Table of Contents
New Journal of Science
Volume 2014, Article ID 635146, 21 pages
http://dx.doi.org/10.1155/2014/635146
Review Article

Genetic Dissection of the Physiological Role of Skeletal Muscle in Metabolic Syndrome

Department of Internal Medicine, Division of Cardiovascular Medicine, University of California, Davis, CA 95616, USA

Received 18 May 2014; Accepted 6 August 2014; Published 19 August 2014

Academic Editor: Hui-Qi Qu

Copyright © 2014 Nobuko Hagiwara. 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. D. E. King, E. Matheson, S. Chirina, A. Shankar, and J. Broman-Fulks, “The status of baby boomers' health in the United States: the healthiest generation?” JAMA Internal Medicine, vol. 173, no. 5, pp. 385–386, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. S. M. Grundy, H. B. Brewer Jr., J. I. Cleeman, S. C. Smith Jr., and C. Lenfant, “Definition of metabolic syndrome report of the National Heart, Lung, and Blood Institute/American Heart Association Conference on scientific issues related to definition,” Circulation, vol. 109, no. 3, pp. 433–438, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Alberti and P. Zimmet, “Definition, diagnosis and classification of diabetes mellitus provisional report of a WHO consultation,” Diabetic Medicine, vol. 15, no. 7, pp. 539–553, 1998. View at Google Scholar
  4. E. Kassi, P. Pervanidou, G. Kaltsas, and G. Chrousos, “Metabolic syndrome: definitions and controversies,” BMC Medicine, vol. 9, article 48, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Espeland, X. Pi-Sunyer, G. Blackburn et al., “Reduction in weight and cardiovascular disease risk factors in individuals with type 2 diabetes one-year results of the look AHEAD trial,” Diabetes Care, vol. 30, no. 6, pp. 1374–1383, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. R. R. Wing, P. Bolin, F. L. Brancati et al., “Cardiovascular effects of intensive lifestyle intervention in type 2 diabetes,” The New England Journal of Medicine, vol. 369, no. 2, pp. 145–154, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. Ameircan Diabetes Association, “Standards of medical care in diabetes—2014,” Diabetes Care, vol. 37, supplement 1, pp. S14–S80, 2014. View at Google Scholar
  8. H. N. Ginsberg, “Insulin resistance and cardiovascular disease,” Journal of Clinical Investigation, vol. 106, no. 4, pp. 453–458, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. A. D. Baron, G. Brechtel, P. Wallace, and S. V. Edelman, “Rates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humans,” American Journal of Physiology. Endocrinology and Metabolism, vol. 255, no. 6, pp. E769–E774, 1988. View at Google Scholar · View at Scopus
  10. D. Thiebaud, E. Jacot, R. A. DeFronzo, E. Maeder, E. Jequier, and J. P. Felber, “The effect of graded doses of insulin on total glucose uptake, glucose oxidation, and glucose storage in man,” Diabetes, vol. 31, no. 11, pp. 957–963, 1982. View at Publisher · View at Google Scholar · View at Scopus
  11. K. F. Petersen, S. Dufour, D. B. Savage et al., “The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 31, pp. 12587–12594, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Schiaffino, “Fibre types in skeletal muscle: a personal account,” Acta Physiologica, vol. 199, no. 4, pp. 451–463, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. J. R. Zierath and J. A. Hawley, “Skeletal muscle fiber type: influence on contractile and metabolic properties,” PLoS Biology, vol. 2, no. 10, Article ID e348, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Ranvier, “Propriétés et structures différentes des muscles rouges et des muscles blancs chez les lapins et chez les raies,” CR Acad Sci Paris, vol. 77, pp. 1030–1034, 1873. View at Google Scholar
  15. D. M. Needam, “Red ans white muscle,” Physiological Reviews, vol. 6, no. 1, pp. 1–27, 1926. View at Google Scholar
  16. M. Bárány, “ATPase activity of myosin correlated with speed of muscle shortening,” The Journal of General Physiology, vol. 50, no. 6, pp. 197–218, 1967. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Schiaffino, V. Hanzlíková, and S. Pierobon, “Relations between structure and function in rat skeletal muscle fibers.,” Journal of Cell Biology, vol. 47, no. 1, pp. 107–119, 1970. View at Publisher · View at Google Scholar · View at Scopus
  18. G. J. M. Stienen, J. L. Kiers, R. Bottinelli, and C. Reggiani, “Myofibrillar ATPase activity in skinned human skeletal muscle fibres: fibre type and temperature dependence,” Journal of Physiology, vol. 493, part 2, pp. 299–307, 1996. View at Google Scholar · View at Scopus
  19. L. Larsson and R. L. Moss, “Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles,” Journal of Physiology, vol. 472, pp. 595–614, 1993. View at Google Scholar · View at Scopus
  20. R. S. Staron, “Correlation between myofibrillar ATPase activity and myosin heavy chain composition in single human muscle fibers,” Histochemistry, vol. 96, no. 1, pp. 21–24, 1991. View at Publisher · View at Google Scholar · View at Scopus
  21. J. B. Peter, R. J. Barnard, V. R. Edgerton, C. A. Gillespie, and K. E. Stempel, “Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits,” Biochemistry, vol. 11, no. 14, pp. 2627–2633, 1972. View at Publisher · View at Google Scholar · View at Scopus
  22. B. C. Harrison, D. L. Allen, B. Girten et al., “Skeletal muscle adaptations to microgravity exposure in the mouse,” Journal of Applied Physiology, vol. 95, no. 6, pp. 2462–2470, 2003. View at Google Scholar · View at Scopus
  23. D. Sandonà, J. Desaphy, G. M. Camerino et al., “Adaptation of mouse skeletal muscle to long-term microgravity in the MDS mission,” PLoS ONE, vol. 7, no. 3, Article ID e33232, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Trappe, T. Trappe, P. Gallagher, M. Harber, B. Alkner, and P. Tesch, “Human single muscle fibre function with 84 day bed-rest and resistance exercise,” The Journal of Physiology, vol. 557, no. 2, pp. 501–513, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. D. B. Thomason and F. W. Booth, “Atrophy of the soleus muscle by hindlimb unweighting,” Journal of Applied Physiology, vol. 68, no. 1, pp. 1–12, 1990. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Bonen, M. H. Tan, and W. M. Watson-Wright, “Insulin binding and glucose uptake differences in rodent skeletal muscles,” Diabetes, vol. 30, no. 8, pp. 702–704, 1981. View at Publisher · View at Google Scholar · View at Scopus
  27. J. R. Daugaard and E. A. Richter, “Relationship between muscle fibre composition, glucose transporter protein 4 and exercise training: possible consequences in non-insulin-dependent diabetes mellitus,” Acta Physiologica Scandinavica, vol. 171, no. 3, pp. 267–276, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Gaster, P. Poulsen, A. Handberg, H. D. Schrøder, and H. Beck-Nielsen, “Direct evidence of fiber type-dependent GLUT-4 expression in human skeletal muscle,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 278, no. 5, pp. E910–E916, 2000. View at Google Scholar · View at Scopus
  29. E. J. Henriksen, R. E. Bourey, K. J. Rodnick, L. Koranyi, M. A. Permutt, and J. O. Holloszy, “Glucose transporter protein content and glucose transport capacity in rat skeletal muscles,” American Journal of Physiology. Endocrinology and Metabolism, vol. 259, no. 4, pp. E593–E598, 1990. View at Google Scholar · View at Scopus
  30. J. R. Zierath, L. He, A. Gumà, E. O. Wahlström, A. Klip, and H. Wallberg-Henriksson, “Insulin action on glucose transport and plasma membrane GLUT4 content in skeletal muscle from patients with NIDDM,” Diabetologia, vol. 39, no. 10, pp. 1180–1189, 1996. View at Publisher · View at Google Scholar · View at Scopus
  31. J. He, S. Watkins, and D. E. Kelley, “Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity,” Diabetes, vol. 50, no. 4, pp. 817–823, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. M. S. Hickey, J. O. Carey, J. L. Azevedo et al., “Skeletal muscle fiber composition is related to adiposity and in vitro glucose transport rate in humans,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 268, no. 3, pp. E453–E457, 1995. View at Google Scholar · View at Scopus
