Enhanced fatty acid oxidation and FATP4 protein expression after endurance exercise training in human skeletal muscle

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Jeppesen, Jacob ^a   Jordy, Andreas B ^a   Sjøberg, Kim A ^a   Füllekrug, Joachim ^b   Stahl, Andreas ^c   Nybo, Lars ^a   Kiens, Bente ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CITRATE SYNTHASE; FATTY ACID TRANSPORTER; FATTY ACID TRANSPORTER 1; FATTY ACID TRANSPORTER 4; UNCLASSIFIED DRUG; FATTY ACID; SLC27A1 PROTEIN, HUMAN; SLC27A4 PROTEIN, HUMAN;

ADULT; AEROBIC EXERCISE; ARTICLE; ENDURANCE TRAINING; ENZYME ACTIVITY; FATTY ACID OXIDATION; HUMAN; HUMAN EXPERIMENT; MALE; MUSCLE LEVEL; NORMAL HUMAN; OXYGEN CONSUMPTION; PHYSICAL ACTIVITY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE; CHEMISTRY; DIET; ENDURANCE; EXERCISE; GENE EXPRESSION REGULATION; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ADULT; DIET; EXERCISE; FATTY ACID TRANSPORT PROTEINS; FATTY ACIDS; GENE EXPRESSION REGULATION; HUMANS; MALE; MUSCLE, SKELETAL; OXIDATION-REDUCTION; PHYSICAL ENDURANCE;

EID: 84855318221     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029391     Document Type: Article

References (59)

