3,961
Views
6
CrossRef citations to date
0
Altmetric
Reviews

Fatty acid transport in skeletal muscle: role in energy provision and insulin resistance

, , , &
Pages 731-745 | Published online: 18 Jan 2017

Bibliography

  • Rolfe DF, Brown GC: Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731–758 (1997).
  • 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 22, 7–14 (2007).
  • Bonen A, Glatz JF, Luiken JJFP: Regulation of fatty acid transport and membrane transporters in health and disease. Mol. Cell. Biochem. 239, 181–192 (2002).
  • 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. 18, 1144–1146 (2004).
  • ▪▪ First human study to report the permanent relocation of CD36 to the sarcolemma and an increase in muscle fatty acid transport in obesity and Type 2 diabetes, and linking these processes to the accumulation of intramuscular lipids.
  • Luiken JJFP, Arumugam Y, Dyck DJ et al.: Increased rates of fatty acid uptake and plasmalemmal fatty acid transporters in obese Zucker rats. J. Biol. Chem. 276, 40567–40573 (2001).
  • ▪▪ First demonstration in a well-known animal model of insulin resistance that fatty acid transport is upregulated owing to the permanent relocation of CD36 to the plasma membrane, while its protein level in muscle is unaltered and fatty acid transporter proteins and mRNAs do not correlate.
  • Luiken JJFP, Arumugam Y, Bell RC et al.: Changes in fatty acid transport and transporters are related to the severity of insulin deficiency. Am. J. Physiol. Endocrinol. Metab. 282, 612–621 (2002).
  • Koonen DPY, Benton CR, Arumugam Y et al.: Different mechanisms can alter fatty acid transport when muscle contractile activity is chronically altered. Am. J. Physiol. Endocrinol. Metab. 286, 1042–1049 (2004).
  • Bonen A, Chabowski A, Luiken JJFP et al.: 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 22, 15–29 (2007).
  • Glatz JF, Luiken JJ, Bonen A: Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol. Rev. 90, 367–417 (2010).
  • Hamilton JA: New insights into the roles of proteins and lipids in membrane transport of fatty acids. Prostaglandins Leukot. Essent. Fatty Acids 77, 355–361 (2007).
  • Bonen A, Luiken JJFP, Lui S et al.: Palmitate transport and fatty acid transporters in red and white muscles. Am. J. Physiol. Endocrinol. Metab. 275, E471-E478 (1998). ?? First study to characterize the fatty acid transport system in metabolically important tissue, namely skeletal muscle.
  • ▪▪ First study to characterize the fatty acid transport system in metabolically important tissue, namely skeletal muscle.
  • Luiken JJFP, Turcotte LP, Bonen A: Protein-mediated palmitate uptake and expression of fatty acid transport proteins in heart giant vesicles. J. Lipid Res. 40, 1007–1016 (1999).
  • Koonen DPY, Coumans WA, Arumugam Y et al.: Giant membrane vesicles as a model to study cellular substrate uptake dissected from metabolism. Mol. Cell. Biochem. 239, 121–130 (2002).
  • Bonen A, Luiken JJFP, Arumugam Y et al.: Acute regulation of fatty acid uptake involves the cellular redistribution of fatty acid translocase. J. Biol. Chem. 275, 14501–14508 (2000).
  • ▪▪ First demonstration that fatty acid transport is acutely regulated, within minutes, via the translocation of CD36 to the plasma membrane when a metabolic challenge (muscle contraction) is provided.
  • Talanian JL, Holloway GP, Snook LA et al.: Exercise training increases sarcolemmal and mitochondrial fatty acid transport proteins in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 299, E180-E188 (2010).
  • Hirsch D, Stahl A, Lodish HF: A family of fatty acid transporters conserved from mycobacterium to man. Proc. Natl Acad. Sci. USA 95, 8625–8629 (1998).