  33. 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,” The Journal of Clinical Investigation, vol. 80, no. 2, pp. 415–424, 1987. View at Publisher · View at Google Scholar · View at Scopus
  34. C. A. Maltin, “Muscle development and obesity: is there a relationship?” Organogenesis, vol. 4, no. 3, pp. 158–169, 2008. View at Google Scholar · View at Scopus
  35. P. Mårin, B. Andersson, M. Krotkiewski, and P. Björntorp, “Muscle fiber composition and capillary density in women and men with NIDDM,” Diabetes Care, vol. 17, no. 5, pp. 382–386, 1994. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Gaster, P. Staehr, H. Beck-Nielsen, H. D. Schrøder, and A. Handberg, “GLUT4 is reduced in slow muscle fibers of type 2 diabetic patients: is insulin resistance in type 2 diabetes a slow, type 1 fiber disease?” Diabetes, vol. 50, no. 6, pp. 1324–1329, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Oberbach, Y. Bossenz, S. Lehmann et al., “Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes,” Diabetes Care, vol. 29, no. 4, pp. 895–900, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. J. A. Simoneau, S. R. Colberg, F. L. Thaete, and D. E. Kelley, “Skeletal muscle glycolitic and oxidative enzyme capacities are determinants of insulin sensitivity and muscle composition in obese women,” The FASEB Journal, vol. 9, no. 2, pp. 273–278, 1995. View at Google Scholar · View at Scopus
  39. J. A. Simoneau and D. E. Kelley, “Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM,” Journal of Applied Physiology, vol. 83, no. 1, pp. 166–171, 1997. View at Google Scholar · View at Scopus
  40. J. Simoneau, J. H. Veerkamp, L. P. Turcotte, and D. E. Kelley, “Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss,” The FASEB Journal, vol. 13, no. 14, pp. 2051–2060, 1999. View at Google Scholar · View at Scopus
  41. C. A. Stuart, M. P. McCurry, A. Marino et al., “Slow-twitch fiber proportion in skeletal muscle correlates with insulin responsiveness,” The Journal of Clinical Endocrinology & Metabolism, vol. 98, no. 5, pp. 2027–2036, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. C. J. Tanner, H. A. Barakat, G. Lynis Dohm et al., “Muscle fiber type is associated with obesity and weight loss,” American Journal of Physiology: Endocrinology and Metabolism, vol. 282, no. 6, pp. E1191–E1196, 2002. View at Google Scholar · View at Scopus
  43. V. K. Mootha, C. M. Lindgren, K. Eriksson et al., “PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes,” Nature Genetics, vol. 34, no. 3, pp. 267–273, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. M. E. Patti, A. J. Butte, S. Crunkhorn et al., “Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 14, pp. 8466–8471, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Sreekumar, P. Halvatsiotis, J. C. Schimke, and K. Sreekumaran Nair, “Gene expression profile in skeletal muscle of type 2 diabetes and the effect of insulin treatment,” Diabetes, vol. 51, no. 6, pp. 1913–1920, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. B. H. Annex, C. E. Torgan, P. Lin et al., “Induction and maintenance of increased VEGF protein by chronic motor nerve stimulation in skeletal muscle,” TheAmerican Journal of Physiology, vol. 274, part 2, no. 3, pp. H860–H867, 1998. View at Google Scholar · View at Scopus
  47. O. Hudlicka, L. Dodd, E. M. Renkin, and S. D. Gray, “Early changes in fiber profile and capillary density in long-term stimulated muscles,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 243, no. 4, pp. H528–H535, 1982. View at Google Scholar · View at Scopus
  48. F. Ingjer, “Capillary supply and mitochondrial content of different skeletal muscle fiber types in untrained and endurance-trained men. A histochemical and ultrastructural study,” European Journal of Applied Physiology and Occupational Physiology, vol. 40, no. 3, pp. 197–209, 1979. View at Google Scholar · View at Scopus
  49. H. Lithell, F. Lindgarde, K. Hellsing et al., “Body weight, skeletal muscle morphology, and enzyme activities in relation to fasting serum insulin concentration and glucose tolerance in 48-year-old men,” Diabetes, vol. 30, no. 1, pp. 19–25, 1981. View at Publisher · View at Google Scholar · View at Scopus
  50. G. Sjøgaard, “Capillary supply and cross-sectional area of slow and fast twitch muscle fibres in man,” Histochemistry, vol. 76, no. 4, pp. 547–555, 1982. View at Google Scholar · View at Scopus
  51. H. Eyre, R. Kahn, R. M. Robertson et al., “Preventing cancer, cardiovascular disease, and diabetes: a common agenda for the American Cancer Society, the American Diabetes Association, and the American Heart Association,” Stroke, vol. 35, no. 8, pp. 1999–2010, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Elgzyri, H. Parikh, Y. Zhou et al., “First-degree relatives of type 2 diabetic patients have reduced expression of genes involved in fatty acid metabolism in skeletal muscle,” The Journal of Clinical Endocrinology and Metabolism, vol. 97, no. 7, pp. E1332–E1337, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. K. Morino, K. F. Petersen, S. Dufour et al., “Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents,” The Journal of Clinical Investigation, vol. 115, no. 12, pp. 3587–3593, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. K. F. Petersen, S. Dufour, D. Befroy, R. Garcia, and G. I. Shulman, “Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes,” The New England Journal of Medicine, vol. 350, no. 7, pp. 664–671, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. J.-A. Simoneau and C. Bouchard, “Genetic determinism of fiber type proportion in human skeletal muscle,” The FASEB Journal, vol. 9, no. 11, pp. 1091–1095, 1995. View at Google Scholar · View at Scopus
  56. B. C. Martin, J. H. Warram, A. S. Krolewski, R. N. Bergman, J. S. Soeldner, and C. R. Kahn, “Role of glucose and insulin resistance in development of type 2 diabetes mellitus: results of a 25-year follow-up study,” The Lancet, vol. 340, no. 8825, pp. 925–929, 1992. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Eriksson, A. Franssila-Kallunki, A. Ekstrand et al., “Early metabolic defects in persons at increased risk for non-insulin-dependent diabetes mellitus,” The New England Journal of Medicine, vol. 321, no. 6, pp. 337–343, 1989. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Lillioja, D. M. Mott, M. Spraul et al., “Insulin resistance and insulin secretory dysfunction as precursors of non-insulin-dependent diabetes mellitus: prospective studies of Pima Indians,” The New England Journal of Medicine, vol. 329, no. 27, pp. 1988–1992, 1993. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Doria, M.-E. Patti, and C. R. Kahn, “The emerging genetic architecture of type 2 diabetes,” Cell Metabolism, vol. 8, no. 3, pp. 186–200, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Almind, C. Bjorbaek, H. Vestergaard, T. Hansen, S. Echwald, and O. Pedersen, “Aminoacid polymorphisms of insulin receptor substrate-1 in non-inslin-dependent diabetes mellitus,” The Lancet, vol. 342, no. 8875, pp. 828–832, 1993. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Almind, G. Inoue, O. Pedersen, and C. R. Kahn, “A common amino acid polymorphism in insulin receptor substrate-1 causes impaired insulin signaling. Evidence from transfection studies,” The Journal of Clinical Investigation, vol. 97, no. 11, pp. 2569–2575, 1996. View at Publisher · View at Google Scholar · View at Scopus
  62. E. Morini, S. Prudente, E. Succurro et al., “IRS1 G972R polymorphism and type 2 diabetes: a paradigm for the difficult ascertainment of the contribution to disease susceptibility of “low-frequency-low-risk” variants,” Diabetologia, vol. 52, no. 9, pp. 1852–1857, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. D. Altshuler, J. N. Hirschhorn, M. Klannemark et al., “The common PPARγ Pro12Ala polymorphism is associated with decreased risk of type 2 diabetes,” Nature Genetics, vol. 26, no. 1, pp. 76–80, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. J. Rung, S. Cauchi, A. Albrechtsen et al., “Genetic variant near IRS1 is associated with type 2 diabetes, insulin resistance and hyperinsulinemia,” Nature Genetics, vol. 41, no. 10, pp. 1110–1115, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Tang, X. Han, X. Sun et al., “Association study of a common variant near IRS1 with type 2 diabetes mellitus in Chinese Han population,” Endocrine, vol. 43, no. 1, pp. 84–91, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. A. P. Morris, B. F. Voight, T. M. Teslovich et al., “Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 diabetes,” Nature Genetics, vol. 44, no. 9, pp. 981–990, 2012. View at Google Scholar