1. Stremmel W, Lotz G, Strohmeyer G, Berk PD, (1985) Identification, isolation, and partial characterization of a fatty acid binding protein from rat jejunal microvillous membranes. J Clin Invest 75: 1068-1076.
2. Gimeno RE, Hirsch DJ, Punreddy S, Sun Y, Ortegon AM, et al. (2003) Targeted deletion of fatty acid transport protein-4 results in early embryonic lethality. J Biol Chem 278: 49512-49516.
3. Hirsch D, Stahl A, Lodish HF, (1998) A family of fatty acid transporters conserved from mycobacterium to man. Proc Natl Acad Sci USA 95: 8625-8629.
4. Schaffer JE, Lodish HF, (1994) Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 79: 427-436.
5. Nickerson JG, Alkhateeb H, Benton CR, Lally J, Nickerson J, et al. (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.
6. 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.
7. Kleine AH, Glatz JF, van Nieuwenhoven FA, Vallinga MI, Salden MH, et al. (1990) Type-specific immunodetection of human heart fatty acid-binding protein with polyclonal anti-peptide antibodies. Mol Cell Biochem 98: 41-48.
8. Faergeman NJ, Knudsen J, (1997) Role of long-chain fatty acyl-CoA esters in the regulation of metabolism and in cell signalling. Biochem J 323 (Pt 1): 1-12.
9. Binas B, Han XX, Erol E, Luiken JJ, Glatz JF, et al. (2003) A null mutation in H-FABP only partially inhibits skeletal muscle fatty acid metabolism. Am J Physiol Endocrinol Metab 285: E481-E489.
10. Luiken JJ, Koonen DP, Coumans WA, Pelsers MM, Binas B, et al. (2003) Long-chain fatty acid uptake by skeletal muscle is impaired in homozygous, but not heterozygous, heart-type-FABP null mice. Lipids 38: 491-496.
11. Neess D, Bloksgaard M, Bek S, Marcher AB, Elle IC, et al. (2010) Disruption of the Acyl-CoA-binding Protein Gene Delays Hepatic Adaptation to Metabolic Changes at Weaning. J Biol Chem 286: 3460-3472.
12. Schubert W, Frank PG, Razani B, Park DS, Chow CW, et al. (2001) Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J Biol Chem 276: 48619-48622.
13. Song KS, Scherer PE, Tang Z, Okamoto T, Li S, et al. (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.
14. Pohl J, Ring A, Ehehalt R, Herrmann T, Stremmel W, (2004) New concepts of cellular fatty acid uptake: role of fatty acid transport proteins and of caveolae. Proc Nutr Soc 63: 259-262.
15. Pohl J, Ring A, Ehehalt R, Schulze-Bergkamen H, Schad A, et al. (2004) Long-chain fatty acid uptake into adipocytes depends on lipid raft function. Biochemistry 43: 4179-4187.
16. Kiens B, Kristiansen S, Jensen P, Richter EA, Turcotte LP, (1997) Membrane associated fatty acid binding protein (FABPpm) in human skeletal muscle is increased by endurance training. Biochem Biophys Res Commun 231: 463-465.
17. Bonen A, Miskovic D, Kiens B, (1999) Fatty acid transporters (FABPpm, FAT, FATP) in human muscle. Can J Appl Physiol 24: 515-523.
18. Vistisen B, Roepstorff K, Roepstorff C, Bonen A, van Deurs B, et al. (2004) Sarcolemmal FAT/CD36 in human skeletal muscle colocalizes with caveolin-3 and is more abundant in type 1 than in type 2 fibers. J Lipid Res 45: 603-609.
19. Kiens B, Roepstorff C, Glatz JF, Bonen A, Schjerling P, et al. (2004) Lipid-binding proteins and lipoprotein lipase activity in human skeletal muscle: influence of physical activity and gender. J Appl Physiol 97: 1209-1218.
20. Talanian JL, Galloway SD, Heigenhauser GJ, Bonen A, Spriet LL, (2006) TWO WEEKS OF HIGH-INTENSITY AEROBIC INTERVAL TRAINING INCREASES THE CAPACITY FOR FAT OXIDATION DURING EXERCISE IN WOMEN. J Appl Physiol.
21. Talanian JL, Holloway GP, Snook LA, Heigenhauser GJ, Bonen A, et al. (2010) EXERCISE TRAINING INCREASES SARCOLEMMAL AND MITOCHONDRIAL FATTY ACID TRANSPORT PROTEINS IN HUMAN SKELETAL MUSCLE. Am J Physiol Endocrinol Metab.
22. Jain SS, Chabowski A, Snook LA, Schwenk RW, Glatz JF, et al. (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.
23. Wu Q, Ortegon AM, Tsang B, Doege H, Feingold KR, et al. (2006) FATP1 is an insulin-sensitive fatty acid transporter involved in diet-induced obesity. Mol Cell Biol 26: 3455-3467.
24. Lewis SE, Listenberger LL, Ory DS, Schaffer JE, (2001) Membrane topology of the murine fatty acid transport protein 1. J Biol Chem 276: 37042-37050.
25. Milger K, Herrmann T, Becker C, Gotthardt D, Zickwolf J, et al. (2006) Cellular uptake of fatty acids driven by the ER-localized acyl-CoA synthetase FATP4. J Cell Sci 119: 4678-4688.
26. Stahl A, Gimeno RE, Tartaglia LA, Lodish HF, (2001) Fatty acid transport proteins: a current view of a growing family. Trends Endocrinol Metab 12: 266-273.
27. Stahl A, (2004) A current review of fatty acid transport proteins (SLC27). Pflugers Arch 447: 722-727.
28. Hall AM, Smith AJ, Bernlohr DA, (2003) Characterization of the Acyl-CoA synthetase activity of purified murine fatty acid transport protein 1. J Biol Chem 278: 43008-43013.
29. Herrmann T, Buchkremer F, Gosch I, Hall AM, Bernlohr DA, et al. (2001) Mouse fatty acid transport protein 4 (FATP4): characterization of the gene and functional assessment as a very long chain acyl-CoA synthetase. Gene 270: 31-40.
30. Tunstall RJ, Mehan KA, Wadley GD, Collier GR, Bonen A, et al. (2002) Exercise training increases lipid metabolism gene expression in human skeletal muscle. Am J Physiol Endocrinol Metab 283: E66-E72.