  • Gimeno RE, Ortegon AM, Patel S et al. Characterization of a heart-specific fatty acid transport protein. J. Biol. Chem. 278, 16039–16044 (2003).
  • 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. 284, 16522–16530 (2009).
  • DiRusso CC, Li H, Darwis D et al.: Comparative biochemical studies of the murine fatty acid transport proteins (FATP) expressed in yeast. J. Biol. Chem. 280, 16829–16837 (2005).
  • Hall AM, Wiczer BM, Herrmann T et al.: Enzymatic properties of purified murine fatty acid transport protein 4 and analysis of acyl-CoA synthetase activities in tissues from FATP4 null mice. J. Biol. Chem. 280, 11948–11954 (2005).
  • Lobo S, Wiczer BM, Smith AJ et al.: Fatty acid metabolism in adipocytes: functional analysis of fatty acid transport proteins 1 and 4. J. Lipid Res. 48, 609–620 (2007).
  • 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 1781, 61–71 (2008).
  • Eyre NS, Cleland LG, Mayrhofer G: FAT/CD36 expression alone is insufficient to enhance cellular uptake of oleate. Biochem. Biophys. Res. Comm. 370, 404–409 (2008).
  • Milger K, Herrmann T, Becker C et al. Cellular uptake of fatty acids driven by the ER-localized acyl-CoA synthetase FATP4. J. Cell. Sci. 119, 4678–4688 (2006).
  • 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. 583(13),p m 2294–300 (2009).
  • Luiken JJFP, Dyck DJ, Han X-X et al.: Insulin induces the translocation of the fatty acid transporter FAT/CD36 to the plasma membrane. Am. J. Physiol. Endocrinol. Metab. 282, E491-E495 (2002).
  • ▪▪ First study demonstrating that insulin stimulates CD36 translocation and fatty acid transport.
  • Sakamoto K, Goodyear LJ: Invited review: intracellular signaling in contracting skeletal muscle. J. Appl. Physiol. 93, 369–383 (2002).
  • Jain S, Glatz JFC, Luiken JJFP et al. Regulation of insulin- and contraction- stimuated faty acid transporters: FAT/CD36, FABPpm, FATP1, FATP4 and FATP6. Presented at: 49th International Congress on the Bioscience of Lipids. Maastricht, The Netherlands, 26–30 August, 2008.
  • Jain S, Bonen A: Munc18c is not required for insulin-, and contraction-induced fatty acid transporter trafficking. Presented at: Ontario Exercise Physiology Coneference 2010. Orillia, Ontario, Canada, 22–24 January 2010.
  • Schwenk RW, Dirkx E, Coumans W et al.: Requirement for distinct vesicle-associated membrane proteins in insulin- and AMPK-activated protein kinase (AMPK)- induced translocation of GLUT4 and CD36 in cultured cardiomyocytes. Diabetologia 53(10), 2209–2219 (2010).
  • Luiken JJFP, Coort SML, Willems J et al.: Contraction-induced fatty acid translocase/ CD36 translocation in rat cardiac myocytes is mediated through AMP-activated protein kinase signaling. Diabetes 52, 1627–1634 (2003).
  • Raney MA, Yee AJ, Todd MK et al.: AMPK activation is not critical in the regulation of muscle FA uptake and oxidation during low-intensity muscle contraction. Am. J. Physiol. Endocrinol. Metab. 288, E592-E598 (2005).
  • 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. 184, 131–139 (2005).
  • ▪ Demonstrates that muscle contraction-induced CD36 translocation is dependent on the ERK1/2 signaling pathway.
  • Raney MA, Turcotte LP: Evidence for the involvement of CaMKII and AMPK in Ca2+-dependent signaling pathways regulating FA uptake and oxidation in contracting rodent muscle. J. Appl. Physiol. 104, 1366–1373 (2008).
  • Abbott MJ, Edelman AM, Turcotte LP: CaMKK is an upstream signal of AMP- activated protein kinase in regulation of substrate metabolism in contracting skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R1724-R1732 (2009).
