Muscle development and obesity: Is there a relationship?

Organogenesis

Volumn 4, Issue 3, 2008, Pages

  Maltin, Charlotte A ^a  

^a ROBERT GORDON UNIVERSITY   (United Kingdom)

Author keywords

Fetal; FOXO; Growth; Muscle fibre type specification; Myogenesis; Myogenic regulatory factors; Obesity; PGC 1 ; PPAR undernutrition

Indexed keywords

FATTY ACID; FIBROBLAST GROWTH FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR NFAT; WNT PROTEIN;

ADAPTATION; CARBOHYDRATE METABOLISM; FATTY ACID OXIDATION; HERITABILITY; HUMAN; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE DEVELOPMENT; MUSCLE INNERVATION; MUSCLE METABOLISM; NONHUMAN; OBESITY; PRENATAL EXPOSURE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SOMITE;

ANIMALIA;

EID: 50849143177     PISSN: 15476278     EISSN: 15558592     Source Type: Journal    
DOI: None     Document Type: Review

References (148)

1. McMillen IC, MacLaughlin SM, Muhlhausler BS, Gentili S, Duffield JL, Morrison JL. Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic Clin Pharmacol Toxicol 2008; 102:82-9.
2. Hanson MA, Gluckman PD. Developmental origins of health and disease: new insights. Basic Clin Pharmacol Toxicol 2008; 102:90-3.
3. Gluckman PD, Lillycrop KA, Vickers MH, Pleasants AB, Phillips ES, Beedle AS, Burdge GC, Hanson MA. Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc Natl Acad Sci USA 2007; 104:12796-800.
4. Maltin CA, Delday MI, Sinclair KD, Steven J, Sneddon AA. Impact of manipulations of myogenesis in utero in the performance of adult muscle. Reproduction 2001; 122:359-74.
5. Rivero JLL, Barrey E. Heritabilities and genetic and phenotypic parameters for gluteus medius muscle fibre type composition, fibre size and capillaries in purebred Spanish horses. Livestock Production Science 2001; 72:233-41.
6. Renard G, Jurie C, Robelin J, Picard B, Geay Y, Menissier F. Genetic variability of muscle biological characteristics of young Limousin bulls. Genet Sel Evol 1995; 27:287-98.
7. Komi PV, Viitasalo JH, Havu M, Thorstensson A, Sjodin B, Karlsson J. Skeletal muscle fibres and muscle enzyme activites in monozygous and dizyogous twins of both sexes. Acta Physiol Scand 1977; 100:385-92.
8. Bouchard C, Simoneau JA, Lortie G, Boulay MR, Marcotte M, Thibault MC. Genetic effects in human skeletal muscle fibre type distribution and enzyme activities. Can J Physiol Pharmacol 1986; 64:1245-51.
9. Abernethy PJ, Thayer R, Taylor AW. Acute and chronic responses of skeletal muscle to endurance and sprint exercise. A review. Sports Med 1990; 10:365-89.
10. Ross A, Leveritt M. Long term metabolic and skeletal muscle adaptations to short-sprint training: implications for sprint training and tapering. Sports Med 2001; 31:1063-82.
11. Costill DL, Fink WJ, Pollock ML. Muscle fibre composition and enzyme activities of elite distance runners. Med Sci Sports 1976; 8:96-100.
12. Martin WH, 3rd. Effects of acute and chronic exercise on fat metabolism. Exerc Sport Sci Rev 1996; 24:203-31.
13. Tanner CJ, Barakat HA, Lynis Dohm G, Pories WJ, MacDonald KG, Cunningham PRG, Swanson MS, Houmard JA. Muscle fibre type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 2002; 282:1191-6.
14. Oberbach A, Bossenz Y, Lehmann S, Niebauer J, Adams V, Paschke R, Schon MR, Bluher M, Punkt K. Altered fibre distribution and fibre specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 2006; 29:895-900.