  67. B. F. Voight, L. J. Scott, V. Steinthorsdottir et al., “Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis,” Nature Genetics, vol. 42, no. 7, pp. 579–589, 2010. View at Google Scholar
  68. T. A. Manolio, F. S. Collins, N. J. Cox et al., “Finding the missing heritability of complex diseases,” Nature, vol. 461, no. 7265, pp. 747–753, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. M. I. McCarthy, G. R. Abecasis, L. R. Cardon et al., “Genome-wide association studies for complex traits: consensus, uncertainty and challenges,” Nature Reviews Genetics, vol. 9, no. 5, pp. 356–369, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. R. J. Neuman, J. Wasson, G. Atzmon et al., “Gene-gene interactions lead to higher risk for development of type 2 diabetes in an Ashkenazi Jewish population,” PLoS ONE, vol. 5, no. 3, Article ID e9903, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. R. Plomin, C. M. A. Haworth, and O. S. P. Davis, “Common disorders are quantitative traits,” Nature Reviews Genetics, vol. 10, no. 12, pp. 872–878, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. X. Sim, R. T. Ong, C. Suo et al., “Transferability of type 2 diabetes implicated loci in multi-ethnic cohorts from Southeast Asia,” PLoS Genetics, vol. 7, no. 4, Article ID e1001363, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. L. A. Hindorff, P. Sethupathy, H. A. Junkins et al., “Potential etiologic and functional implications of genome-wide association loci for human diseases and traits,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 23, pp. 9362–9367, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. J. A. Tennessen, A. W. Bigham, T. D. O'Connor et al., “Evolution and functional impact of rare coding variation from deep sequencing of human exomes,” Science, vol. 337, no. 6090, pp. 64–69, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. K. E. Lohmueller, T. Sparsø, Q. Li et al., “Whole-exome sequencing of 2,000 Danish individuals and the role of rare coding variants in type 2 diabetes,” The American Journal of Human Genetics, vol. 93, no. 6, pp. 1072–1086, 2013. View at Google Scholar
  76. J. C. Denny, M. D. Ritchie, M. A. Basford et al., “PheWAS: demonstrating the feasibility of a phenome-wide scan to discover gene-disease associations,” Bioinformatics, vol. 26, no. 9, pp. 1205–1210, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. J. C. Denny, L. Bastarache, M. D. Ritchie et al., “Systematic comparison of phenome-wide association study of electronic medical record data and genome-wide association study data,” Nature Biotechnology, vol. 31, no. 12, pp. 1102–1111, 2013. View at Publisher · View at Google Scholar
  78. S. J. Hebbring, “The challenges, advantages and future of phenome-wide association studies,” Immunology, vol. 141, no. 2, pp. 157–165, 2014. View at Publisher · View at Google Scholar
  79. S. A. Pendergrass, K. Brown-Gentry, S. Dudek et al., “Phenome-Wide Association Study (PheWAS) for detection of pleiotropy within the Population Architecture using Genomics and Epidemiology (PAGE) network,” PLoS Genetics, vol. 9, no. 1, Article ID e1003087, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. K. D. Baker and C. S. Thummel, “Diabetic larvae and obese flies-emerging studies of metabolism in Drosophila,” Cell Metabolism, vol. 6, no. 4, pp. 257–266, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. S. K. Kim and E. J. Rulifson, “Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells,” Nature, vol. 431, no. 7006, pp. 316–320, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Oldham and E. Hafen, “Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control,” Trends in Cell Biology, vol. 13, no. 2, pp. 79–85, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. R. T. Birse, J. Choi, K. Reardon et al., “High-fat-diet-induced obesity and heart dysfunction are regulated by the TOR pathway in Drosophila,” Cell Metabolism, vol. 12, no. 5, pp. 533–544, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. J. Pendse, P. V. Ramachandran, J. Na et al., “A Drosophila functional evaluation of candidates from human genome-wide association studies of type 2 diabetes and related metabolic traits identifies tissue-specific roles for dHHEX,” BMC Genomics, vol. 14, article 136, 2013. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Fröjdö, C. Durand, L. Molin et al., “Phosphoinositide 3-kinase as a novel functional target for the regulation of the insulin signaling pathway by SIRT1,” Molecular and Cellular Endocrinology, vol. 335, no. 2, pp. 166–176, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. S. Hashmi, Y. Wang, R. S. Parhar et al., “A C. elegans model to study human metabolic regulation,” Nutrition and Metabolism, vol. 10, no. 1, article 31, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Zhang, R. Bakheet, R. S. Parhar et al., “Regulation of fat storage and reproduction by Krüppel-like transcription factor KLF3 and fat-associated genes in Caenorhabditis elegans,” Journal of Molecular Biology, vol. 411, no. 3, pp. 537–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. C. Slawson, R. J. Copeland, and G. W. Hart, “O-GlcNAc signaling: a metabolic link between diabetes and cancer?” Trends in Biochemical Sciences, vol. 35, no. 10, pp. 547–555, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. D. M. Lehman, D. Fu, A. B. Freeman et al., “A single nucleotide polymorphism in MGEA5 encoding O-GlcNAc-selective N-acetyl-β-D glucosaminidase is associated with type 2 diabetes im Mexican Americans,” Diabetes, vol. 54, no. 4, pp. 1214–1221, 2005. View at Publisher · View at Google Scholar · View at Scopus
  90. M. E. Forsythe, D. C. Love, B. D. Lazarus et al., “Caenorhabditis elegans ortholog of a diabetes susceptibility locus: oga-1 (O-GlcNAcase) knockout impacts O-GlcNAc cycling, metabolism, and dauer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 32, pp. 11952–11957, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. A. Seth, D. L. Stemple, and I. Barroso, “The emerging use of zebrafish to model metabolic disease,” Disease Models & Mechanisms, vol. 6, no. 5, pp. 1080–1088, 2013. View at Google Scholar
  92. V. M. Bedell, Y. Wang, J. M. Campbell et al., “In vivo genome editing using a high-efficiency TALEN system,” Nature, vol. 491, no. 7422, pp. 114–118, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. N. Chang, C. Sun, L. Gao et al., “Genome editing with RNA-guided Cas9 nuclease in Zebrafish embryos,” Cell Research, vol. 23, no. 4, pp. 465–472, 2013. View at Publisher · View at Google Scholar · View at Scopus
  94. A. T. Chinwalla, L. L. Cook, K. D. Delehaunty et al., “Initial sequencing and comparative analysis of the mouse genome,” Nature, vol. 420, no. 6915, pp. 520–562, 2002. View at Google Scholar
  95. The ENCODE Project Consortium, “A user's guide to the encyclopedia of DNA elements (ENCODE),” PLoS Biology, vol. 9, no. 4, Article ID e1001046, 2011. View at Publisher · View at Google Scholar
  96. M. M. Hoffman, J. Ernst, S. P. Wilder et al., “Integrative annotation of chromatin elements from ENCODE data,” Nucleic Acids Research, vol. 41, no. 2, pp. 827–841, 2013. View at Publisher · View at Google Scholar · View at Scopus
  97. C. Dina, D. Meyre, S. Gallina et al., “Variation in FTO contributes to childhood obesity and severe adult obesity,” Nature Genetics, vol. 39, no. 6, pp. 724–726, 2007. View at Publisher · View at Google Scholar · View at Scopus
  98. T. M. Frayling, N. J. Timpson, M. N. Weedon et al., “A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity,” Science, vol. 316, no. 5826, pp. 889–894, 2007. View at Publisher · View at Google Scholar · View at Scopus
