Table of Contents Author Guidelines Submit a Manuscript
Erratum

An erratum for this article has been published. To view the erratum, please click here.

Biochemistry Research International
Volume 2012 (2012), Article ID 714074, 12 pages
http://dx.doi.org/10.1155/2012/714074
Research Article

Overexpression of PGC-1α Increases Fatty Acid Oxidative Capacity of Human Skeletal Muscle Cells

1Department of Pharmaceutical Biosciences, School of Pharmacy, University of Oslo, P.O. Box 1068 Blindern, N-0316 Oslo, Norway
2AstraZeneca Reseach and Development, SE-43185 Mölndal, Sweden
3Boden Institute of Obesity, Nutrition and Exercise, University of Sydney, Sydney, NSW 2006, Australia

Received 15 April 2011; Accepted 29 June 2011

Academic Editor: Paul Denny

Copyright © 2012 Nataša Nikolić 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. J. C. Clapham and L. H. Storlien, “The fatty acid oxidation pathway as a therapeutic target for insulin resistance,” Expert Opinion on Therapeutic Targets, vol. 10, no. 5, pp. 749–757, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Puigserver, Z. Wu, C. W. Park et al., “A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis,” Cell, vol. 92, no. 6, pp. 829–839, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Puigserver and B. M. Spiegelman, “Peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α): transcriptional coactivator and metabolic regulator,” Endocrine Reviews, vol. 24, no. 1, pp. 78–90, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Lin, C. Handschin, and B. M. Spiegelman, “Metabolic control through the PGC-1 family of transcription coactivators,” Cell Metabolism, vol. 1, no. 6, pp. 361–370, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. A. J. Gilde and M. Van Bilsen, “Peroxisome proliferator-activated receptors (PPARS): regulators of gene expression in heart and skeletal muscle,” Acta Physiologica Scandinavica, vol. 178, no. 4, pp. 425–434, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Herzig, F. Long, U. S. Jhala et al., “CREB regulates hepatic gluconeogenesis through the coactivator PGC-1,” Nature, vol. 413, pp. 179–183, 2001. View at Google Scholar · View at Scopus
  7. J. Rhee, Y. Inoue, J. C. Yoon et al., “Regulation of hepatic fasting response by PPARγ coactivator-1α (PGC-1): requirement for hepatocyte nuclear factor 4α in gluconeogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 7, pp. 4012–4017, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. J. J. Lehman, P. M. Barger, A. Kovacs et al., “Peroxisome proliferator-activated receptor ? coactivator-1 promotes cardiac mitochondrial biogenesis,” Journal of Clinical Investigation, vol. 106, no. 7, pp. 847–856, 2000. View at Google Scholar · View at Scopus
  9. T. C. Leone, J. J. Lehman, B. N. Finck et al., “PGC-1α deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis,” PLoS Biology, vol. 3, no. 4, Article ID e101, 2005. View at Google Scholar
  10. K. Baar, A. R. Wende, T. E. Jones et al., “Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1,” The FASEB Journal, vol. 16, no. 14, pp. 1879–1886, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Goto, S. Terada, M. Kato et al., “CDNA cloning and mRNA analysis of PGC-1 in epitrochlearis muscle in swimming-exercised rats,” Biochemical and Biophysical Research Communications, vol. 274, no. 2, pp. 350–354, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Terada, M. Goto, M. Kato et al., “Effects of low-intensity prolonged exercise on PGC-1 mRNA expression in rat epitrochlearis muscle,” Biochemical and Biophysical Research Communications, vol. 296, no. 2, pp. 350–354, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Pilegaard, B. Saltin, and P. D. Neufer, “Exercise induces transient transcriptional activation of the PGC-1α gene in human skeletal muscle,” Journal of Physiology, vol. 546, no. 3, pp. 851–858, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. I. Irrcher, P. J. Adhihetty, T. Sheehan et al., “PPAR? coactivator-1a expression during thyroid hormone—and contractile activity-induced mitochondrial adaptations,” American Journal of Physiology, vol. 284, no. 6, pp. C1669–C1677, 2003. View at Google Scholar · View at Scopus
  15. J. P. Little, A. Safdar, N. Cermak et al., “Acute endurance exercise increases the nuclear abundance of PGC-1a in trained human skeletal muscle,” American Journal of Physiology, vol. 298, no. 4, pp. R912–R917, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Lin, H. Wu, P. T. Tarr et al., “Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres,” Nature, vol. 418, no. 6899, pp. 797–801, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. V. K. Mootha, C. Handschin, D. Arlow et al., “Errα and gabpa/b specify pgc-1α-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 17, pp. 6570–6575, 2004. View at Google Scholar
  18. F. W. Booth and D. B. Thomason, “Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models,” Physiological Reviews, vol. 71, no. 2, pp. 541–585, 1991. View at Google Scholar · View at Scopus