  • Holloszy JO, Booth FW: Biochemical adaptations to endurance exercise in muscle. Ann. Rev. Physiol. 38, 273–291 (1976).
  • Kiens B: Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol. Rev. 86, 205–243 (2006).
  • Bonen A, Dyck DJ, Ibrahimi A et al.: Muscle contractile activity increases fatty acid metabolism and transport and FAT/CD36. Am. J. Physiol. Endocrinol. Metab. 276, E642-E649 (1999).
  • Turcotte LP, Swenberger JR, Tucker MZ et al.: Training-induced elevation in FABPpm is associated with increased palmitate use in contracting muscle. J. Appl. Physiol. 87, 285–293 (1999).
  • McFarlan JT, Holloway GP, Spriet LL et al.: Fatty acid transport protein CD36 is essential for the training-induced increase in fatty acid oxidation. Med. Sci. Sports Exercise 42(5), 43 (2010).
  • Tunstall RJ, Mehan KA, Wadley GD et al.: Exercise training increases lipid metabolism gene expression in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 283, E66-E72 (2002).
  • Kiens B, Kristiansen S, Jensen P et al.: Membrane associated fatty acid binding protein (FABPpm) in human skeletal muscle is increased by endurance training. Biochem. Biophys. Res. Comm. 231, 463–465 (1997).
  • Talanian JL, Galloway SD, Heigenhauser GJ et al.: Two weeks of high-intensity aerobic interval training increases the capacity for fat oxidation during exercise in women. J. Appl. Physiol. 102, 1439–1447 (2007).
  • Burgomaster KA, Cermak NM, Phillips SM et al.: Divergent response of metabolite transport proteins in human skeletal muscle after sprint interval training and detraining. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R1970-R1976 (2007).
  • De Bock K, Derave W, Eijnde BO et al.: Effect of training in the fasted state on metabolic responses during exercise with carbohydrate intake. J. Appl. Physiol. 104, 1045–1055 (2008).
  • Bonen A, Han X-X, Habets DDJ et al.: A null mutation in skeletal muscle FAT/CD36 reveals its essential role in insulin-, and AICAR-stimulated fatty acid metabolism. Am. J. Physiol. Endocrinol. Metab. 292, E1740-E1749 (2007).
  • ▪▪ Demonstrates that skeletal muscle fatty acid metabolism cannot respond adequately to metabolic challenges in the absence of CD36.
  • Campbell SE, Tandon NN, Woldegiorgis G et al.: A novel function for FAT/CD36: involvement in long chain fatty acid transfer into the mitochondria. J. Biol. Chem 279, 36335–36341 (2004).
  • ▪▪ Demonstrates that CD36 is present in mitochondria and that it contributes in an unknown manner to the regulation of skeletal muscle fatty acid oxidation.
  • Holloway GP, Jain SS, Bezaire V 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. 297, R960-R967 (2009).
  • Benton CR, Nickerson J, Lally J et al.: Modest PGC-1a overexpression in muscle in vivo is sufficient to increase insulin sensitivity and palmitate oxidation in SS, not IMF, mitochondria. J. Biol. Chem. 283, 4228–4240 (2008).
  • Benton CR, Holloway GP, Campbell SE et al.: Rosiglitazone increases fatty acid oxidation and fatty acid translocase (FAT/CD36) but not carnitine palmitoyltransferase I in rat muscle mitochondria. J. Physiol. 586, 1755–1766 (2008).
  • Holloway GP, Thrush AB, Heigenhauser GJ et al.: Skeletal muscle mitochondrial FAT/CD36 and palmitate oxidation are not decreased in obese women. Am. J. Physiol. Endocrinol. Metab. 292, E1782-E1789 (2007).
  • 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. 290, E509-E515 (2006).