  99. A. Scuteri, S. Sanna, W. Chen et al., “Genome-wide association scan shows genetic variants in the FTO gene are associated with obesity-related traits,” PLoS Genetics, vol. 3, no. 7, Article ID e115, 2007. View at Publisher · View at Google Scholar · View at Scopus
  100. S. A. Al-Attar, R. L. Pollex, M. R. Ban et al., “Association between the FTO rs9939609 polymorphism and the metabolic syndrome in a non-Caucasian multi-ethnic sample,” Cardiovascular Diabetology, vol. 7, article 5, 2008. View at Publisher · View at Google Scholar · View at Scopus
  101. R. M. Freathy, N. J. Timpson, D. A. Lawlor et al., “Common variation in the FTO gene alters diabetes-related metabolic traits to the extent expected given its effect on BMI,” Diabetes, vol. 57, no. 5, pp. 1419–1426, 2008. View at Publisher · View at Google Scholar · View at Scopus
  102. K. A. Fawcett and I. Barroso, “The genetics of obesity: FTO leads the way,” Trends in Genetics, vol. 26, no. 6, pp. 266–274, 2010. View at Publisher · View at Google Scholar · View at Scopus
  103. C. Church, L. Moir, F. McMurray et al., “Overexpression of Fto leads to increased food intake and results in obesity,” Nature Genetics, vol. 42, no. 12, pp. 1086–1092, 2010. View at Publisher · View at Google Scholar · View at Scopus
  104. J. Fischer, L. Koch, C. Emmerling et al., “Inactivation of the Fto gene protects from obesity,” Nature, vol. 458, no. 7240, pp. 894–898, 2009. View at Publisher · View at Google Scholar · View at Scopus
  105. X. Gao, Y. Shin, M. Li, F. Wang, Q. Tong, and P. Zhang, “The fat mass and obesity associated gene FTO functions in the brain to regulate postnatal growth in mice,” PLoS ONE, vol. 5, no. 11, Article ID e14005, 2010. View at Publisher · View at Google Scholar · View at Scopus
  106. L. G. Grunnet, E. Nilsson, C. Ling et al., “Regulation and function of FTO mRNA expression in human skeletal muscle and subcutaneous adipose tissue,” Diabetes, vol. 58, no. 10, pp. 2402–2408, 2009. View at Publisher · View at Google Scholar · View at Scopus
  107. N. Klöting, D. Schleinitz, K. Ruschke et al., “Inverse relationship between obesity and FTO gene expression in visceral adipose tissue in humans,” Diabetologia, vol. 51, no. 4, pp. 641–647, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. K. Wåhlén, E. Sjölin, and J. Hoffstedt, “The common rs9939609 gene variant of the fat mass- and obesity-associated gene FTO is related to fat cell lipolysis,” Journal of Lipid Research, vol. 49, no. 3, pp. 607–611, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. G. Stratigopoulos, S. L. Padilla, C. A. LeDuc et al., “Regulation of Fto/Ftm gene expression in mice and humans,” The American Journal of Physiology—Regulatory, Integrative and Comparative Physiology, vol. 294, no. 4, pp. R1185–R1196, 2008. View at Google Scholar
  110. S. Smemo, J. J. Tena, K. H. Kim, and et al, “Obesity-associated variants within FTO form long-range functional connections with IRX3,” Nature, vol. 507, no. 7492, pp. 371–375, 2014. View at Google Scholar
  111. D. Pette and R. S. Staron, “Myosin isoforms, muscle fiber types, and transitions,” Microscopy Research and Technique, vol. 50, no. 6, pp. 500–509, 2000. View at Publisher · View at Google Scholar
  112. J. L. Andersen, A. Weiss, C. Sandri et al., “The 2B myosin heavy chain gene is expressed in human skeletal muscle,” The Journal of Physiology, vol. 539, supplement, pp. 29–30, 2000. View at Google Scholar
  113. A. Weiss, D. McDonough, B. Wertman et al., “Organization of human and mouse skeletal myosin heavy chain gene clusters is highly conserved,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 6, pp. 2958–2963, 1999. View at Publisher · View at Google Scholar · View at Scopus
  114. R. Granit, H. D. Henatsch, and G. Steg, “Tonic and phasic ventral horn cells differentiated by post-tetanic potentiation in cat extensors,” Acta Physiologica Scandinavica, vol. 37, no. 2-3, pp. 114–126, 1956. View at Publisher · View at Google Scholar · View at Scopus
  115. D. Pette and G. Vrbová, “What does chronic electrical stimulation teach us about muscle plasticity?” Muscle & Nerve, vol. 22, no. 6, pp. 666–677, 1999. View at Google Scholar
  116. R. Hennig and T. Lømo, “Firing patterns of motor units in normal rats,” Nature, vol. 314, no. 6007, pp. 164–166, 1985. View at Publisher · View at Google Scholar · View at Scopus
  117. S. Ausoni, L. Gorza, S. Schiaffino, K. Gundersen, and T. Lomo, “Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles,” The Journal of Neuroscience, vol. 10, no. 1, pp. 153–160, 1990. View at Google Scholar · View at Scopus
  118. M. Nuhr, R. Crevenna, B. Gohlsch et al., “Functional and biochemical properties of chronically stimulated human skeletal muscle,” European Journal of Applied Physiology, vol. 89, no. 2, pp. 202–208, 2003. View at Publisher · View at Google Scholar · View at Scopus
  119. M. J. Nuhr, D. Pette, R. Berger et al., “Beneficial effects of chronic low-frequency stimulation of thigh muscles in patients with advanced chronic heart failure,” European Heart Journal, vol. 25, no. 2, pp. 136–143, 2004. View at Publisher · View at Google Scholar · View at Scopus
  120. M. J. Sullivan, B. D. Duscha, H. Klitgaard, W. E. Kraus, F. R. Cobb, and B. Saltin, “Altered expression of myosin heavy chain in human skeletal muscle in chronic heart failure,” Medicine and Science in Sports and Exercise, vol. 29, no. 7, pp. 860–866, 1997. View at Publisher · View at Google Scholar · View at Scopus
  121. B. B. Lowell and G. I. Shulman, “Mitochondrial dysfunction and type 2 diabetes,” Science, vol. 307, no. 5708, pp. 384–387, 2005. View at Publisher · View at Google Scholar · View at Scopus
  122. C. B. Klee, H. Ren, and X. Wang, “Regulation of the calmodulin-stimulated protein phosphatase, calcineurin,” Journal of Biological Chemistry, vol. 273, no. 22, pp. 13367–13370, 1998. View at Publisher · View at Google Scholar · View at Scopus
  123. E. R. Chin, E. N. Olson, J. A. Richardson et al., “A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type,” Genes and Development, vol. 12, no. 16, pp. 2499–2509, 1998. View at Publisher · View at Google Scholar · View at Scopus
  124. F. J. Naya, B. Mercer, J. Shelton, J. A. Richardson, R. S. Williams, and E. N. Olson, “Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo,” The Journal of Biological Chemistry, vol. 275, no. 7, pp. 4545–4548, 2000. View at Publisher · View at Google Scholar · View at Scopus
  125. A. L. Serrano, M. Murgia, G. Pallafacchina et al., “Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growth,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 23, pp. 13108–13113, 2001. View at Publisher · View at Google Scholar · View at Scopus
  126. E. Calabria, S. Ciciliot, I. Moretti et al., “NFAT isoforms control activity-dependent muscle fiber type specification,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 32, pp. 13335–13340, 2009. View at Publisher · View at Google Scholar · View at Scopus
  127. P. G. Hogan, L. Chen, J. Nardone, and A. Rao, “Transcriptional regulation by calcium, calcineurin, and NFAT,” Genes and Development, vol. 17, no. 18, pp. 2205–2232, 2003. View at Publisher · View at Google Scholar · View at Scopus
  128. J. D. Meissner, P. K. Umeda, K. Chang, G. Gros, and R. J. Scheibe, “Activation of the β myosin heavy chain promoter by MEF-2D, MyoD, p300, and the calcineurin/NFATc1 pathway,” Journal of Cellular Physiology, vol. 211, no. 1, pp. 138–148, 2007. View at Publisher · View at Google Scholar · View at Scopus
  129. Z. A. Rana, K. Gundersen, A. Buonanno, and D. Vullhorst, “Imaging transcription in vivo: distinct regulatory effects of fast and slow activity patterns on promoter elements from vertebrate troponin I isoform genes,” The Journal of Physiology, vol. 562, part 3, pp. 815–828, 2005. View at Publisher · View at Google Scholar · View at Scopus
  130. Z. A. Rana, K. Gundersen, and A. Buonanno, “Activity-dependent repression of muscle genes by NFAT,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 15, pp. 5921–5926, 2008. View at Publisher · View at Google Scholar · View at Scopus