  19. C. Handschin, S. Chin, P. Li et al., “Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1α muscle-specific knock-out animals,” Journal of Biological Chemistry, vol. 282, no. 41, pp. 30014–30021, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. O. H. Mortensen, L. Frandsen, P. Schjerling et al., “PGC-1a and PGC-1ß have both similar and distinct effects on myofiber switching toward an oxidative phenotype,” American Journal of Physiology, vol. 291, no. 4, pp. E807–E816, 2006. View at Google Scholar
  21. C. R. Benton, G. P. Holloway, X. X. Han et al., “Increased levels of peroxisome proliferator-activated receptor gamma, 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, vol. 53, no. 9, pp. 2008–2019, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. C. R. Benton, J. G. Nickerson, J. Lally et al., “Modest PGC-1α overexpression in muscle in vivo is sufficient to increase insulin sensitivity and palmitate oxidation in subsarcolemmal, not intermyofibrillar, mitochondria,” Journal of Biological Chemistry, vol. 283, no. 7, pp. 4228–4240, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Liang, B. Balas, P. Tantiwong et al., “Whole body overexpression of PGC-1a has opposite effects on hepatic and muscle insulin sensitivity,” American Journal of Physiology, vol. 296, no. 4, pp. E945–E954, 2009. View at Google Scholar
  24. L. F. Michael, Z. Wu, R. B. Cheatham et al., “Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 7, pp. 3820–3825, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. X. Wang, C. H. Lee, S. Tiep et al., “Peroxisome-proliferator-activated receptor Δ activates fat metabolism to prevent obesity,” Cell, vol. 113, no. 2, pp. 159–170, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. D. C. Wright, P. C. Geiger, D. H. Han et al., “Calcium induces increases in peroxisome proliferator-activated receptor ? coactivator-1a and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation,” Journal of Biological Chemistry, vol. 282, no. 26, pp. 18793–18799, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. X. Wang, C. L. Zhang, R. T. Yu et al., “Regulation of muscle fiber type and running endurance by PPARΔ,” PLoS Biology, vol. 2, no. 10, Article ID e294, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Luquet, J. Lopez-Soriano, D. Holst et al., “Roles of peroxisome proliferator-activated receptor Δ (PPARΔ) in the control of fatty acid catabolism. A new target for the treatment of metabolic syndrome,” Biochimie, vol. 86, no. 11, pp. 833–837, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. V. Sarabia, L. Lam, E. Burdett et al., “Glucose transport in human skeletal muscle cells in culture. Stimulation by insulin and metformin,” Journal of Clinical Investigation, vol. 90, no. 4, pp. 1386–1395, 1992. View at Google Scholar · View at Scopus
  30. B. Ukropcova, M. McNeil, O. Sereda et al., “Dynamic changes in fat oxidation in human primary myocytes mirror metabolic characteristics of the donor,” Journal of Clinical Investigation, vol. 115, no. 7, pp. 1934–1941, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. 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
  32. N. Gleyzer, K. Vercauteren, and R. C. Scarpulla, “Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators,” Molecular and Cellular Biology, vol. 25, no. 4, pp. 1354–1366, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. D. P. Kelly and R. C. Scarpulla, “Transcriptional regulatory circuits controlling mitochondrial biogenesis and function,” Genes and Development, vol. 18, no. 4, pp. 357–368, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. J. R. Crew, K. Falzari, and J. X. DiMario, “Muscle fiber type specific induction of slow myosin heavy chain 2 gene expression by electrical stimulation,” Experimental Cell Research, vol. 316, no. 6, pp. 1039–1049, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. L. A. Consitt, J. A. Bell, T. R. Koves et al., “Peroxisome proliferator-activated receptor-γ coactivator-1α overexpression increases lipid oxidation in myocytes from extremely obese individuals,” Diabetes, vol. 59, no. 6, pp. 1407–1415, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. R. R. Henry, L. Abrams, S. Nikoulina et al., “Insulin action and glucose metabolism in nondiabetic control and NIDDM subjects. Comparison using human skeletal muscle cell cultures,” Diabetes, vol. 44, no. 8, pp. 936–946, 1995. View at Google Scholar · View at Scopus
  37. M. Gaster, H. Beck-Nielsen, and H. D. Schroder, “Proliferation conditions for human satellite cells. The fractional content of satellite cells,” Acta Pathologica Microbiologica et Immunologica Scandinavica, vol. 109, no. 11, pp. 726–734, 2001. View at Google Scholar · View at Scopus
  38. S. Skrede, P. Wu, and J. Bremer, “Tetradecylthioacrylic acid, a β-oxidation metabolite of tetradecylthiopropionic acid, inhibits fatty acid activation and oxidation in rat,” World Review of Nutrition and Dietetics, vol. 75, pp. 30–34, 1994. View at Google Scholar · View at Scopus
