Exercise- and training-induced upregulation of skeletal muscle fatty acid oxidation are not solely dependent on mitochondrial machinery and biogenesis

Journal of Physiology

Volumn 591, Issue 18, 2013, Pages 4415-4426

  Yoshida, Yuko ^a   Jain, Swati S ^a   Mcfarlan, Jay T ^a   Snook, Laelie A ^a   Chabowski, Adrian ^b   Bonen, Arend ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; CD36 ANTIGEN; FATTY ACID BINDING PROTEIN 2; FATTY ACID TRANSPORTER 4; GLUCOSE TRANSPORTER 4; MITOGEN ACTIVATED PROTEIN KINASE 3;

BIOGENESIS; CELL DENSITY; CONTROLLED STUDY; ENDURANCE TRAINING; ENZYME METABOLISM; EXERCISE; EXERCISE TEST; FATTY ACID METABOLISM; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; HUMAN; MITOCHONDRION; MOUSE; MUSCLE CONTRACTION; MUSCLE EXCITATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SARCOLEMMA; SKELETAL MUSCLE; SOLEUS MUSCLE; TRAINING; UPREGULATION;

ANIMALS; ANTIGENS, CD36; EXERCISE; FATTY ACIDS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL TURNOVER; MUSCLE, SKELETAL; OXIDATION-REDUCTION; PHYSICAL EXERTION;

EID: 84884222352     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.238451     Document Type: Review

References (60)