  131. J. Tothova, B. Blaauw, G. Pallafacchina et al., “NFATc1 nucleocytoplasmic shuttling is controlled by nerve activity in skeletal muscle,” Journal of Cell Science, vol. 119, no. 8, pp. 1604–1611, 2006. View at Publisher · View at Google Scholar · View at Scopus
  132. J. A. Drenning, V. A. Lira, C. G. Simmons, Q. A. Soltow, J. E. Sellman, and D. S. Criswell, “Nitric oxide facilitates NFAT-dependent transcription in mouse myotubes,” The American Journal of Physiology—Cell Physiology, vol. 294, no. 4, pp. C1088–C1095, 2008. View at Publisher · View at Google Scholar · View at Scopus
  133. J. S. Stamler and G. Meissner, “Physiology of nitric oxide in skeletal muscle,” Physiological Reviews, vol. 81, no. 1, pp. 209–237, 2001. View at Google Scholar · View at Scopus
  134. P. J. Reiser, W. O. Kline, and P. L. Vaghy, “Induction of neuronal type nitric oxide synthase in skeletal muscle by chronic electrical stimulation in vivo,” Journal of Applied Physiology, vol. 82, no. 4, pp. 1250–1255, 1997. View at Google Scholar · View at Scopus
  135. K. J. B. Martins, M. St-Louis, G. K. Murdoch et al., “Nitric oxide synthase inhibition prevents activity-induced calcineurin-NFATc1 signalling and fast-to-slow skeletal muscle fibre type conversions,” Journal of Physiology, vol. 590, no. 6, pp. 1427–1442, 2012. View at Publisher · View at Google Scholar · View at Scopus
  136. K. Punkt, M. Fritzsche, C. Stockmar et al., “Nitric oxide synthase in human skeletal muscles related to defined fibre types,” Histochemistry and Cell Biology, vol. 125, no. 5, pp. 567–573, 2006. View at Publisher · View at Google Scholar · View at Scopus
  137. S. R. Kashyap, L. J. Roman, J. Lamont et al., “Insulin resistance is associated with impaired nitric oxide synthase activity in skeletal muscle of type 2 diabetic subjects,” Journal of Clinical Endocrinology and Metabolism, vol. 90, no. 2, pp. 1100–1105, 2005. View at Publisher · View at Google Scholar · View at Scopus
  138. P. de Koninck and H. Schulman, “Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations,” Science, vol. 279, no. 5348, pp. 227–230, 1998. View at Publisher · View at Google Scholar · View at Scopus
  139. F. Eshete and R. D. Fields, “Spike frequency decoding and autonomous activation of Ca2+-calmodulin-dependent protein kinase II in dorsal root ganglion neurons,” Journal of Neuroscience, vol. 21, no. 17, pp. 6694–6705, 2001. View at Google Scholar · View at Scopus
  140. M. Pelosi and A. Donella-Deana, “Localization, purification, and characterization of the rabbit sarcoplasmic reticulum associated calmodulin-dependent protein kinase,” Biochemistry, vol. 65, no. 2, pp. 259–268, 2000. View at Google Scholar · View at Scopus
  141. A. J. Rose and M. Hargreaves, “Exercise increases Ca2+-calmodulin-dependent protein kinase II activity in human skeletal muscle,” The Journal of Physiology, vol. 553, no. 1, pp. 303–309, 2003. View at Publisher · View at Google Scholar · View at Scopus
  142. A. J. Rose, B. Kiens, and E. A. Richter, “Ca2+-calmodulin-dependent protein kinase expression and signalling in skeletal muscle during exercise,” Journal of Physiology, vol. 574, no. 3, pp. 889–903, 2006. View at Publisher · View at Google Scholar · View at Scopus
  143. H. Wu, F. J. Naya, T. A. McKinsey et al., “MEF2 responds to multiple calcium-regulated signals in the control of skeletal muscle fiber type,” EMBO Journal, vol. 19, no. 9, pp. 1963–1973, 2000. View at Publisher · View at Google Scholar · View at Scopus
  144. H. Wu, B. Rothermel, S. Kanatous et al., “Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway,” EMBO Journal, vol. 20, no. 22, pp. 6414–6423, 2001. View at Publisher · View at Google Scholar · View at Scopus
  145. U. Dressel, P. J. Bailey, S. C. Wang, M. Downes, R. M. Evans, and G. E. O. Muscat, “A Dynamic role for HDAC7 in MEF2-mediated muscle differentiation,” The Journal of Biological Chemistry, vol. 276, no. 20, pp. 17007–17013, 2001. View at Publisher · View at Google Scholar · View at Scopus
  146. C. Lemercier, A. Verdel, B. Galloo, S. Curtet, M. Brocard, and S. Khochbin, “mHDA1/HDAC5 histone deacetylase interacts with and represses MEF2A transcriptional activity,” The Journal of Biological Chemistry, vol. 275, no. 20, pp. 15594–15599, 2000. View at Publisher · View at Google Scholar · View at Scopus
  147. E. A. Miska, C. Karlsson, E. Langley, S. J. Nielsen, J. Pines, and T. Kouzarides, “HDAC4 deacetylase associates with and represses the MEF2 transcription factor,” EMBO Journal, vol. 18, no. 18, pp. 5099–5107, 1999. View at Publisher · View at Google Scholar · View at Scopus
  148. A. H. Wang, N. R. Bertos, M. Vezmar et al., “HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor,” Molecular and Cellular Biology, vol. 19, no. 11, pp. 7816–7827, 1999. View at Google Scholar · View at Scopus
  149. J. Lu, T. A. McKinsey, C. Zhang, and E. N. Olson, “Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II histone deacetylases,” Molecular Cell, vol. 6, no. 2, pp. 233–244, 2000. View at Publisher · View at Google Scholar · View at Scopus
  150. T. A. McKinsey, C.-L. Zhang, J. Lu, and E. N. Olson, “Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation,” Nature, vol. 408, no. 6808, pp. 106–111, 2000. View at Publisher · View at Google Scholar · View at Scopus
  151. Y. Liu, W. R. Randall, and M. F. Schneider, “Activity-dependent and -independent nuclear fluxes of HDAC4 mediated by different kinases in adult skeletal muscle,” Journal of Cell Biology, vol. 168, no. 6, pp. 887–897, 2005. View at Publisher · View at Google Scholar · View at Scopus
  152. C. R. Bruce, M. J. Anderson, A. L. Carey et al., “Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status,” Journal of Clinical Endocrinology and Metabolism, vol. 88, no. 11, pp. 5444–5451, 2003. View at Publisher · View at Google Scholar · View at Scopus
  153. M. P. Czubryt, J. McAnally, G. I. Fishman, and E. N. Olson, “Regulation of peroxisome proliferator-activated receptor γ coactivator 1α (PGC-1α) and mitochondrial function by MEF2 and HDAC5,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 4, pp. 1711–1716, 2003. View at Publisher · View at Google Scholar · View at Scopus
  154. 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
  155. R. B. Vega, J. M. Huss, and D. P. Kelly, “The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor α in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes,” Molecular and Cellular Biology, vol. 20, no. 5, pp. 1868–1876, 2000. View at Publisher · View at Google Scholar · View at Scopus
  156. Z. Wu, P. Puigserver, U. Andersson et al., “Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1,” Cell, vol. 98, no. 1, pp. 115–124, 1999. View at Publisher · View at Google Scholar · View at Scopus
  157. 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
  158. H. Pilegaard, B. Saltin, and D. P. 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
  159. E. B. Taylor, J. D. Lamb, R. W. Hurst et al., “Endurance training increases skeletal muscle LKB1 and PGC-1α protein abundance: effects of time and intensity,” American Journal of Physiology. Endocrinology and Metabolism, vol. 289, no. 6, pp. E960–E968, 2005. View at Publisher · View at Google Scholar · View at Scopus
  160. T. Akimoto, S. C. Pohnert, P. Li et al., “Exercise stimulates Pgc-1α transcription in skeletal muscle through activation of the p38 MAPK pathway,” Journal of Biological Chemistry, vol. 280, no. 20, pp. 19587–19593, 2005. View at Publisher · View at Google Scholar · View at Scopus
  161. D. C. Wright, P. C. Geiger, D. Han, T. E. Jones, and J. O. Holloszy, “Calcium induces increases in peroxisome proliferator-activated receptor γ coactivator-1α and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation,” The Journal of Biological Chemistry, vol. 282, no. 26, pp. 18793–18799, 2007. View at Publisher · View at Google Scholar · View at Scopus
  162. F. Lluís, E. Perdiguero, A. R. Nebreda, and P. Muñoz-Cánoves, “Regulation of skeletal muscle gene expression by p38 MAP kinases,” Trends in Cell Biology, vol. 16, no. 1, pp. 36–44, 2006. View at Publisher · View at Google Scholar · View at Scopus
