Prostaglandins, Leukotrienes and Essential Fatty Acids
Volume 82, Issue 4 , Pages 149-154 , April 2010

Fatty acid transport across the cell membrane: Regulation by fatty acid transporters

  • Robert W. Schwenk

      Affiliations

    • Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, P.O. Box 616, NL-6200 MD Maastricht, The Netherlands
  • ,
  • Graham P. Holloway

      Affiliations

    • Department of Human Health & Nutritional Sciences, University of Guelph, Guelph, Ontario, Canada
  • ,
  • Joost J.F.P. Luiken

      Affiliations

    • Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, P.O. Box 616, NL-6200 MD Maastricht, The Netherlands
  • ,
  • Arend Bonen

      Affiliations

    • Department of Human Health & Nutritional Sciences, University of Guelph, Guelph, Ontario, Canada
  • ,
  • Jan F.C. Glatz

      Affiliations

    • Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, P.O. Box 616, NL-6200 MD Maastricht, The Netherlands
    • Corresponding Author InformationCorresponding author. Tel.: +31433881208, +31433881998; fax: +31433884574.

References 

  1. Vorum H, Brodersen R, Kragh-Hansen U, Pedersen AO. Solubility of long-chain fatty acids in phosphate buffer at pH 7.4. Biochim. Biophys. Acta. 1992;1126(2):135–142
  2. Richieri GV, Anel A, Kleinfeld AM. Interactions of long-chain fatty acids and albumin: determination of free fatty acid levels using the fluorescent probe ADIFAB. Biochemistry. 1993;32(29):7574–7580
  3. Vork MM, Glatz JF, Van Der Vusse GJ. On the mechanism of long chain fatty acid transport in cardiomyocytes as facilitated by cytoplasmic fatty acid-binding protein. J. Theor. Biol. 1993;160(2):207–222
  4. Richieri GV, Ogata RT, Kleinfeld AM. Equilibrium constants for the binding of fatty acids with fatty acid-binding proteins from adipocyte, intestine, heart, and liver measured with the fluorescent probe ADIFAB. J. Biol. Chem. 1994;269(39):23918–23930
  5. Richieri GV, Kleinfeld AM. Unbound free fatty acid levels in human serum. J. Lipid Res. 1995;36(2):229–240
  6. Luiken JJ, Koonen DP, Coumans WA, et al. Long-chain fatty acid uptake by skeletal muscle is impaired in homozygous, but not heterozygous, heart-type-FABP null mice. Lipids. 2003;38(4):491–496
  7. Kampf JP, Kleinfeld AM. Is membrane transport of FFA mediated by lipid, protein, or both? An unknown protein mediates free fatty acid transport across the adipocyte plasma membrane. Physiology (Bethesda). 2007;22:7–14
  8. Bonen A, Chabowski A, Luiken JJ, Glatz JF. Is membrane transport of FFA mediated by lipid, protein, or both? Mechanisms and regulation of protein-mediated cellular fatty acid uptake: molecular, biochemical, and physiological evidence. Physiology (Bethesda). 2007;22:15–29
  9. Kamp F, Hamilton JA. pH gradients across phospholipid membranes caused by fast flip-flop of un-ionized fatty acids. Proc. Natl. Acad. Sci. USA. 1992;89(23):11367–11370
  10. Kamp F, Hamilton JA. How fatty acids of different chain length enter and leave cells by free diffusion. Prostaglandins Leukot. Essent. Fatty Acids. 2006;75(3):149–159
  11. Hamilton JA. New insights into the roles of proteins and lipids in membrane transport of fatty acids. Prostaglandins Leukot. Essent. Fatty Acids. 2007;77(5-6):355–361
  12. Glatz JF, Luiken JJ, Bonen A. Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol. Rev. 2010;90:367–417
  13. Clarke DC, Miskovic D, Han XX, et al. Overexpression of membrane-associated fatty acid binding protein (FABPpm) in vivo increases fatty acid sarcolemmal transport and metabolism. Physiol. Genomics. 2004;17(1):31–37
  14. Nickerson JG, Alkhateeb H, Benton CR, et al. Greater transport efficiencies of the membrane fatty acid transporters FAT/CD36 and FATP4 compared with FABPpm and FATP1 and differential effects on fatty acid esterification and oxidation in rat skeletal muscle. J. Biol. Chem. 2009;284(24):16522–16530
  15. Bonen A, Luiken JJ, Arumugam Y, Glatz JF, Tandon NN. Acute regulation of fatty acid uptake involves the cellular redistribution of fatty acid translocase. J. Biol. Chem. 2000;275(19):14501–14508