  39. J. Franch, R. Aslesen, and J. Jensen, “Regulation of glycogen synthesis in rat skeletal muscle after glycogen-depleting contractile activity: effects of adrenaline on glycogen synthesis and activation of glycogen synthase and glycogen phosphorylase,” Biochemical Journal, vol. 344, part 1, pp. 231–235, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. M. L. Sznaidman, C. D. Haffner, P. R. Maloney et al., “Novel selective small molecule agonists for peroxisome proliferator-activated receptor ? (PPAR?)—synthesis and biological activity,” Bioorganic & Medicinal Chemistry Letters, vol. 13, no. 9, pp. 1517–1521, 2003. View at Google Scholar
  41. C. C. Ciocoiu, N. Nikolic, H. H. Nguyen et al., “Synthesis and dual PPARa/? agonist effects of 1,4-disubstituted 1,2,3-triazole analogues of GW 501516,” European Journal of Medicinal Chemistry, vol. 45, no. 7, pp. 3047–3055, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. T. J. Alsted, L. Nybo, M. Schweiger et al., “Adipose triglyceride lipase in human skeletal muscle is upregulated by exercise training,” American Journal of Physiology, vol. 296, no. 3, pp. E445–E453, 2009. View at Google Scholar
  43. J. W. Helge, T. O. Biba, H. Galbo et al., “Muscle triacylglycerol and hormone-sensitive lipase activity in untrained and trained human muscles,” European Journal of Applied Physiology, vol. 97, no. 5, pp. 566–572, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. J. W. Jocken, E. Smit, G. H. Goossens et al., “Adipose triglyceride lipase (ATGL) expression in human skeletal muscle is type I (oxidative) fiber specific,” Histochemistry and Cell Biology, vol. 129, no. 4, pp. 535–538, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. D. A. Hood, I. Irrcher, V. Ljubicic et al., “Coordination of metabolic plasticity in skeletal muscle,” Journal of Experimental Biology, vol. 209, no. 12, pp. 2265–2275, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. D. A. Hood, “Invited review: contractile activity-induced mitochondrial biogenesis in skeletal muscle,” Journal of Applied Physiology, vol. 90, no. 3, pp. 1137–1157, 2001. View at Google Scholar · View at Scopus
  47. M. A. Tarnopolsky, C. D. Rennie, H. A. Robertshaw et al., “Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity,” American Journal of Physiology, vol. 292, no. 3, pp. R1271–R1278, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. G. S. Shadel and D. A. Clayton, “Mitochondrial transcription initiation. Variation and conservation,” Journal of Biological Chemistry, vol. 268, no. 22, pp. 16083–16086, 1993. View at Google Scholar · View at Scopus
  49. S. Lee, H. Van Remmen, and M. Csete, “Sod2 overexpression preserves myoblast mitochondrial mass and function, but not muscle mass with aging,” Aging Cell, vol. 8, no. 3, pp. 296–310, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Kleiner, V. Nguyen-Tran, O. Bare et al., “PPAR? agonism activates fatty acid oxidation via PGC-1a but does not increase mitochondrial gene expression and function,” Journal of Biological Chemistry, vol. 284, no. 28, pp. 18624–18633, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Al-Khalili, G. D. Cartee, and A. Krook, “Rna interference-mediated reduction in GLUT1 inhibits serum-induced glucose transport in primary human skeletal muscle cells,” Biochemical and Biophysical Research Communications, vol. 307, no. 1, pp. 127–132, 2003. View at Google Scholar
  52. M. Gaster, A. Handberg, A. Schurmann et al., “GLUT11, but not GLUT8 or GLUT12, is expressed in human skeletal muscle in a fibre type-specific pattern,” Pflugers Archiv European Journal of Physiology, vol. 448, no. 1, pp. 105–113, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. E. T. Kase, G. H. Thoresen, S. Westerlund et al., “Liver X receptor antagonist reduces lipid formation and increases glucose metabolism in myotubes from lean, obese and type 2 diabetic individuals,” Diabetologia, vol. 50, no. 10, pp. 2171–2180, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. E. T. Kase, A. J. Wensaas, V. Aas et al., “Skeletal muscle lipid accumulation in type 2 diabetes may involve the liver X receptor pathway,” Diabetes, vol. 54, no. 4, pp. 1108–1115, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. L. L. Tortorella and P. F. Pilch, “C2C12 myocytes lack an insulin-responsive vesicular compartment despite dexamethasone-induced GLUT4 expression,” American Journal of Physiology, vol. 283, no. 3, pp. E514–E524, 2002. View at Google Scholar
  56. S. Lillioja, A. A. Young, C. L. Culter et al., “Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man,” Journal of Clinical Investigation, vol. 80, no. 2, pp. 415–424, 1987. View at Google Scholar · View at Scopus
  57. A. D. Kriketos, D. A. Pan, S. Lillioja et al., “Interrelationships between muscle morphology, insulin action, and adiposity,” American Journal of Physiology, vol. 270, no. 6, pp. R1332–R1339, 1996. View at Google Scholar · View at Scopus