  163. P. Puigserver, J. Rhee, J. Lin et al., “Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARγ coactivator-1,” Molecular Cell, vol. 8, no. 5, pp. 971–982, 2001. View at Publisher · View at Google Scholar · View at Scopus
  164. W. Niu, C. Huang, Z. Nawaz et al., “Maturation of the regulation of GLUT4 activity by p38 MAPK during L6 cell myogenesis,” Journal of Biological Chemistry, vol. 278, no. 20, pp. 17953–17962, 2003. View at Publisher · View at Google Scholar · View at Scopus
  165. T. Geng, P. Li, M. Okutsu et al., “PGC-1α plays a functional role in exercise-induced mitochondrial biogenesis and angiogenesis but not fiber-type transformation in mouse skeletal muscle,” The American Journal of Physiology—Cell Physiology, vol. 298, no. 3, pp. C572–C579, 2010. View at Publisher · View at Google Scholar · View at Scopus
  166. A. R. Pogozelski, T. Geng, P. Li et al., “p38γ mitogen-activated protein kinase is a key regulator in skeletal muscle metabolic adaptation in mice,” PLoS ONE, vol. 4, no. 11, Article ID e7934, 2009. View at Publisher · View at Google Scholar · View at Scopus
  167. S. Crunkhorn, F. Dearie, C. Mantzoros et al., “Peroxisome proliferator activator receptor γ coactivator-1 expression is reduced in obesity: potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation,” The Journal of Biological Chemistry, vol. 282, no. 21, pp. 15439–15450, 2007. View at Publisher · View at Google Scholar · View at Scopus
  168. A. Sriwijitkamol, J. L. Ivy, C. Christ-Roberts, R. A. DeFronzo, L. J. Mandarino, and N. Musi, “LKB1-AMPK signaling in muscle from obese insulin-resistant Zucker rats and effects of training,” American Journal of Physiology—Endocrinology and Metabolism, vol. 290, no. 5, pp. E925–E932, 2006. View at Publisher · View at Google Scholar · View at Scopus
  169. 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
  170. D. G. Hardie, F. A. Ross, and S. A. Hawley, “AMPK: a nutrient and energy sensor that maintains energy homeostasis,” Nature Reviews Molecular Cell Biology, vol. 13, no. 4, pp. 251–262, 2012. View at Publisher · View at Google Scholar · View at Scopus
  171. S. Jäer, C. Handschin, J. St-Pierre, and B. M. Spiegelman, “AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 29, pp. 12017–12022, 2007. View at Publisher · View at Google Scholar · View at Scopus
  172. Z. Gerhart-Hines, J. T. Rodgers, O. Bare et al., “Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1α,” EMBO Journal, vol. 26, no. 7, pp. 1913–1923, 2007. View at Publisher · View at Google Scholar · View at Scopus
  173. S. Nemoto, M. M. Fergusson, and T. Finkel, “SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1α,” The Journal of Biological Chemistry, vol. 280, no. 16, pp. 16456–16460, 2005. View at Publisher · View at Google Scholar · View at Scopus
  174. C. Cantó, Z. Gerhart-Hines, J. N. Feige et al., “AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity,” Nature, vol. 458, no. 7241, pp. 1056–1060, 2009. View at Publisher · View at Google Scholar · View at Scopus
  175. K. Sakamoto, A. McCarthy, D. Smith et al., “Deficiency of LKB1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction,” EMBO Journal, vol. 24, no. 10, pp. 1810–1820, 2005. View at Publisher · View at Google Scholar · View at Scopus
  176. M. Lagouge, C. Argmann, Z. Gerhart-Hines et al., “Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α,” Cell, vol. 127, no. 6, pp. 1109–1122, 2006. View at Publisher · View at Google Scholar · View at Scopus
  177. V. A. Narkar, M. Downes, R. T. Yu et al., “AMPK and PPARδ agonists are exercise mimetics,” Cell, vol. 134, no. 3, pp. 405–415, 2008. View at Publisher · View at Google Scholar · View at Scopus
  178. K. Svensson and C. Handschin, “Modulation of PGC-1alpha activity as a treatment for metabolic and muscle-related diseases,” Drug Discovery Today, vol. 19, no. 7, pp. 1024–1029, 2014. View at Publisher · View at Google Scholar
  179. C. Bouchard, J. A. Simoneau, G. Lortie, M. R. Boulay, M. Marcotte, and M. C. Thibault, “Genetic effects in human skeletal muscle fiber type distribution and enzyme activities,” Canadian Journal of Physiology and Pharmacology, vol. 64, no. 9, pp. 1245–1251, 1986. View at Google Scholar · View at Scopus
  180. P. V. Komi, J. H. T. Viitasalo, M. Havu, A. Thorstensson, B. Sjödin, and J. Karlsson, “Skeletal muscle fibres and muscle enzyme activities in monozygous and dizygous twins of both sexes,” Acta Physiologica Scandinavica, vol. 100, no. 4, pp. 385–392, 1977. View at Google Scholar · View at Scopus
  181. K. Condon, L. Silberstein, H. M. Blau, and W. J. Thompson, “Differentiation of fiber types in aneural musculature of the prenatal rat hindlimb,” Developmental Biology, vol. 138, no. 2, pp. 275–295, 1990. View at Publisher · View at Google Scholar · View at Scopus
  182. P. W. Sheard and M. J. Duxson, “Composition of newly forming motor units in prenatal rat intercostal muscle,” Developmental Dynamics, vol. 205, no. 2, pp. 196–212, 1996. View at Google Scholar
  183. M. Oh, I. I. Rybkin, V. Copeland et al., “Calcineurin is necessary for the maintenance but not embryonic development of slow muscle fibers,” Molecular and Cellular Biology, vol. 25, no. 15, pp. 6629–6638, 2005. View at Publisher · View at Google Scholar · View at Scopus
  184. S. Biressi, M. Molinaro, and G. Cossu, “Cellular heterogeneity during vertebrate skeletal muscle development,” Developmental Biology, vol. 308, no. 2, pp. 281–293, 2007. View at Publisher · View at Google Scholar · View at Scopus
  185. F. E. Stockdale, “Myogenic cell lineages,” Developmental Biology, vol. 154, no. 2, pp. 284–298, 1992. View at Publisher · View at Google Scholar · View at Scopus
  186. M. Narusawa, R. B. Fitzsimons, S. Izumo, B. Nadal-Ginard, N. A. Rubinstein, and A. M. Kelly, “Slow myosin in developing rat skeletal muscle,” Journal of Cell Biology, vol. 104, no. 3, pp. 447–459, 1987. View at Publisher · View at Google Scholar · View at Scopus
  187. L. G. Robson and S. M. Hughes, “Local signals in the chick limb bud can override myoblast lineage commitment: induction of slow myosin heavy chain in fast myoblasts,” Mechanisms of Development, vol. 85, no. 1-2, pp. 59–71, 1999. View at Publisher · View at Google Scholar · View at Scopus
  188. A. S. Cachaço, S. M. Chuva de Sousa Lopes, I. Kuikman et al., “Knock-in of integrin β1D affects primary but not secondary myogenesis in mice,” Development, vol. 130, no. 8, pp. 1659–1671, 2003. View at Publisher · View at Google Scholar · View at Scopus
  189. P. M. Wigmore and G. F. Dunglison, “The generation of fiber diversity during myogenesis,” International Journal of Developmental Biology, vol. 42, no. 2, pp. 117–125, 1998. View at Google Scholar · View at Scopus
  190. J. P. Barbet, L.-E. Thornell, and G. S. Butler-Browne, “Immunocytochemical characterisation of two generations of fibers during the development of the human quadriceps muscle,” Mechanisms of Development, vol. 35, no. 1, pp. 3–11, 1991. View at Publisher · View at Google Scholar · View at Scopus
  191. A. Aziz, S. Sebastian, and J. Dilworth, “The origin and fate of muscle satellite cells,” Stem Cell Reviews and Reports, vol. 8, no. 2, pp. 609–622, 2012. View at Publisher · View at Google Scholar · View at Scopus
  192. J. D. Rosenblatt, D. J. Parry, and T. A. Partridge, “Phenotype of adult mouse muscle myoblasts reflects their fiber type of origin,” Differentiation, vol. 60, no. 1, pp. 39–45, 1996. View at Publisher · View at Google Scholar · View at Scopus
  193. J. M. Kalhovde, R. Jerkovic, I. Sefland et al., ““Fast” and “slow” muscle fibres in hindlimb muscles of adult rats regenerate from intrinsically different satellite cells,” The Journal of Physiology, vol. 562, no. 3, pp. 847–857, 2005. View at Publisher · View at Google Scholar · View at Scopus
  194. N. Hagiwara, M. Yeh, and A. Liu, “Sox6 is required for normal fiber type differentiation of fetal skeletal muscle in mice,” Developmental Dynamics, vol. 236, no. 8, pp. 2062–2076, 2007. View at Publisher · View at Google Scholar · View at Scopus