  16. Luiken JJ, Koonen DP, Willems J, et al. Insulin stimulates long-chain fatty acid utilization by rat cardiac myocytes through cellular redistribution of FAT/CD36. Diabetes. 2002;51(10):3113–3119
  17. Luiken JJ, Coort SL, Willems J, et al. Contraction-induced fatty acid translocase/CD36 translocation in rat cardiac myocytes is mediated through AMP-activated protein kinase signaling. Diabetes. 2003;52(7):1627–1634
  18. Luiken JJ, Willems J, van der Vusse GJ, Glatz JF. Electrostimulation enhances FAT/CD36-mediated long-chain fatty acid uptake by isolated rat cardiac myocytes. Am. J. Physiol. Endocrinol. Metab. 2001;281(4):E704–E712
  19. Karlsson HK, Chibalin AV, Koistinen HA, et al. Kinetics of GLUT4 trafficking in rat and human skeletal muscle. Diabetes. 2009;58(4):847–854
  20. van Oort MM, van Doorn JM, Bonen A, et al. Insulin-induced translocation of CD36 to the plasma membrane is reversible and shows similarity to that of GLUT4. Biochim. Biophys. Acta. 2008;1781(1-2):61–71
  21. Turcotte LP, Raney MA, Todd MK. ERK1/2 inhibition prevents contraction-induced increase in plasma membrane FAT/CD36 content and FA uptake in rodent muscle. Acta Physiol. Scand. 2005;184(2):131–139
  22. Jain SS, Chabowski A, Snook LA, et al. Additive effects of insulin and muscle contraction on fatty acid transport and fatty acid transporters FAT/CD36, FABPpm, FATP1, 4 and 6. FEBS Lett. 2009;583(13):2294–2300
  23. Habets DD, Coumans WA, Voshol PJ, et al. AMPK-mediated increase in myocardial long-chain fatty acid uptake critically depends on sarcolemmal CD36. Biochem. Biophys. Res. Commun. 2007;355(1):204–210
  24. Holloway GP, Jain SS, Bezaire VS, et al. FAT/CD36 null mice reveal that mitochondrial FAT/CD36 is required to up-regulate mitochondrial fatty acid oxidation in contracting muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009;297(4):R960–R967
  25. Luiken JJ, Coort SL, Willems J, Coumans WA, Bonen A, Glatz JF. Dipyridamole alters cardiac substrate preference by inducing translocation of FAT/CD36, but not that of GLUT4. Mol. Pharmacol. 2004;65(3):639–645
  26. Luiken JJ, Momken I, Habets DD, et al. Arsenite modulates cardiac substrate preference by translocation of GLUT4, but not CD36, independent of mitogen-activated protein kinase signaling. Endocrinology. 2006;147(11):5205–5216
  27. Schwenk RW, Luiken JJ, Bonen A, Glatz JF. Regulation of sarcolemmal glucose and fatty acid transporters in cardiac disease. Cardiovasc. Res. 2008;79(2):249–258
  28. Campbell SE, Tandon NN, Woldegiorgis G, Luiken JJ, Glatz JF, Bonen A. A novel function for fatty acid translocase (FAT)/CD36: involvement in long chain fatty acid transfer into the mitochondria. J. Biol. Chem. 2004;279(35):36235–36241
  29. Bezaire V, Bruce CR, Heigenhauser GJ, et al. Identification of fatty acid translocase on human skeletal muscle mitochondrial membranes: essential role in fatty acid oxidation. Am. J. Physiol. Endocrinol. Metab. 2006;290(3):E509–E515
  30. Sebastian D, Guitart M, Garcia-Martinez C, et al. Novel role of FATP1 in mitochondrial fatty acid oxidation in skeletal muscle cells. J. Lipid Res. 2009;
  31. Holloway GP, Bezaire V, Heigenhauser GJ, et al. Mitochondrial long chain fatty acid oxidation, fatty acid translocase/CD36 content and carnitine palmitoyltransferase I activity in human skeletal muscle during aerobic exercise. J. Physiol. 2006;571(Part 1):201–210
  32. Schwenk RW, Luiken JJ, Eckel J. FIP2 and Rip11 specify Rab11a-mediated cellular distribution of GLUT4 and FAT/CD36 in H9c2-hIR cells. Biochem. Biophys. Res. Commun. 2007;363(1):119–125
  33. Eguez L, Lee A, Chavez JA, et al. Full intracellular retention of GLUT4 requires AS160 Rab GTPase activating protein. Cell Metab. 2005;2(4):263–272
  34. Sano H, Eguez L, Teruel MN, et al. Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell. Metab. 2007;5(4):293–303
  35. Ishikura S, Bilan PJ, Klip A. Rabs 8A and 14 are targets of the insulin-regulated Rab-GAP AS160 regulating GLUT4 traffic in muscle cells. Biochem. Biophys. Res. Commun. 2007;353(4):1074–1079
  36. Kramer HF, Witczak CA, Fujii N, et al. Distinct signals regulate AS160 phosphorylation in response to insulin AICAR, and contraction in mouse skeletal muscle. Diabetes. 2006;55(7):2067–2076
