Table of Contents
ISRN Obesity
Volume 2012, Article ID 647348, 14 pages
http://dx.doi.org/10.5402/2012/647348
Research Article

Docosahexaenoic Acid Protects Muscle Cells from Palmitate-Induced Atrophy

Division of Exercise Physiology, School of Medicine, West Virginia University, Morgantown, WV 26506-9227, USA

Received 6 July 2012; Accepted 29 August 2012

Academic Editors: K. Abberton and E. Rodríguez Rodríguez

Copyright © 2012 Randall W. Bryner et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Ghosh and B. Rodrigues, “Cardiac cell death in early diabetes and its modulation by dietary fatty acids,” Biochimica et Biophysica Acta, vol. 1761, no. 10, pp. 1148–1162, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. J. A. Houmard, C. J. Tanner, C. Yu et al., “Effect of weight loss on insulin sensitivity and intramuscular long-chain fatty acyl-CoAs in morbidly obese subjects,” Diabetes, vol. 51, no. 10, pp. 2959–2963, 2002. View at Google Scholar · View at Scopus
  3. J. M. Peterson, R. W. Bryner, and S. E. Alway, “Satellite cell proliferation is reduced in muscles of obese Zucker rats but restored with loading,” American Journal of Physiology, vol. 295, no. 2, pp. C521–C528, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. S. A. Warmington, R. Tolan, and S. McBennett, “Functional and histological characteristics of skeletal muscle and the effects of leptin in the genetically obese (ob/ob) mouse,” International Journal of Obesity, vol. 24, no. 8, pp. 1040–1050, 2000. View at Google Scholar · View at Scopus
  5. R. N. Baumgartner, “Body composition in healthy aging,” Annals of the New York Academy of Sciences, vol. 904, pp. 437–448, 2000. View at Google Scholar · View at Scopus
  6. J. S. Lee, S. K. Pinnamaneni, J. E. Su et al., “Saturated, but not n-6 polyunsaturated, fatty acids induce insulin resistance: role of intramuscular accumulation of lipid metabolites,” Journal of Applied Physiology, vol. 100, no. 5, pp. 1467–1474, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. V. Aas, M. H. Rokling-Andersen, E. T. Kase, G. H. Thoresen, and A. C. Rustan, “Eicosapentaenoic acid (20:5 n-3) increases fatty acid and glucose uptake in cultured human skeletal muscle cells,” Journal of Lipid Research, vol. 47, no. 2, pp. 366–374, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Taouis, C. Dagou, C. Ster, G. Durand, M. Pinault, and J. Delarue, “N-3 Polyunsaturated fatty acids prevent the defect of insulin receptor signaling in muscle,” American Journal of Physiology, vol. 282, no. 3, pp. E664–E671, 2002. View at Google Scholar · View at Scopus
  9. E. Montell, M. Turini, M. Marotta et al., “DAG accumulation from saturated fatty acids desensitizes insulin stimulation of glucose uptake in muscle cells,” American Journal of Physiology, vol. 280, no. 2, pp. E229–E237, 2001. View at Google Scholar · View at Scopus
  10. L. H. Storlien, E. W. Kraegen, and D. J. Chisholm, “Fish oil prevents insulin resistance induced by high-fat feeding in rats,” Science, vol. 237, no. 4817, pp. 885–888, 1987. View at Google Scholar · View at Scopus
  11. L. H. Storlien, A. B. Jenkins, D. J. Chisholm, W. S. Pascoe, S. Khouri, and E. W. Kraegen, “Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and ω-3 fatty acids in muscle phospholipid,” Diabetes, vol. 40, no. 2, pp. 280–289, 1991. View at Google Scholar · View at Scopus
  12. V. A. Mustad, S. DeMichele, Y. S. Huang et al., “Differential effects of n-3 polyunsaturated fatty acids on metabolic control and vascular reactivity in the type 2 diabetic ob/ob mouse,” Metabolism, vol. 55, no. 10, pp. 1365–1374, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. Ghafoorunissa, A. Ibrahim, L. Rajkumar, and V. Acharya, “Dietary (n-3) long chain polyunsaturated fatty acids prevent sucrose-induced insulin resistance in rats,” Journal of Nutrition, vol. 135, no. 11, pp. 2634–2638, 2005. View at Google Scholar · View at Scopus