15. Adachi T, Kikuchi N, Yasuda K, Anahara R, Gu N, Matsunaga T, Yamamura T, Mori C, Tsujimoto G, TsudaK, Ishihara A. Fibre type distribution and gene expression levels of both succinate dehydrogenase and peroxisome proliferator-activated receptor-gamma coactivator-1alpha of fibres in the soleus muscle of Zucker diabetic fatty rats. Exp Physiol 2007; 92:449-55.
16. Berggren J, Boyle KE, Chapman WH, Houmard JA. Skeletal muscle lipid oxidation and obesity: influence of weight loss and exercise. Am J Physiol Endocrinol Metab 2008; [E pub before print] doi:10.1152/ajpendo.00354.2007.
17. Mensink M, Hesselink MK, Russell AP, Schaart G, Sels JP, Schrauwen P. Improved skeletal muscle oxidative enzyme activity and restoration of PGC-1alpha and PPAR beta/delta gene expression upon rosiglitazone treatment in obese patients with type 2 diabetes mellitus. Int J Obes (Lond) 2007; 8:1302-10.
18. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, Bayuga-Ocampo CR, Ham J, Kang H, Evans RM. Regulation of muscle fibre type and running endurance by PPARδ. PLoS Biology 2004; 2:294.
19. Ryder JW, Bassel-Duby R, Olsen EN, Zierath JR. Skeletal muscle reprogramming by activation of calcineurin improves insulin action on metabolite pathways. J Biol Chem 2003; 278:44298-304.
20. Bruce CR, Anderson MJ, Carey AL, Newman DG, Bonen A, Kriketos AD, Cooney GJ, Hawley JA. Muscle oxidative capacity is a better predictor of insulin sensitivity that lipid status. J Clin Endocrinol Metab 2003; 88:5444-51.
21. Lillioja S, Young AA, Culter CL, Ivy JL, Abbott WG, Zawadzki JK, Yki-Järvinen H, Christin L, Secomb TW, Bogardus C. Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 1987; 80:415-24.
22. Reilly SM, Lee CH. PPARδ as a therapeutic target in metabolic disease. FEBS letts 2008; 582:26-31.
23. Luquet S, Lopez-Soriano J, Holst D, Fredenrich A, Melki J, Rassoulzadegan M, Grimaldi PA. Peroxisome proliferator-activated receptor delta controls muscle development and oxidative capability. FASEB J 2003; 17:2299-301.
24. Krämer DK, Ahlsén M, Norrbom J, Jansson E, Hjeltnes N, Gustafsson T, Krook A. Human skeletal muscle fibre type variations correlate with PPAR alpha, PPAR delta and PGC-1 alpha mRNA. Acta Physiol 2006; 188:207-16.
25. Christ B, Huang R, Scaal M. Amniote somite derivatives. Dev Dyn 2007; 236:2382-96.
26. Buckingham M, Bajard L, Chang T, Daubas P, Hadchouel J, Meilhac S, Montarras D, Rocancourt D, Relaix F. The formation of skeletal muscle from somite to limb. J Anat 2003; 202:59-68.
27. Buckingham M. Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr Opin Genet Dev 2006; 16:525-32.
28. Kalcheim C, Ben-Yair R. Cell rearrangements during development of the somite and its derivatives. Curr Opin Genet Dev 2005; 15:371-80.
29. Francis-West PH, Antoni L, Anakwe K. Regulation of myogenic differentiation in the developing limb bud. J Anat 2003; 202:69-81.
30. Te Kronnie G, Reggiani C. Skeletal muscle fibre type specification during embryonic development J Muscle Res Cell Motil 2002; 23:65-9.
31. Bergstrom DA, Tapscott SJ. Molecular distinction between specification and differentiation in the myogenic basic helix-loop-helix transcription factor family. Mol Cell Biol 2001; 21:2404-12.
32. Kassar Duchossoy L, Gayraud-Morel B, Gomes D, Rocancourt D, Buckingham M, Shinin V, Tajbakhsh S. Mrf 4 determines skeletal muscle identity in Myf5:MyoD double-mutant mice. Nature 2004; 431:466-71.
33. Hadchouel J, Carvajal JJ, Daubas P, Bajard L, Chang T, Rocancourt D, Cox D, Summerbell D, Tajbakhsh S, Rigby PW, Buckingham M. Analysis of a key regulatory region upstream of the Myf5 gene reveals multiple phases of myogenesis, orchestrated at each site by a combination of elements dispersed throughout the locus. Development 2003; 130:3415-26.
34. Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, Jaenisch R. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 1993; 75:1351-9.
35. Tapscott SJ. The circuitry of a master switch: MyoD and the regulation of skeletal muscle gene transcription. Development 2005; 132:2685-95.
36. Davis RL, Weintraub H, Lassar AB. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 1987; 51:987-1000.
37. Valdez MR, Richardson JA, Klein WH, Olson EN. Failure of Myf5 to support myogenic differentiation without myogenin, MyoD, and MRF4. Dev Biol 2000; 219:287-98.
38. Summerbell D, Halai C, Rigby PWJ. Expression of the myogenic regulatory factor Mrf4 precedes or is contemporaneous with that of Myf5 in the somatic bud. Mech Dev 2002; 117:331-5.
39. McKinsey TA, Zhang CL, Olsen EN. Signaling chromatin to make muscle. Curr Opin Cell Biol 2002; 14:763-72.
40. Hughes SM, Taylor JM, Tapscott SJ, Gurley CM, Carter WJ, Peterson CA. Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones. Development 1993; 118:1137-47.
41. Dunglisson GF, Scotting PJ, Wigmore PM. Rat embryonic myoblasts are restricted to forming primary fibres while later myogenic populations are pluripotent. Mech Dev 1999; 87:11-9.
42. Pin CL, Hrycyshyn AW, Rogers KA, Rushlow WJ, Merrifield PA. Embryonic and fetal rat myoblasts form different muscle fiber types in an ectopic in vivo environment. Dev Dyn 2002; 224:253-66.
43. Wigmore PM, Dunglisson GF. The generation of fibre diversity during myogenesis. Int J Dev Biol 1998; 42:117-25.
44. Wilson SJ, McEwan JC, Sheard PW, Harris AJ. Early stages of myogenesis in a large mammal: formation of successive generations of myotubes in sheep tibialis cranialis muscle. J Muscle Res Cell Motil 1992; 13:534-50.
45. Barbet JP, Thornell LE, Butler-Browne GS. Immunocytochemical characterisation of two generations of fibres during the development of the human quadriceps muscle. Mech Dev 1991; 35:3-11.
46. Duxson MJ, Sheard PW. Formation of new myoblasts occurs exclusively at the multiple innervations zones of and embryonic large muscle. Dev Dyn 1995; 204:391-405.
47. Drager A, Wees AG, Fitzsimons RB. Primary secondary and tertiary myotubes in developing skeletal muscle a new approach to the analysis of human myogenesis. J Neurol Sci 1987; 81:19-43.
48. Stockdale FE. Mechanisms of formation of muscle fibre types. Cell Struct Funct 1997; 22:37-43.
49. Hughes SM, Blau HM. Muscle fiber pattern is independent of cell lineage in postnatal rodent development. Cell 1992; 68:659-71.
50. DiMario JX, Fernyak SE, Stoackdale FE. Myoblasts transferred to the limbs of embryos are committed to specific fibre fates. Nature 1993; 362:165-7.
51. Van Swearingen J, Lance-Jones C. Slow and fast muscle fibres are preferentially derived from myoblasts migrating into the chick limb bud at different developmental times. Dev Biol 1995; 170:321-37.
52. Nikovits W, Cann GM, Huang R, Christ B, Stockdale FE. Patterning of fast and slow fibres within embryonic muscles is established independantly of signals from the surrounding mesenchyme. Development 2001; 128:2537-44.
53. Cho M, Webster SG, Blau HM. Evidence for myoblast-extrinsic regulation of slow myosin heavy chain expression during fibre formation in embryonic development. J Cell Biol 1993; 121:795-810.
54. Robson LG, Hughes SM. Local signals in the chick limb bud can override myoblast lineage commitment; induction of slow myosin heavy chain in fast myoblasts. Mech Dev 1999; 85:59-71.