  • Holloway GP, Bezaire V, Heigenhauser GJ et al.: Mitochondrial long chain fatty acid oxidation, fatty acid translocase/CD36 content and carnitine palmitoyltransferase 1 activity in human skeletal muscle during aerobic exercise. J. Physiol. 571, 201–210 (2006).
  • Jeppesen J, Mogensen M, Prats C et al. : FAT/CD36 is localized in sarcolemma and in vesicle-like structures in subsarcolemma regions, but not in mitochondria. J. Lipid Res. 51(6), 1504–1512 (2010).
  • Schenk S, Horowitz JF: Coimmunoprecipitation of FAT/CD36 and CPTI in skeletal muscle increases proportionally with fat oxidation after endurance exercise training. Am. J. Physiol. Endocrinol. Metab. 291, E254-E260 (2006).
  • Aoi W, Naito Y, Takanami Y et al. : Astaxanthin improves muscle lipid metabolism in exercise via inhibitory effect of oxidative CPT I modification. Biochem. Biophys. Res. Comm. 366, 892–897 (2008).
  • King KL, Stanley WC, Rosca M et al. : Fatty acid oxidation in cardiac and skeletal muscle mitochondria is unaffected by deletion of CD36. Arch. Biochem. Biophys. 467, 234–238 (2007).
  • Distler AM, Kerner J, Peterman SM et al.: A targeted proteomic approach for the analysis of rat liver mitochondrial outer membrane proteins with extensive sequence coverage. Anal. Biochem. 356, 18–29 (2006).
  • Holloway GP, Lally J, Nickerson JG et al. : Fatty acid binding protein facilitates sarcolemmal fatty acid transport but not mitochondrial oxidation in rat and human skeletal muscle. J. Physiol. 582, 393–405 (2007).
  • 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. 50, 1789–1799 (2009).
  • Habets DDJ, 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. 355, 204–210 (2007).
  • Koves TR, Noland RC, Bates AL et al. : Subsarcolemmal and intermyofibrillar mitochondria play distinct roles in regulating skeletal muscle fatty acid metabolism. Am. J. Physiol. Cell Physiol. 288, C1074-C1082 (2005).
  • 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. 296, E738-E747 (2009).
  • Holloway GP, Luiken JJFP, Glatz JFC et al.: Contribution of FAT/CD36 to the regulation of skeletal muscle fatty acid oxidation: an overview. Acta Physiol. 194, 293–309 (2008).
  • Holland WL, Knotts TA, Chavez JA et al. : Lipid mediators of insulin resistance. Nutr. Rev. 65, S39-S46 (2007).
  • Hancock CR, Han DH, Chen M et al.: High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc. Natl Acad. Sci. USA 105, 7815–7820 (2008).
  • Turner N, Bruce CR, Beale SM et al.: Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56, 2085–2092 (2007).
  • Aguer C, Mercier J, Yong Wai Man C et al. : Intramyocellular lipid accumulation is associated with permanent relocation ex vivo and in vitro of fatty acid translocase (FAT)/CD36 in obese patients. Diabetologia 53(6), 1151–1163 (2010).
  • Holloway GP, Bonen A, Spriet LL: Regulation of skeletal muscle mitochondrial fatty acid metabolism in lean and obese individuals. Am. J. Clin. Nutr. 89, 455S-462S (2009).
  • Mogensen M, Sahlin K, Fernstrom M et al.: Mitochondrial respiration is decreased in skeletal muscle of patients with Type 2 diabetes. Diabetes 56, 1592–1599 (2007).
  • Bandyopadhyay GK, Yu JG, Ofrecio J et al.: Increased malonyl-CoA levels in muscle from obese and Type 2 diabetic subjects lead to decreased fatty acid oxidation and increased lipogenesis; thiazolidinedione treatment reverses these defects. Diabetes 55, 2277–2285 (2006).
  • Mootha VK, Lindgren CM, Eriksson KF et al.: PGC-1a-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267–273 (2003).