  14. Y. B. Lombardo, G. Hein, and A. Chicco, “Metabolic syndrome: effects of n-3 PUFAs on a model of dyslipidemia, insulin resistance and adiposity,” Lipids, vol. 42, no. 5, pp. 427–437, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. A. S. Rossi, Y. B. Lombardo, J. M. Lacorte et al., “Dietary fish oil positively regulates plasma leptin and adiponectin levels in sucrose-fed, insulin-resistant rats,” American Journal of Physiology, vol. 289, no. 2, pp. R486–R494, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. M. E. D'Alessandro, Y. B. Lombardo, and A. Chicco, “Effect of dietary fish oil on insulin sensitivity and metabolic fate of glucose in the skeletal muscle of normal rats,” Annals of Nutrition and Metabolism, vol. 46, no. 3-4, pp. 114–120, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. A. A. Gingras, P. J. White, P. Y. Chouinard et al., “Long-chain omega-3 fatty acids regulate bovine whole-body protein metabolism by promoting muscle insulin signalling to the Akt-mTOR-S6K1 pathway and insulin sensitivity,” Journal of Physiology, vol. 579, no. 1, pp. 269–284, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. S. D. Clarke, “Polyunsaturated fatty acid regulation of gene transcription: a molecular mechanism to improve the metabolic syndrome,” Journal of Nutrition, vol. 131, no. 4, pp. 1129–1132, 2001. View at Google Scholar · View at Scopus
  19. J. A. Chavez and S. A. Summers, “Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes,” Archives of Biochemistry and Biophysics, vol. 419, no. 2, pp. 101–109, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. J. E. De Vries, M. M. Vork, T. H. M. Roemen et al., “Saturated but not mono-unsaturated fatty acids induce apoptotic cell death in neonatal rat ventricular myocytes,” Journal of Lipid Research, vol. 38, no. 7, pp. 1384–1394, 1997. View at Google Scholar · View at Scopus
  21. R. Mishra and M. S. Simonson, “Saturated free fatty acids and apoptosis in microvascular mesangial cells: palmitate activates pro-apoptotic signaling involving caspase 9 and mitochondrial release of endonuclease G,” Cardiovascular Diabetology, vol. 4, article 2, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Staiger, H. Staiger, C. Weigert, C. Haas, H. U. Häring, and M. Kellerer, “Saturated, but not unsaturated, fatty acids induce apoptosis of human coronary artery endothelial cells via nuclear factor-κB activation,” Diabetes, vol. 55, no. 11, pp. 3121–3126, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. H. J. Welters, M. Tadayyon, J. H. B. Scarpello, S. A. Smith, and N. G. Morgan, “Mono-unsaturated fatty acids protect against β-cell apoptosis induced by saturated fatty acids, serum withdrawal or cytokine exposure,” FEBS Letters, vol. 560, no. 1–3, pp. 103–108, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. M. A. De Pablo, S. A. Susin, E. Jacotot et al., “Palmitate induces apoptosis via a direct effect on mitochondria,” Apoptosis, vol. 4, no. 2, pp. 81–87, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. L. I. Rachek, S. I. Musiyenko, S. P. LeDoux, and G. L. Wilson, “Palmitate induced mitochondrial deoxyribonucleic acid damage and apoptosis in L6 rat skeletal muscle cells,” Endocrinology, vol. 148, no. 1, pp. 293–299, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. J. A. Chavez, T. A. Knotts, L. P. Wang et al., “A role for ceramide, but not diacylglycerol, in the antagonism of insulin signal transduction by saturated fatty acids,” Journal of Biological Chemistry, vol. 278, no. 12, pp. 10297–10303, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Schmitz-Peiffer, D. L. Craig, and T. J. Biden, “Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate,” Journal of Biological Chemistry, vol. 274, no. 34, pp. 24202–24210, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. R. T. Watson and J. E. Pessin, “Bridging the GAP between insulin signaling and GLUT4 translocation,” Trends in Biochemical Sciences, vol. 31, no. 4, pp. 215–222, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Liu, Q. Wan, Q. Guan, L. Gao, and J. Zhao, “High-fat diet feeding impairs both the expression and activity of AMPKa in rats' skeletal muscle,” Biochemical and Biophysical Research Communications, vol. 339, no. 2, pp. 701–707, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. M. A. Iglesias, J.-M. Ye, G. Frangioudakis et al., “AICAR administration causes an apparent enhancement of muscle and liver insulin action in insulin-resistant high-fat-fed rats,” Diabetes, vol. 51, no. 10, pp. 2886–2894, 2002. View at Google Scholar · View at Scopus
  31. M. A. Iglesias, S. M. Furler, G. J. Cooney, E. W. Kraegen, and J. M. Ye, “AMP-activated protein kinase activation by AICAR increases both muscle fatty acid and glucose uptake in white muscle of insulin-resistant rats in vivo,” Diabetes, vol. 53, no. 7, pp. 1649–1654, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. J. S. Fisher, J. Gao, D. H. Han, J. O. Holloszy, and L. A. Nolte, “Activation of AMP kinase enhances sensitivity of muscle glucose transport to insulin,” American Journal of Physiology, vol. 282, no. 1, pp. E18–E23, 2002. View at Google Scholar · View at Scopus