31. Roepstorff C, Helge JW, Vistisen B, Kiens B, (2004) Studies of plasma membrane fatty acid-binding protein and other lipid-binding proteins in human skeletal muscle. Proc Nutr Soc 63: 239-244.
32. Turcotte LP, Richter EA, Kiens B, (1992) Increased plasma FFA uptake and oxidation during prolonged exercise in trained vs. untrained humans. Am J Physiol 262: E791-E799.
33. Kiens B, Essen-Gustavsson B, Christensen NJ, Saltin B, (1993) Skeletal muscle substrate utilization during submaximal exercise in man: effect of endurance training. J Physiol 469: 459-478.
34. Kiens B, (1997) Effect of endurance training on fatty acid metabolism: local adaptations. Med Sci Sports Exerc 29: 640-645.
35. Stellingwerff T, Boon H, Jonkers RA, Senden JM, Spriet LL, et al. (2007) Significant intramyocellular lipid use during prolonged cycling in endurance trained males as assessed by three different methodologies. Am J Physiol Endocrinol Metab.
36. Svedenhag J, Lithell H, Juhlin-Dannfelt A, Henriksson J, (1983) Increase in skeletal muscle lipoprotein lipase following endurance training in man. Atherosclerosis 49: 203-207.
37. Kiens B, Lithell H, (1989) Lipoprotein metabolism influenced by training-induced changes in human skeletal muscle. J Clin Invest 83: 558-564.
38. Alsted TJ, Nybo L, Schweiger M, Fledelius C, Jacobsen P, et al. (2009) Adipose triglyceride lipase in human skeletal muscle is upregulated by exercise training. Am J Physiol Endocrinol Metab 296: E445-E453.
39. Yao-Borengasser A, Varma V, Coker RH, Ranganathan G, Phanavanh B, et al. (2010) Adipose triglyceride lipase expression in human adipose tissue and muscle. Role in insulin resistance and response to training and pioglitazone. Metabolism.
40. Nybo L, Pedersen K, Christensen B, Aagaard P, Brandt N, et al. (2009) Impact of carbohydrate supplementation during endurance training on glycogen storage and performance. Acta Physiol (Oxf) 197: 117-127.
41. Friedlander AL, Casazza GA, Horning MA, Huie MJ, Piacentini MF, et al. (1998) Training-induced alterations of carbohydrate metabolism in women: women respond differently from men. J Appl Physiol 85: 1175-1186.
42. Passonneau JV, Gatfield PD, Schulz DW, Lowry OH, (1967) An enzymic method for measurement of glycogen. Anal Biochem 19: 315-326.
43. Kiens B, Richter EA, (1996) Types of carbohydrate in an ordinary diet affect insulin action and muscle substrates in humans. Am J Clin Nutr 63: 47-53.
44. Lowry CV, Kimmey JS, Felder S, Chi MM, Kaiser KK, et al. (1978) Enzyme patterns in single human muscle fibers. J Biol Chem 253: 8269-8277.
45. Wu Q, Kazantzis M, Doege H, Ortegon AM, Tsang B, et al. (2006) Fatty acid transport protein 1 is required for nonshivering thermogenesis in brown adipose tissue. Diabetes 55: 3229-3237.
46. Lobo S, Bernlohr DA, (2007) Fatty acid transport in adipocytes and the development of insulin resistance. Novartis Found Symp 286: 113-121.
47. 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.
48. Kim JK, Gimeno RE, Higashimori T, Kim HJ, Choi H, et al. (2004) Inactivation of fatty acid transport protein 1 prevents fat-induced insulin resistance in skeletal muscle. J Clin Invest 113: 756-763.
49. Lobo S, Wiczer BM, Smith AJ, Hall AM, Bernlohr DA, (2007) Fatty acid metabolism in adipocytes: functional analysis of fatty acid transport proteins 1 and 4. Journal of Lipid Research 48: 609-620.
50. Wiczer BM, Bernlohr DA, (2009) A novel role for fatty acid transport protein 1 in the regulation of tricarboxylic acid cycle and mitochondrial function in 3T3-L1 adipocytes. J Lipid Res 50: 2502-2513.
51. Sebastian D, Guitart M, Garcia-Martinez C, Mauvezin C, Orellana-Gavalda JM, et al. (2009) Novel role of FATP1 in mitochondrial fatty acid oxidation in skeletal muscle cells. J Lipid Res 50: 1789-1799.
52. Guitart M, Andreu AL, Garcia-Arumi E, Briones P, Quintana E, et al. (2009) FATP1 localizes to mitochondria and enhances pyruvate dehydrogenase activity in skeletal myotubes. Mitochondrion 9: 266-272.
53. Hagberg CE, Falkevall A, Wang X, Larsson E, Huusko J, et al. (2010) Vascular endothelial growth factor B controls endothelial fatty acid uptake. Nature 464: 917-921.
54. Watkins PA, Lu JF, Steinberg SJ, Gould SJ, Smith KD, et al. (1998) Disruption of the Saccharomyces cerevisiae FAT1 gene decreases very long-chain fatty acyl-CoA synthetase activity and elevates intracellular very long-chain fatty acid concentrations. J Biol Chem 273: 18210-18219.
55. Watkins PA, Lu JF, Braiterman LT, Steinberg SJ, Smith KD, (2000) Disruption of a yeast very-long-chain acyl-CoA synthetase gene simulates the cellular phenotype of X-linked adrenoleukodystrophy. Cell Biochem Biophys 32 Spring: 333-337.
56. Schiaffino S, Reggiani C, (2011) Fiber types in Mammalian skeletal muscles. Physiol Rev 91: 1447-1531.
57. Roepstorff C, Vistisen B, Roepstorff K, Kiens B, (2004) Regulation of plasma long-chain fatty acid oxidation in relation to uptake in human skeletal muscle during exercise. Am J Physiol Endocrinol Metab 287: E696-E705.
58. Bonen A, Dyck DJ, Ibrahimi A, Abumrad NA, (1999) Muscle contractile activity increases fatty acid metabolism and transport and FAT/CD36. Am J Physiol 276: E642-649.
59. Benton CR, Koonen DP, Calles-Escandon J, Tandon NN, Glatz JF, et al. (2006) Differential effects of contraction and PPAR agonists on the expression of fatty acid transporters in rat skeletal muscle. J Physiol 573: 199-210.