1. Abumrad NA, El-Maghrabi MR, Amri E-Z, Lopez E & Grimaldi P (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.
2. Aoi W, Naito Y, Takanami Y, Ishii T, Kawai Y, Akagiri S, Kato Y, Osawa T & Yoshikawa T (2008). Astaxanthin improves muscle lipid metabolism in exercise via inhibitory effect of oxidative CPT I modification. Biochem Biophys Res Commun 366, 892-897.
3. Benton CR, Holloway GP, Han XX, Yoshida Y, Snook LA, Lally J, Glatz JF, Luiken JJ, Chabowski A & Bonen A (2010). Increased levels of peroxisome proliferator-activated receptor gamma, coactivator 1 alpha (PGC-1α) improve lipid utilisation, insulin signalling and glucose transport in skeletal muscle of lean and insulin-resistant obese Zucker rats. Diabetologia 53, 2008-2019.
4. Benton CR, Nickerson J, Lally J, Han X-X, Holloway GP, Glatz JFC, Luiken JJFP, Graham TE, Heikkila JJ & Bonen A (2008). Modest PGC-1α 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.
5. Bergstrom J, Hermansen L, Hultman E & Saltin B (1967). Diet, muscle glycogen and physical performance. Acta Physiol Scand 71, 140-150.
6. Bergstrom J & Hultman E (1966). Muscle glycogen synthesis after exercise: an enhancing factor localized to the muscle cells in man. Nature 210, 309-310.
7. Bergstrom J & Hultman E (1967). A study of the glycogen metabolism during exercise in man. Scand J Clin Lab Invest 19, 218-228.
8. Bezaire V, Bruce CR, Heigenhauser GJ, Tandon NN, Glatz JF, Luiken JJ, Bonen A & Spriet LL (2006). 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.
9. Bonen A, Chabowski A, Luiken JJFP & Glatz JFC (2007a). 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) 22, 15-29.
10. Bonen A, Han X-X, Habets DDJ, Febbraio M, Glatz JFC & Luiken JJFP (2007b). 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.
11. 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.
12. Bradley NS, Snook LA, Jain SS, Heigenhauser GJ, Bonen A & Spriet LL (2012). Acute endurance exercise increases plasma membrane fatty acid transport proteins in rat and human skeletal muscle. Am J Physiol Endocrinol Metab 302, E183-189.
13. Bruce CR, Thrush AB, Mertz VA, Bezaire V, Chabowski A, Heigenhauser GJ & Dyck DJ (2006). Endurance training in obese humans improves glucose tolerance, mitochondrial fatty acid oxidation and alters muscle lipid content. Am J Physiol Endocrinol Metab 291, E99-E107.
14. Campbell SE, Tandon NN, Woldegiorgis G, Luiken JJFP, Glatz JFC & Bonen A (2004). A novel function for FAT/CD36: involvement in long chain fatty acid transfer into the mitochondria. J Biol Chem 279, 36335-36341.
15. Coburn CT, Knapp FF Jr, Febbraio M, Beets AL, Silverstein RL & Abumrad NA (2000). Defective uptake and utilization of long chain fatty acids in muscle and adipose tissue of CD36 knockout mice. J Biol Chem 275, 32523-32529.
16. Febbraio M, Abumrad NA, Hajjar DP, Sharma K, Cheng W, Frieda S, Pearce A & Silverstein RL (1999). A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J Biol Chem 274, 19055-19062.
17. Fernandez C, Hansson O, Nevsten P, Holm C & Klint C (2008). Hormone-sensitive lipase is necessary for normal mobilization of lipids during submaximal exercise. Am J Physiol Endocrinol Metab 295, E179-186.
18. Glatz JFC, Luiken JJFP & Bonen A (2010). Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol Rev 90, 367-417.
19. Goudriaan JR, Dahlmans VE, Teusink B, Ouwens DM, Febbraio M, Maassen JA, Romijn JA, Havekes LM & Voshol PJ (2003). CD36 deficiency increases insulin sensitivity in muscle, but induces insulin resistance in the liver in mice. J Lipid Res 44, 2270-2277.
20. Hagenfeldt L (1979). Metabolism of free fatty acids and ketone bodies during exercise in normal and diabetic man. Diabetes 28(Suppl 1), 66-70.
21. Hajri T, Han XX, Bonen A & Abumrad NA (2002). Defective fatty acid uptake modulates insulin responsiveness and metabolic responses to diet in CD36-null mice. J Clin Invest 109, 1381-1389.
22. Hamilton J, Guo W & Kamp F (2002). Mechanisms of cellular uptake of long-chain fatty acids: Do we need cellular proteins Mol Cell Biochem 239, 17-23.
23. Hermansen L, Hultman E & Saltin B (1967). Muscle glycogen during prolonged severe exercise. Acta Physiol Scand 71, 129-139.
24. Hickson RC, Rennie MJ, Conlee RK, Winder WW & Holloszy JO (1977). Effects of increased plasma fatty acids on glycogen utilization and endurance. J Appl Physiol 43, 829-833.
25. Holloszy JO & Booth FW (1976). Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol 38, 273-291.
26. Holloway GP, Jain SS, Han X-X, Glatz JFC, Luiken JJFP & Bonen A (2009). 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.
27. Huijsman E, van de Par C, Economou C, van der Poel C, Lynch GS, Schoiswohl G, Haemmerle G, Zechner R & Watt MJ (2009). Adipose triacylglycerol lipase deletion alters whole body energy metabolism and impairs exercise performance in mice. Am J Physiol Endocrinol Metab 297, E505-513.
28. Ibrahimi A, Bonen A, Blinn WD, Hajri T, Li X, Zhong K, Cameron R & Abumrad NA (1999). Muscle-specific overexpression of FAT/CD36 enhances fatty acid oxidation by contracting muscles, reduces plasma triglycerides and fatty acids, and increases plasma glucose and insulin. J Biol Chem 274, 26761-26766.
29. Jain SS, Chabowski A, Snook LA, Schwenk RW, Glatz JFC, Luiken JJFP & Bonen A (2009). 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, 2294-2300.
30. Jeppesen J, Albers P, Luiken JJ, Glatz JF & Kiens B (2009). Contractions but not AICAR increase FABPpm content in rat muscle sarcolemma. Mol Cell Biochem 326, 45-53.
31. Jeppesen J, Albers PH, Rose AJ, Birk JB, Schjerling P, Dzamko N, Steinberg GR & Kiens B (2011). Contraction-induced skeletal muscle FAT/CD36 trafficking and FA uptake is AMPK independent. J Lipid Res 52, 699-711.
32. Jeppesen J, Jordy AB, Sjoberg KA, Fullekrug J, Stahl A, Nybo L & Kiens B (2012). Enhanced fatty acid oxidation and FATP4 protein expression after endurance exercise training in human skeletal muscle. PLoS One 7, e29391.