  33. G. S. Olsen and B. F. Hansen, “AMP kinase activation ameliorates insulin resistance induced by free fatty acids in rat skeletal muscle,” American Journal of Physiology, vol. 283, no. 5, pp. E965–E970, 2002. View at Google Scholar · View at Scopus
  34. X. M. Song, M. Fiedler, D. Galuska et al., “5-Aminoimidazole-4-carboxamide ribonucleoside treatment improves glucose homeostasis in insulin-resistant diabetic (ob/ob) mice,” Diabetologia, vol. 45, no. 1, pp. 56–65, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. T. L. Martin, T. Alquier, K. Asakura, N. Furukawa, F. Preitner, and B. B. Kahn, “Diet-induced obesity alters AMP kinase activity in hypothalamus and skeletal muscle,” Journal of Biological Chemistry, vol. 281, no. 28, pp. 18933–18941, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. M. E. D'Alessandro, A. Chicco, L. Karabatas, and Y. B. Lombardo, “Role of skeletal muscle on impaired insulin sensitivity in rats fed a sucrose-rich diet: effect of moderate levels of dietary fish oil,” Journal of Nutritional Biochemistry, vol. 11, no. 5, pp. 273–280, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Simoncíkova, S. Wein, D. Gasperikova et al., “Comparison of the extrapancreatic action of γ-linolenic acid and n-3 PUFAs in the high fat diet-induced insulin resistance,” Endocrine Regulations, vol. 36, no. 4, pp. 143–149, 2002. View at Google Scholar · View at Scopus
  38. A. D. Kinkel, M. E. Fernyhough, D. L. Helterline et al., “Oil red-O stains non-adipogenic cells: a precautionary note,” Cytotechnology, vol. 46, no. 1, pp. 49–56, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. P. A. Srere, “Citrate synthase,” Methods in Enzymology, vol. 13, pp. 3–11, 1969. View at Publisher · View at Google Scholar · View at Scopus
  40. M. J. Ryan, J. R. Jackson, Y. Hao et al., “Suppression of oxidative stress by resveratrol after isometric contractions in gastrocnemius muscles of aged mice,” Journals of Gerontology A, vol. 65, no. 8, pp. 815–831, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Liu, V. E. Baracos, H. A. Quinney, and M. T. Clandinin, “Dietary ω-3 and polyunsaturated fatty acids modify fatty acyl composition and insulin binding in skeletal-muscle sarcolemma,” Biochemical Journal, vol. 299, no. 3, pp. 831–837, 1994. View at Google Scholar · View at Scopus
  42. A. Suzuki, S. Okamoto, S. Lee, K. Saito, T. Shiuchi, and Y. Minokoshi, “Leptin stimulates fatty acid oxidation and peroxisome proliferator- activated receptor α gene expression in mouse C2C12 myoblasts by changing the subcellular localization of the α2 form of amp-activated protein kinase,” Molecular and Cellular Biology, vol. 27, no. 12, pp. 4317–4327, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. W. J. Lee, M. Kim, H. S. Park et al., “AMPK activation increases fatty acid oxidation in skeletal muscle by activating PPARα and PGC-1,” Biochemical and Biophysical Research Communications, vol. 340, no. 1, pp. 291–295, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. R. C. Hresko and M. Mueckler, “mTOR·RICTOR is the Ser473 kinase for Akt/protein kinase B in 3T3-L1 adipocytes,” Journal of Biological Chemistry, vol. 280, no. 49, pp. 40406–40416, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Le Foll, C. Corporeau, V. Le Guen, J. P. Gouygou, J. P. Bergé, and J. Delarue, “Long-chain n-3 polyunsaturated fatty acids dissociate phosphorylation of Akt from phosphatidylinositol 3′-kinase activity in rats,” American Journal of Physiology, vol. 292, no. 4, pp. E1223–E1230, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. J. M. Peterson, Y. Wang, R. W. Bryner, D. L. Williamson, and S. E. Alway, “Bax signaling regulates palmitate-mediated apoptosis in C2C12 myotubes,” American Journal of Physiology, vol. 295, no. 6, pp. E1307–E1314, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. M. A. Sabin, C. E. H. Stewart, E. C. Crowne et al., “Fatty acid-induced defects in insulin signalling, in myotubes derived from children, are related to ceramide production from palmitate rather than the accumulation of intramyocellular lipid,” Journal of Cellular Physiology, vol. 211, no. 1, pp. 244–252, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. N. Dimopoulos, M. Watson, K. Sakamoto, and H. S. Hundal, “Differential effects of palmitate and palmitoleate on insulin action and glucose utilization in rat L6 skeletal muscle cells,” Biochemical Journal, vol. 399, no. 3, pp. 473–481, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. P. Brauner, P. Kopecky, P. Flachs et al., “Expression of uncoupling protein 3 and GLUT4 gene in skeletal muscle of preterm newborns: possible control by AMP-activated protein