  • Koves TR, Ussher JR, Noland RC et al.: Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell. Metab. 7, 45–56 (2008).
  • Chabowski A, Chatham JC, Tandon NN et al.: Fatty acid transport and FAT/CD36 are increased in red but not in white muscle skeletal muscle of Zucker diabetic fatty (ZDF) rats. Am. J. Physiol. Endocrinol. Metab. 291, E675-E682 (2006).
  • Blaak EE, Wagenmakers AJ: The fate of [U-13C] palmitate extracted by skeletal muscle in subjects with Type 2 diabetes and control subjects. Diabetes 51, 784–789 (2002).
  • Wilmsen HM, Ciaraldi TP, Carter L et al.: Thiazolidinediones upregulate impaired fatty acid uptake in skeletal muscle of Type 2 diabetics. Am. J. Physiol. Endocrinol. Metab. 285, E354-E362 (2003).
  • Pelsers MM, Tsintzas K, Boon H et al.: Skeletal muscle fatty acid transporter protein expression in Type 2 diabetes patients compared with overweight, sedentary men and age-matched, endurance-trained cyclists. Acta Physiol. 190, 209–219 (2007).
  • Binnert C, Koistinen HA, Martin G et al.: Fatty acid transport protein-1 mRNA expression in skeletal muscle and in adipose tissue in humans. Am. J. Physiol. Endocrinol. Metab. 279, E1072-E1079 (2000).
  • Simoneau J-A, Veerkamp JH, Turcotte LP et al.: Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J. 13, 2051–2060 (1999).
  • Bell JA, Reed MA, Consitt LA et al.: Lipid partitioning, incomplete fatty acid oxidation, and insulin signal transduction in primary human muscle cells: effects of severe obesity, fatty acid incubation, and fatty acid translocase/CD36 overexpression. J. Clin. Endocrinol. Metab. 95(7), 3400–3410 (2010).
  • Smith AC, Mullen KL, Junkin KA et al. Metformin and exercise reduce muscle FAT/CD36 and lipid accumulation and blunt the progression of high-fat diet induced hyperglycemia. Am. J. Physiol. Endocrinol. Metab. 293, E172-E181 (2007).
  • Michael LF, Wu Z, Cheatham RB et al. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc. Natl. Acad. Sci. USA 98, 3820–3825 (2001).
  • Patti ME, Butte AJ, Crunkhorn S et al.: Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc. Natl Acad. Sci. USA 100, 8466–8471 (2003).
  • Miura S, Kai Y, Ono M et al.: Overexpression of peroxisome proliferator- activated receptor γ coactivator-1α down- regulates GLUT4 mRNA in skeletal muscles. J. Biol. Chem. 278, 31385–31390 (2003).
  • Choi CS, Befroy DE, Codella R et al.: Paradoxical effects of increased expression of PGC-1α on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc. Natl Acad. Sci. USA 105, 19926–19931 (2008).
  • Russell LK, Mansfield CM, Lehman JJ et al. Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor g coactivator-1a promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner. Circ. Res. 94, 525–533 (2004).
  • Benton CR, Wright DC, Bonen A: PGC-1α-mediated regulation of gene expression and metabolism: implications for nutrition and exercise prescriptions. Appl. Physiol. Nutr. Metab. 33, 843–862 (2008).
  • Lira VA, Benton CR, Yan Z et al.: PGC-1α regulation by exercise training and its influence on muscle function and insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 299, E145-E161 (2010).
  • Benton CR, Holloway GP, Han X-X et al. : Increased levels of peroxisome proliferator- activated receptor γ, coactivator 1 α (PGC-1α) improve lipid utilisation, insulin signalling and glucose transport in skeletal muscle of lean and insulin-resistant obese Zucker rats. Diabetologia 53(9), 2008–2019 (2010).
  • Listenberger LL, Han X, Lewis SE et al. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl Acad. Sci. USA 100, 3077–3082 (2003).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.