33. Kampf JP & Kleinfeld AM (2007). 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) 22, 7-14.
34. Kampf JP, Kleinfeld AM, Bonen A, Chabowski A, Luiken JJFP & Glatz JFC (2007). Is membrane transport of FFA mediated by lipid, protein, or both?: Points of agreement. Physiology (Bethesda) 22, 29.
35. Kiens B (2006). Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol Rev 86, 205-243.
36. King KL, Stanley WC, Rosca M, Kerner J, Hoppel CL & Febbraio M (2007). Fatty acid oxidation in cardiac and skeletal muscle mitochondria is unaffected by deletion of CD36. Arch Biochem Biophys 467, 234-238.
37. Koonen DPY, Benton CR, Arumugam Y, Tandon NN, Calles-Escandon J, Glatz JFC, Luiken JJFP & Bonen A (2004). Different mechanism can alter fatty acid transport when muscle contractile activity is chronically altered. Am J Physiol Endocrinol Metab 286, 1042-1049.
38. Koves TR, Li P, An J, Akimoto T, Slentz D, Ilkayeva O, Dohm GL, Yan Z, Newgard CB & Muoio DM (2005a). Peroxisome proliferator-activated receptor-γ co-activator 1α-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J Biol Chem 280, 33588-33598.
39. Koves TR, Noland RC, Bates AL, Henes ST, Muoio DM & Cortright RN (2005b). Subsarcolemmal and intermyofibrillar mitochondria play distinct roles in regulating skeletal muscle fatty acid metabolism. Am J Physiol Cell Physiol 288, C1074-1082.
40. Lally JS, Jain SS, Han XX, Snook LA, Glatz JF, Luiken JJ, McFarlan J, Holloway GP & Bonen A (2012). Caffeine-stimulated fatty acid oxidation is blunted in CD36 null mice. Acta Physiol (Oxf) 205, 71-81.
41. 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.
42. Matsuno K, Diaz-Ricard M, Montgomery RR, Aster T, Jamieson GA & Tandon NN (1996). Inhibition of platelet adhesion to collagen by monoclonal anti-CD36 antibodies. Br J Haematol 92, 960-967.
43. McFarlan JT, Yuko Yoshida Y, Jain SS, Han X-X, Snook LA, Lally J, Smith BK, Glatz JFC, Luiken JJFP, Sayer RA, Tupling AR, Chabowski A, Holloway GP & Bonen A (2012). In vivo, fatty acid translocase (CD36) critically regulates skeletal muscle fuel selection, exercise performance and training-induced adaptation of fatty acid oxidation. J Biol Chem 287, 23502-23516.
44. Nickerson JG, Alkhateeb H, Benton CR, Lally J, Nickerson J, Han X-X, Wilson MH, Jain SS, Snook LA, Glatz JFC, Chabowski A, Luiken JJFP & Bonen A (2009). 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.
45. Nilsson LH & Hultman E (1973). Liver glycogen in man - the effect of total starvation or a carbohydrate-poor diet followed by carbohydrate refeeding. Scand J Clin Lab Invest 32, 325-330.
46. Perry CG, Heigenhauser GJ, Bonen A & Spriet LL (2008). High-intensity aerobic interval training increases fat and carbohydrate metabolic capacities in human skeletal muscle. Appl Physiol Nutr Metab 33, 1112-1123.
47. Raney MA & Turcotte LP (2006). Regulation of contraction-induced FA uptake and oxidation by AMPK and ERK1/2 is intensity dependent in rodent muscle. Am J Physiol Endocrinol Metab 291, E1220-1227.
48. Rangwala SM, Wang X, Calvo JA, Lindsley L, Zhang Y, Deyneko G, Beaulieu V, Gao J, Turner G & Markovits J (2010). Estrogen-related receptor gamma is a key regulator of muscle mitochondrial activity and oxidative capacity. J Biol Chem 285, 22619-22629.
49. Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, Endert E & Wolfe RR (1993). Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol Endocrinol Metab 265, E380-E391.
50. Romijn JA, Coyle EF, Sidossis LS, Zhang X-J & Wolfe RR (1995). Relationship between fatty acid delivery and fatty acid oxidation during strenuous exercise. J Appl Physiol 79, 1939-1945.
51. Schenk S & Horowitz JF (2006). Coimmunoprecipitation of FAT/CD36 and CPTI in skeletal muscle increases proportionally with fat oxidation after endurance exercise training. Am J Physiol Endocrinol Metab 291, E254-260.
52. Schoiswohl G, Schweiger M, Schreiber R, Gorkiewicz G, Preiss-Landl K, Taschler U, Zierler KA, Radner FP, Eichmann TO, Kienesberger PC, Eder S, Lass A, Haemmerle G, Alsted TJ, Kiens B, Hoefler G, Zechner R & Zimmermann R (2010). Adipose triglyceride lipase plays a key role in the supply of the working muscle with fatty acids. J Lipid Res 51, 490-499.
53. Sebastian D, Guitart M, Garcia-Martinez C, Mauvezin C, Orellana-Gavalda JM, Serra D, Gomez-Foix AM, Hegardt FG & Asins G (2009). Novel role of FATP1 in mitochondrial fatty acid oxidation in skeletal muscle cells. J Lipid Res 50, 1789-1799.
54. Smith BK, Jain S, Rimbaud S, Dam A, Quadrilatero J, Ventura-Clapier R, Bonen A & Holloway GP (2011). FAT/CD36 is located on the outer mitochondrial membrane, upstream of long chain acyl-CoA synthetase, and regulates palmitate oxidation. Biochem J 437, 125-134.
55. Stefanyk LE, Bonen A & Dyck DJ (2012). Insulin and contraction-induced movement of fatty acid transport proteins to skeletal muscle transverse-tubules is distinctly different than to the sarcolemma. Metabolism (in press).
56. Talanian JL, Holloway GP, Snook LA, Heigenhauser GJ, Bonen A & Spriet LL (2010). Exercise training Increases sarcolemmal and mitochondrial fatty acid transport proteins in human skeletal muscle. Am J Physiol Endocrinol Metab 299, E180-E188.
57. Turcotte LP, Raney MA & Todd MK (2005). 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.
58. van Loon LJ, Greenhaff PL, Constantin-Teodosiu D, Saris WH & Wagenmakers AJ (2001). The effects of increasing exercise intensity on muscle fuel utilisation in humans. J Physiol 536, 295-304.
59. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, Bayuga-Ocampo CR, Ham J, Kang H & Evans RM (2004). Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2, e294.
60. Watt MJ, Heigenhauser GJ & Spriet LL (2002). Intramuscular triacylglycerol utilization in human skeletal muscle during exercise: is there a controversy J Appl Physiol 93, 1185-1195.