kinase,” Pediatric Research, vol. 60, no. 5, pp. 569–575, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Delarue, C. LeFoll, C. Corporeau, and D. Lucas, “n-3 long chain polyunsaturated fatty acids: a nutritional tool to prevent insulin resistance associated to type 2 diabetes and obesity?” Reproduction Nutrition Development, vol. 44, no. 3, pp. 289–299, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. B. Viollet, L. Lantier, J. Devin-Leclerc et al., “Targeting the AMPK pathway for the treatment of type 2 diabetes,” Frontiers in Bioscience, vol. 14, no. 9, pp. 3380–3400, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. D. L. Williamson, D. C. Butler, and S. E. Alway, “AMPK inhibits myoblast differentiation through a PGC-1α-dependent mechanism,” American Journal of Physiology, vol. 297, no. 2, pp. E304–E314, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Cantó and J. Auwerx, “PGC-1α, SIRT1 and AMPK, an energy sensing network that controls energy expenditure,” Current Opinion in Lipidology, vol. 20, no. 2, pp. 98–105, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. A. S. Pimenta, M. P. Gaidhu, S. Habib et al., “Prolonged exposure to palmitate impairs fatty acid oxidation despite activation of AMP-activated protein kinase in skeletal muscle cells,” Journal of Cellular Physiology, vol. 217, no. 2, pp. 478–485, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. P. Malenfant, A. Tremblay, É. Doucet, P. Imbeault, J. A. Simoneau, and D. R. Joanisse, “Elevated intramyocellular lipid concentration in obese subjects is not reduced after diet and exercise training,” American Journal of Physiology, vol. 280, no. 4, pp. E632–E639, 2001. View at Google Scholar · View at Scopus
  56. M. Roden, “Muscle triglycerides and mitochondrial function: possible mechanisms for the development of type 2 diabetes,” International Journal of Obesity, vol. 29, supplement 2, pp. S111–S115, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. Z. K. Guo and M. D. Jensen, “Accelerated intramyocellular triglyceride synthesis in skeletal muscle of high-fat-induced obese rats,” International Journal of Obesity, vol. 27, no. 9, pp. 1014–1019, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Timmers, J. De Vogel-Van Den Bosch, M. C. Towler et al., “Prevention of high-fat diet-induced muscular lipid accumulation in rats by α lipoic acid is not mediated by ampk activation,” Journal of Lipid Research, vol. 51, no. 2, pp. 352–359, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. N. P. Hessvik, S. S. Bakke, K. Fredriksson et al., “Metabolic switching of human myotubes is improved by n-3 fatty acids,” Journal of Lipid Research, vol. 51, no. 8, pp. 2090–2104, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Kelly, M. S. Gauthier, A. K. Saha, and N. B. Ruderman, “Activation of AMP-activated protein kinase by interleukin-6 in rat skeletal muscle: association with changes in cAMP, energy state, and endogenous fuel mobilization,” Diabetes, vol. 58, no. 9, pp. 1953–1960, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Vaarmann, D. Fortin, V. Veksler, I. Momken, R. Ventura-Clapier, and A. Garnier, “Mitochondrial biogenesis in fast skeletal muscle of CK deficient mice,” Biochimica et Biophysica Acta, vol. 1777, no. 1, pp. 39–47, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Sandri, J. Lin, C. Handschin et al., “PGC-1α protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 44, pp. 16260–16265, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. T. Wenz, S. G. Rossi, R. L. Rotundo, B. M. Spiegelman, and C. T. Moraes, “Increased muscle PGC-1α expression protects from sarcopenia and metabolic disease during aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 48, pp. 20405–20410, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. N. Turner, C. R. Bruce, S. M. Beale 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, vol. 56, no. 8, pp. 2085–2092, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. G. P. Holloway, C. R. Benton, K. L. Mullen et al., “In obese rat muscle transport of palmitate is increased and is channeled to triacylglycerol storage despite an increase in mitochondrial palmitate oxidation,” American Journal of Physiology, vol. 296, no. 4, pp. E738–E747, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. T. R. Koves, P. Li, J. An et al., “Peroxisome proliferator-activated receptor-γ co-activator 1α-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency,” Journal of Biological Chemistry, vol. 280, no. 39, pp. 33588–33598, 2005. View at Publisher · View at Google Scholar · View at Scopus