  37. Jahn R, Scheller RH. SNAREs—engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 2006;7(9):631–643
  38. Sevilla L, Tomas E, Munoz P, et al. Characterization of two distinct intracellular GLUT4 membrane populations in muscle fiber. Differential protein composition and sensitivity to insulin. Endocrinology. 1997;138(7):3006–3015
  39. Kawanishi M, Tamori Y, Okazawa H, Araki S, Shinoda H, Kasuga M. Role of SNAP23 in insulin-induced translocation of GLUT4 in 3T3-L1 adipocytes. Mediation of complex formation between syntaxin4 and VAMP2. J. Biol. Chem. 2000;275(11):8240–8247
  40. Tamori Y, Kawanishi M, Niki T, et al. Inhibition of insulin-induced GLUT4 translocation by Munc18c through interaction with syntaxin4 in 3T3-L1 adipocytes. J. Biol. Chem. 1998;273(31):19740–19746
  41. Fukuda N, Emoto M, Nakamori Y, et al. DOC2B: a novel syntaxin-4 binding protein mediating insulin-regulated GLUT4 vesicle fusion in adipocytes. Diabetes. 2009;58(2):377–384
  42. Boden G, Chen X, Iqbal N. Acute lowering of plasma fatty acids lowers basal insulin secretion in diabetic and nondiabetic subjects. Diabetes. 1998;47(10):1609–1612
  43. Pan DA, Lillioja S, Kriketos AD, et al. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes. 1997;46(6):983–988
  44. Unger RH. Lipotoxic diseases. Annu. Rev. Med. 2002;53:319–336
  45. Holland WL, Knotts TA, Chavez JA, Wang LP, Hoehn KL, Summers SA. Lipid mediators of insulin resistance. Nutr. Rev. 2007;65(6, Part 2):S39–S46
  46. Luiken JJ, Arumugam Y, Dyck DJ, et al. Increased rates of fatty acid uptake and plasmalemmal fatty acid transporters in obese Zucker rats. J. Biol. Chem. 2001;276(44):40567–40573
  47. Coort SL, Hasselbaink DM, Koonen DP, et al. Enhanced sarcolemmal FAT/CD36 content and triacylglycerol storage in cardiac myocytes from obese Zucker rats. Diabetes. 2004;53(7):1655–1663
  48. Ouwens DM, Diamant M, Fodor M, et al. Cardiac contractile dysfunction in insulin-resistant rats fed a high-fat diet is associated with elevated CD36-mediated fatty acid uptake and esterification. Diabetologia. 2007;50(9):1938–1948
  49. Holloway GP, Benton CR, Mullen KL, et al. In obese rat muscle transport of palmitate is increased and is channeled to triacylglycerol storage despite an increase in mitochondrial palmitate oxidation. Am. J. Physiol. Endocrinol. Metab. 2009;296(4):E738–E747
  50. Bonen A, Parolin ML, Steinberg GR, et al. Triacylglycerol accumulation in human obesity and type 2 diabetes is associated with increased rates of skeletal muscle fatty acid transport and increased sarcolemmal FAT/CD36. FASEB J. 2004;18(10):1144–1146
  51. Glatz JF, Bonen A, Ouwens DM, Luiken JJ. Regulation of sarcolemmal transport of substrates in the healthy and diseased heart. Cardiovasc. Drugs Ther. 2006;20(6):471–476
  52. Su X, Abumrad NA. Cellular fatty acid uptake: a pathway under construction. Trends Endocrinol. Metab. 2009;20(2):72–77
  53. Doege H, Stahl A. Protein-mediated fatty acid uptake: novel insights from in vivo models. Physiology (Bethesda). 2006;21:259–268
  54. Febbraio M, Silverstein RL. CD36: implications in cardiovascular disease. Int. J. Biochem. Cell Biol. 2007;39(11):2012–2030
  55. Yang J, Sambandam N, Han X, et al. CD36 deficiency rescues lipotoxic cardiomyopathy. Circ. Res. 2007;100(8):1208–1217
  56. Mitchell RW, Edmundson CL, Miller DW, Hatch GM. On the mechanism of oleate transport across human brain microvessel endothelial cells. J. Neurochem. 2009;110(3):1049–1057
  57. Owada Y. Fatty acid binding protein: localization and functional significance in the brain. Tohoku J. Exp. Med. 2008;214(3):213–220
  58. Glatz JF, Storch J. Unravelling the significance of cellular fatty acid-binding proteins. Curr. Opin. Lipidol. 2001;12(3):267–274
  59. Storch J, Corsico B. The emerging functions and mechanisms of mammalian fatty acid-binding proteins. Annu. Rev. Nutr. 2008;28:73–95

PII: S0952-3278(10)00073-6

doi: 10.1016/j.plefa.2010.02.029

Prostaglandins, Leukotrienes and Essential Fatty Acids
Volume 82, Issue 4 , Pages 149-154 , April 2010