  195. N. Hagiwara, “Sox6, jack of all trades: a versatile regulatory protein in vertebrate development,” Developmental Dynamics, vol. 240, no. 6, pp. 1311–1321, 2011. View at Publisher · View at Google Scholar · View at Scopus
  196. C. An, Y. Dong, and N. Hagiwara, “Genome-wide mapping of Sox6 binding sites in skeletal muscle reveals both direct and indirect regulation of muscle terminal differentiation by Sox6,” BMC Developmental Biology, vol. 11, article 59, 2011. View at Publisher · View at Google Scholar · View at Scopus
  197. D. Quiat, K. A. Voelker, J. Pei et al., “Concerted regulation of myofiber-specific gene expression and muscle performance by the transcriptional repressor Sox6,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 25, pp. 10196–10201, 2011. View at Publisher · View at Google Scholar · View at Scopus
  198. V. A. Narkar, W. Fan, M. Downes et al., “Exercise and PGC-1α-independent synchronization of type i muscle metabolism and vasculature by ERRγ,” Cell Metabolism, vol. 13, no. 3, pp. 283–293, 2011. View at Publisher · View at Google Scholar · View at Scopus
  199. S. M. Rangwala, X. Wang, J. A. Calvo et al., “Estrogen-related receptor γ is a key regulator of muscle mitochondrial activity and oxidative capacity,” The Journal of Biological Chemistry, vol. 285, no. 29, pp. 22619–22629, 2010. View at Publisher · View at Google Scholar · View at Scopus
  200. J. J. McCarthy, K. A. Esser, C. A. Peterson, and E. E. Dupont-Versteegden, “Evidence of MyomiR network regulation of β-myosin heavy chain gene expression during skeletal muscle atrophy,” Physiological Genomics, vol. 39, no. 3, pp. 219–226, 2009. View at Publisher · View at Google Scholar · View at Scopus
  201. E. van Rooij, D. Quiat, B. A. Johnson et al., “A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance,” Developmental Cell, vol. 17, no. 5, pp. 662–673, 2009. View at Publisher · View at Google Scholar · View at Scopus
  202. Z. Gan, J. Rumsey, B. C. Hazen et al., “Nuclear receptor/microRNA circuitry links muscle fiber type to energy metabolism,” The Journal of Clinical Investigation, vol. 123, no. 6, pp. 2564–2575, 2013. View at Publisher · View at Google Scholar · View at Scopus
  203. R. J. Delahanty, A. Beeghly-Fadiel, Y. Xiang et al., “Association of obesity-related genetic variants with endometrial cancer risk: a report from the shanghai endometrial cancer genetics study,” The American Journal of Epidemiology, vol. 174, no. 10, pp. 1115–1126, 2011. View at Publisher · View at Google Scholar · View at Scopus
  204. N. Franceschini, E. Fox, Z. Zhang et al., “Genome-wide association analysis of blood-pressure traits in African-ancestry individuals reveals common associated genes in African and non-African populations,” The American Journal of Human Genetics, vol. 93, no. 3, pp. 545–554, 2013. View at Google Scholar
  205. S. K. Ganesh, V. Tragante, W. Guo et al., “Loci influencing blood pressure identified using a cardiovascular gene-centric array,” Human Molecular Genetics, vol. 22, no. 8, pp. 1663–1678, 2013. View at Google Scholar
  206. T. Johnson, T. R. Gaunt, S. J. Newhouse, S. Padmanabhan, M. Tomaszewski, and M. Kumari, “Blood pressure loci identified with a gene-centric array,” The American Journal of Human Genetics, vol. 89, no. 6, pp. 688–700, 2011. View at Google Scholar
  207. R. Grifone, C. Laclef, F. Spitz et al., “Six1 and Eya1 expression can reprogram adult muscle from the slow-twitch phenotype into the fast-twitch phenotype,” Molecular and Cellular Biology, vol. 24, no. 14, pp. 6253–6267, 2004. View at Publisher · View at Google Scholar · View at Scopus
  208. A. F. Richard, J. Demignon, I. Sakakibara et al., “Genesis of muscle fiber-type diversity during mouse embryogenesis relies on Six1 and Six4 gene expression,” Developmental Biology, vol. 359, no. 2, pp. 303–320, 2011. View at Publisher · View at Google Scholar · View at Scopus
  209. J. W. Ryder, R. Bassel-Duby, E. N. Olson, and J. R. Zierath, “Skeletal muscle reprogramming by activation of calcineurin improves insulin action on metabolic pathways,” Journal of Biological Chemistry, vol. 278, no. 45, pp. 44298–44304, 2003. View at Publisher · View at Google Scholar · View at Scopus
  210. R. C. Scarpulla, R. B. Vega, and D. P. Kelly, “Transcriptional integration of mitochondrial biogenesis,” Trends in Endocrinology and Metabolism, vol. 23, no. 9, pp. 459–466, 2012. View at Publisher · View at Google Scholar · View at Scopus
  211. J. A. Calvo, T. G. Daniels, X. Wang et al., “Muscle-specific expression of PPARγ coactivator-1α improves exercise performance and increases peak oxygen uptake,” Journal of Applied Physiology, vol. 104, no. 5, pp. 1304–1312, 2008. View at Publisher · View at Google Scholar · View at Scopus
  212. 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,” The Journal of Biological Chemistry, vol. 282, no. 41, pp. 30014–30021, 2007. View at Publisher · View at Google Scholar · View at Scopus
  213. C. S. Choi, D. E. Befroy, R. Codella et al., “Paradoxical effects of increased expression of PGC-1α on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 50, pp. 19926–19931, 2008. View at Publisher · View at Google Scholar · View at Scopus
  214. B. D. Hegarty, S. M. Furler, J. Ye, G. J. Cooney, and E. W. Kraegen, “The role of intramuscular lipid in insulin resistance,” Acta Physiologica Scandinavica, vol. 178, no. 4, pp. 373–383, 2003. View at Publisher · View at Google Scholar · View at Scopus
  215. B. N. Finck, X. Han, M. Courtois et al., “A critical role for PPARα-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 3, pp. 1226–1231, 2003. View at Publisher · View at Google Scholar · View at Scopus
  216. B. N. Finck, C. Bernal-Mizrachi, D. H. Han et al., “A potential link between muscle peroxisome proliferator- activated receptor-α signaling and obesity-related diabetes,” Cell Metabolism, vol. 1, no. 2, pp. 133–144, 2005. View at Publisher · View at Google Scholar · View at Scopus
  217. S. Kleiner, V. Nguyen-Tran, O. Baré, X. Huang, B. Spiegelman, and Z. Wu, “PPARδ agonism activates fatty acid oxidation via PGC-1α but does not increase mitochondrial gene expression and function,” The Journal of Biological Chemistry, vol. 284, no. 28, pp. 18624–18633, 2009. View at Publisher · View at Google Scholar · View at Scopus
  218. T. Tanaka, J. Yamamoto, S. Iwasaki et al., “Activation of peroxisome proliferator-activated receptor δ induces fatty acid β-oxidation in skeletal muscle and attenuates metabolic syndrome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 26, pp. 15924–15929, 2003. View at Publisher · View at Google Scholar · View at Scopus
  219. 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 e294, 2004. View at Publisher · View at Google Scholar · View at Scopus
  220. D. G. Hardie, “AMPK: a target for drugs and natural products with effects on both diabetes and cancer,” Diabetes, vol. 62, no. 7, pp. 2164–2172, 2013. View at Publisher · View at Google Scholar
  221. R. J. Shaw, K. A. Lamia, D. Vasquez et al., “Medicine: the kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin,” Science, vol. 310, no. 5754, pp. 1642–1646, 2005. View at Publisher · View at Google Scholar · View at Scopus
  222. M. Zang, A. Zuccollo, X. Hou et al., “AMP-activated protein kinase is required for the lipid-lowering effect of metformin in insulin-resistant human HepG2 cells,” Journal of Biological Chemistry, vol. 279, no. 46, pp. 47898–47905, 2004. View at Publisher · View at Google Scholar · View at Scopus
  223. L. Lantier, J. Fentz, R. Mounier, and et al, “AMPK controls exercise endurance, mitochondrial oxidative capacity and skeletal muscle integrity,” The FASEB Journal, pp. 3211–3224, Jul 2014. View at Google Scholar
  224. H. M. O'Neill, S. J. Maarbjerg, J. D. Crane et al., “AMP-activated protein kinase (AMPK) β1β2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 38, pp. 16092–16097, 2011. View at Publisher · View at Google Scholar · View at Scopus
  225. B. R. Barnes, S. Marklund, T. L. Steiler et al., “The 5′-AMP-activated protein kinase γ3 isoform has a key role in carbohydrate and lipid metabolism in glycolytic skeletal muscle,” Journal of Biological Chemistry, vol. 279, no. 37, pp. 38441–38447, 2004. View at Publisher · View at Google Scholar · View at Scopus
