparison with insulin action. Biochem J 309:1–5

    PubMed  Google Scholar 

  117. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135:913–924

    CAS  PubMed  Google Scholar 

  118. Unger RH, Orci L (2001) Diseases of liporegulation: new perspective on obesity and related disorders. FASEB J 15:312–321

    CAS  PubMed  Google Scholar 

  119. Uphues I, Kolter T, Goud B, Eckel J (1994) Insulin-induced translocation of the glucose transporter GLUT4 in cardiac muscle: studies on the role of small-molecular-mass GTP-binding proteins. Biochem J 301:177–182

    CAS  PubMed  Google Scholar 

  120. Uphues I, Chern Y, Eckel J (1995) Insulin-dependent translocation of the small GTP-binding protein rab3C in cardiac muscle: studies on insulin-resistant Zucker rats. FEBS Lett 377:109–112

    Article  CAS  PubMed  Google Scholar 

  121. Van der Vusse GJ, Coumans WA, Van der Veen E, Drake AJ, Flameng W, Suy R (1984) ATP, creatine phosphate and glycogen content in human myocardial biopsies: markers for the efficacy of cardioprotection during aorto-coronary bypass surgery. Vasc Surg 18:127–134

    Google Scholar 

  122. Van der Vusse GJ, Glatz JF, Stam HC, Reneman RS (1992) Fatty acid homeostasis in the normoxic and ischemic heart. Physiol Rev 72:881–940

    PubMed  Google Scholar 

  123. Van der Vusse GJ, van Bilsen M, Glatz JFC (2000) Cardiac fatty acid uptake and transport in health and disease. Cardiovasc Res 45:279–293

    Google Scholar 

  124. Van Nieuwenhoven FA, Willemsen PHM, Van der Vusse GJ, Glatz JFC (1999) Co-expression in rat heart and skeletal muscle of four genes coding for proteins implicated in long-chain fatty acid uptake. Int J Biochem Cell Biol 31:489–498

    Article  PubMed  Google Scholar 

  125. Watson RT, Pessin JE (2001) Subcellular compartmentalization and trafficking of the insulin-responsive glucose transporter, GLUT4. Exp Cell Res 271:75–83

    Article  CAS  PubMed  Google Scholar 

  126. Weisiger RA, Fitz JG, Scharschmidt BF (1989) Hepatic oleate uptake. Electrochemical driving forces in intact rat liver. J Clin Invest 83:411–420

    Google Scholar 

  127. Wheeler TJ, Fell RD, Hauck MA (1994) Translocation of two glucose transporters in heart: effects of rotenone, uncouplers, workload, palmitate, insulin and anoxia. Biochim Biophys Acta 1196:191–200

    Article  CAS  PubMed  Google Scholar 

  128. Wu G, Yussman MG, Barrett TJ, Hahn HS, Osinska H, Hilliard GM, Wang X, Toyokawa T, Yatani A, Lynch RA, Robbins J, Dorn GW 2nd (2001) Increased myocardial Rab GTPase expression: a consequence and cause of cardiomyopathy. Circ Res 89:1130–1137

    CAS  PubMed  Google Scholar 

  129. Yeh JI, Gulve EA, Rameh L, Birnbaum MJ (1995) The effects of wortmannin on rat skeletal muscle. Dissociation of signaling pathways for insulin- and contraction-activated hexose transport. J Biol Chem 270:2107–2111

    Article  CAS  PubMed  Google Scholar 

  130. Ylitalo K, Ala-Rami A, Vuorinen K, Peuhkurinen K, Lepojarvi M, Kaukoranta P, Kiviluoma K, Hassinen I (2001) Reversible ischemic inhibition of F1F0-ATPase in rat and human myocardium. Biochim Biophys Acta 1504:329–339

    Article  CAS  PubMed  Google Scholar 

  131. Young LH, Renfu Y, Russell R, Hu X, Caplan M, Ren J, Shulman GI, Sinusas AJ (1997) Low-flow ischemia leads to translocation of canine heart GLUT-4 and GLUT-1 glucose transporters to the sarcolemma in vivo. Circulation 95:415–422

    CAS  PubMed  Google Scholar 

  132. Zerial M, Stenmark H (1993) Rab GTPases in vesicular transport. Curr Opin Cell Biol 5:613–620

    CAS  PubMed  Google Scholar 

  133. Zhou SL, Potter BJ, Stump D, Sorrentino D, Berk PD (1990) Quantitation of plasma membrane fatty acid-binding protein by enzyme dilution and monoclonal antibody based immunoassay. Mol Cell Biochem 98:183–189

    CAS  PubMed  Google Scholar 

  134. Zhou M, Sevilla L, Vallega G, Chen P, Palacin M, Zorzano A, Pilch PF, Kandror KV (1998) Insulin-dependent protein trafficking in skeletal muscle cells. Am J Physiol 275:E187–E196

    CAS  PubMed  Google Scholar 

  135. Zorzano A, Sevilla L, Camps M, Becker C, Meyer J, Kammermeier H, Munoz P, Guma A, Testar X, Palacin M, Blasi J, Fischer Y (1997) Regulation of glucose transport, and glucose transporters expression and trafficking in the heart: studies in cardiac myocytes. Am J Cardiol 80:65A–76A

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Work in the authors’ laboratories is supported by the Netherlands Heart Foundation, grant 2000.156, and by the Heart and Stroke Foundation of Ontario. Joost Luiken is the recipient of a VIDI-Innovational Research grant from the Netherlands Organisation for Scientific Research (NWO-ZonMw grant No. 016.036.305). Arend Bonen is a Canada Research Chair in Metabolism and Health. Jan Glatz is Netherlands Heart Foundation Professor of Cardiac Metabolism.

Author information

Authors and Affiliations

  1. Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, P.O. Box 616, 6200 MD, Maastricht, The Netherlands

    Joost J. F. P. Luiken, Susan L. M. Coort, Debby P. Y. Koonen & Jan F. C. Glatz

  2. Department of Biochemical Physiology and Institute of Biomembranes, Utrecht University, 3584 CH, Utrecht, TheNetherlands

    Dick J. van der Horst

  3. Department of Human Biology and Nutritional Sciences, University of Guelph, Guelph, N1WG 2W1, Canada

    Arend Bonen

  4. Departament de Bioquímica i Biologia Molecular, Facultat de Biologia, Universitat de Barcelona and Parc Científic de Barcelona, Barcelona, Spain

    Antonio Zorzano

Authors
  1. Joost J. F. P. Luiken
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susan L. M. Coort
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Debby P. Y. Koonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dick J. van der Horst
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arend Bonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Antonio Zorzano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jan F. C. Glatz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joost J. F. P. Luiken.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Luiken, J.J.F.P., Coort, S.L.M., Koonen, D.P.Y. et al. Regulation of cardiac long-chain fatty acid and glucose uptake by translocation of substrate transporters. Pflugers Arch - Eur J Physiol 448, 1–15 (2004). https://doi.org/10.1007/s00424-003-1199-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-003-1199-4

Keywords

Search

Navigation