  226. M. Mahlapuu, C. Johansson, K. Lindgren et al., “Expression profiling of the γ-subunit isoforms of AMP-activated protein kinase suggests a major role for γ3 in white skeletal muscle,” The American Journal of Physiology: Endocrinology and Metabolism, vol. 286, no. 2, pp. E194–E200, 2004. View at Google Scholar · View at Scopus
  227. B. R. Barnes, C. L. Yun, T. L. Steiler et al., “Changes in exercise-induced gene expression in 5′-AMP-activated protein kinase γ3-null and γ3 R225Q transgenic mice,” Diabetes, vol. 54, no. 12, pp. 3484–3489, 2005. View at Publisher · View at Google Scholar · View at Scopus
  228. B. B. Zhang, G. Zhou, and C. Li, “AMPK: an emerging drug target for diabetes and the metabolic syndrome,” Cell Metabolism, vol. 9, no. 5, pp. 407–416, 2009. View at Publisher · View at Google Scholar · View at Scopus
  229. E. S. Buhl, N. Jessen, R. Pold et al., “Long-term AICAR administration reduces metabolic disturbances and lowers blood pressure in rats displaying features of the insulin resistance syndrome,” Diabetes, vol. 51, no. 7, pp. 2199–2206, 2002. View at Publisher · View at Google Scholar · View at Scopus
  230. 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
  231. Z. Yang, X. Wang, Y. He et al., “The full capacity of AICAR to reduce obesity-induced inflammation and insulin resistance requires Myeloid SIRT1,” PLoS ONE, vol. 7, no. 11, Article ID e49935, 2012. View at Publisher · View at Google Scholar · View at Scopus
  232. Y. Izumiya, T. Hopkins, C. Morris et al., “Fast/glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice,” Cell Metabolism, vol. 7, no. 2, pp. 159–172, 2008. View at Publisher · View at Google Scholar · View at Scopus
  233. R. Feil and M. F. Fraga, “Epigenetics and the environment: emerging patterns and implications,” Nature Reviews Genetics, vol. 13, no. 2, pp. 97–109, 2012. View at Publisher · View at Google Scholar · View at Scopus
  234. H. T. Bjornsson, M. Daniele Fallin, and A. P. Feinberg, “An integrated epigenetic and genetic approach to common human disease,” Trends in Genetics, vol. 20, no. 8, pp. 350–358, 2004. View at Publisher · View at Google Scholar · View at Scopus
  235. M. F. Fraga, E. Ballestar, M. F. Paz et al., “Epigenetic differences arise during the lifetime of monozygotic twins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 30, pp. 10604–10609, 2005. View at Publisher · View at Google Scholar · View at Scopus
  236. A. P. Bird, “DNA methylation and the frequency of CpG in animal DNA,” Nucleic Acids Research, vol. 8, no. 7, pp. 1499–1504, 1980. View at Publisher · View at Google Scholar · View at Scopus
  237. S. Saxonov, P. Berg, and D. L. Brutlag, “A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 5, pp. 1412–1417, 2006. View at Publisher · View at Google Scholar · View at Scopus
  238. R. J. Klose and A. P. Bird, “Genomic DNA methylation: The mark and its mediators,” Trends in Biochemical Sciences, vol. 31, no. 2, pp. 89–97, 2006. View at Publisher · View at Google Scholar · View at Scopus
  239. R. Ribel-Madsen, M. F. Fraga, S. Jacobsen et al., “Genome-wide analysis of DNA methylation differences in muscle and fat from monozygotic twins discordant for type 2 diabetes,” PLoS ONE, vol. 7, no. 12, Article ID e51302, 2012. View at Publisher · View at Google Scholar · View at Scopus
  240. R. Barres, H. Kirchner, M. Rasmussen et al., “Weight loss after gastric bypass surgery in human obesity remodels promoter methylation,” Cell Reports, vol. 3, no. 4, pp. 1020–1027, 2013. View at Publisher · View at Google Scholar · View at Scopus
  241. J. J. Issa, “DNA methylation as a therapeutic target in cancer,” Clinical Cancer Research, vol. 13, no. 6, pp. 1634–1637, 2007. View at Publisher · View at Google Scholar · View at Scopus
  242. T. Chen and S. Y. Dent, “Chromatin modifiers and remodellers: regulators of cellular differentiation,” Nature Reviews Genetics, vol. 15, no. 2, pp. 93–106, 2014. View at Google Scholar
  243. P. Asp, R. Blum, V. Vethantham et al., “Genome-wide remodeling of the epigenetic landscape during myogenic differentiation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 22, pp. E149–E158, 2011. View at Publisher · View at Google Scholar · View at Scopus
  244. M. P. Creyghton, A. W. Cheng, G. G. Welstead et al., “Histone H3K27ac separates active from poised enhancers and predicts developmental state,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 50, pp. 21931–21936, 2010. View at Publisher · View at Google Scholar · View at Scopus
  245. B. Lenhard, A. Sandelin, and P. Carninci, “Metazoan promoters: emerging characteristics and insights into transcriptional regulation,” Nature Reviews Genetics, vol. 13, no. 4, pp. 233–245, 2012. View at Publisher · View at Google Scholar · View at Scopus
  246. J. F. Martin, C. S. Johnston, C. Han, and D. C. Benyshek, “Nutritional origins of insulin resistance: a rat model for diabetes- prone human populations,” The Journal of Nutrition, vol. 130, no. 4, pp. 741–744, 2000. View at Google Scholar · View at Scopus
  247. D. C. Benyshek, C. S. Johnston, and J. F. Martin, “Glucose metabolism is altered in the adequately-nourished grand-offspring (F3 generation) of rats malnourished during gestation and perinatal life,” Diabetologia, vol. 49, no. 5, pp. 1117–1119, 2006. View at Publisher · View at Google Scholar · View at Scopus
  248. M. Thamotharan, M. Garg, S. Oak et al., “Transgenerational inheritance of the insulin-resistant phenotype in embryo-transferred intrauterine growth-restricted adult female rat offspring,” American Journal of Physiology: Endocrinology and Metabolism, vol. 292, no. 5, pp. E1270–E1279, 2007. View at Publisher · View at Google Scholar · View at Scopus
  249. E. Zambrano, P. M. Martínez-Samayoa, C. J. Bautista et al., “Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation,” Journal of Physiology, vol. 566, no. 1, pp. 225–236, 2005. View at Publisher · View at Google Scholar · View at Scopus
  250. N. Raychaudhuri, S. Raychaudhuri, M. Thamotharan, and S. U. Devaskar, “Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring,” Journal of Biological Chemistry, vol. 283, no. 20, pp. 13611–13626, 2008. View at Publisher · View at Google Scholar · View at Scopus
  251. K. Hartil, P. M. Vuguin, M. Kruse et al., “Maternal substrate utilization programs the development of the metabolic syndrome in male mice exposed to high fat in utero,” Pediatric Research, vol. 66, no. 4, pp. 368–373, 2009. View at Publisher · View at Google Scholar · View at Scopus
  252. A. Samuelsson, P. A. Matthews, M. Argenton et al., “Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: A novel murine model of developmental programming,” Hypertension, vol. 51, no. 2, pp. 383–392, 2008. View at Publisher · View at Google Scholar · View at Scopus
  253. M. Tachibana, M. Nozaki, N. Takeda, and Y. Shinkai, “Functional dynamics of H3K9 methylation during meiotic prophase progression,” EMBO Journal, vol. 26, no. 14, pp. 3346–3359, 2007. View at Publisher · View at Google Scholar · View at Scopus
  254. T. Inagaki, M. Tachibana, K. Magoori et al., “Obesity and metabolic syndrome in histone demethylase JHDM2a-deficient mice,” Genes to Cells, vol. 14, no. 8, pp. 991–1001, 2009. View at Publisher · View at Google Scholar · View at Scopus
  255. K. Tateishi, Y. Okada, E. M. Kallin, and Y. Zhang, “Role of Jhdm2a in regulating metabolic gene expression and obesity resistance,” Nature, vol. 458, no. 7239, pp. 757–761, 2009. View at Publisher · View at Google Scholar · View at Scopus
  256. S. Glaser, S. Lubitz, K. L. Loveland et al., “The histone 3 lysine 4 methyltransferase, Mll2, is only required briefly in development and spermatogenesis,” Epigenetics & Chromatin, vol. 2, no. 1, article 5, 2009. View at Publisher · View at Google Scholar
  257. M. Goldsworthy, N. L. Absalom, D. Schröter et al., “Mutations in Mll2, an H3K4 methyltransferase, result in insulin resistance and impaired glucose tolerance in mice,” PLoS ONE, vol. 8, no. 6, Article ID e61870, 2013. View at Publisher · View at Google Scholar · View at Scopus