55. Kardon G, Campbell JK, Tabin CJ. Local extrinsic signals determine muscle and endothelial cell fate and patterning in the vertebrate limb. Dev Cell 2002; 3:533-45.
56. Norris W, Neyt C, Ingham PW, Currie PD. Slow muscle induction by Hedgehog signalling in vitro. J Cell Sci 2000; 113:2695-703.
57. Blagden CS, Currie PD, Ingham PW, Hughes SM. Hedgehog induction of zebrafish slow muscle is mediated by Sonic hedgehog. Genes Dev 1997; 11:2163-75.
58. Kruger M, Mennerich D, Fees S, Schafer R, Mundios S, Braun T. Sonic hedgehog is a survival factor for hypaxial muscle during mouse development. Development 2001; 128:743-52.
59. Bren-Mattison Y, Olwin BB. Sonic hedgehog inhibits the terminal differentiation of limb myoblasts committed to the slow lineage. Dev Biol 2002; 242:130-48.
60. Li X, Blagden CS, Bildsoe H, Bonnin MA, Duprez D, Hughes SM. Hedgehog can derive terminal differentiation of amniote slow skeletal muscle. BMC Dev Biol 2004; 4:9.
61. Baxendale S, Davison C, Muxworthy C, Wolff C, Ingham PW, Roy S. The B-cell maturation factor Blimp-1 specifies vertebrate slow-twitch muscle fibre identity in response to Hedgehog signalling. Nature Genetics 2004; 36:88-93.
62. Lavine KJ, White AC, Park C, Smith CS, Choi K, Long F, Hui C, Ornitz DM. Fibroblast growth factor signals regulate a wave of Hedgehog activation that is essential for coronary vascular development. Genes Dev 2006; 20:1651-66.
63. Armand AS, Laziz I, Chanoine C. FGF6 in myogenesis. Biochim Biophys Acta 2006; 1763:773-8.
64. Kahane N, Cinnamon Y, Bachelet I, Kalcheim C. The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development. Development 2001; 128:2187-98.
65. Katoh M, Katoh M. Cross-talk of WNT and FGF signalling pathways at GSK3beta to regulate beta catenin and SNAIL signalling cascades. Cancer Biol Ther 2006; 5:1059-64.
66. Anakwe K, Robson L, Hadley J, Buxton P, Church V, Allen S, Hartmann C, Harfe B, Nohno T, Brown AM, Evans DJ, Francis-West P. Wnt signalling regulates myogenic differentiation in the developing avian wing. Development 2003; 130:3503-14.
67. Takata H, Trada K, Oka H, Sunada Y, Moriguchi T, Nohno T. Involvement of Wnt4 signaling during myogenic proliferation and differentiation of skeletal muscle. Dev Dyn 2007; 236:2800-7.
68. Lee SJ. Quadrupling muscle mass in mice by targeting TGFbeta signaling pathways. PLoS ONE 2007; 2:789.
69. Amthor H, Macharia R, Navarrete R, SChuelke M, Brown SC, Otto A, Voit T, Muntoni F, Vbrova G, Partridge T, Zammit P, Bunger L, Patel K. Lack of myostatin results in excessive muscle growth but impaired force generation. PNAS 2007; 104:1835-40.
70. Almeida M, Han L, Martin-Millan M, O'Brien CA, Manolagas SC. Oxidative stress antagonizes Wnt signalling in osteoblast precursors by diverting β-catenin from TCF- to FOXO-mediated transcription. J Biol Chem 2007; 282:27298-305.
71. Nakae J, Oki M, Cao Y. The FOXO transcription factors and metabolic regulation. FEBS letts 2008; 582:54-67.
72. Dowell P, Otto T, Adi S, Lane DM. Convergence of the peroxisome proliferator-activated receptor γ and Foxo1 signaling pathways. J Biol Chem 2003; 278:45485-91.
73. Southgate RJ, Bruce CR, Carey AL, Steinberg GR, Walder K, Monks R, Watt MJ, Hawley JA, Birnbaum MJ, Febbraio MA. PGC-1alpha gene expression is downregulated by Akt- mediated phosphorylation and nuclear exclusion of FoxO1 in insulin-stimulated skeletal muscle. FASEB J 2005; 19:2072-4.
74. Daitoku H, Yamagata K, Matsuzakai H, Hatta M, Fukamizu A. Regulation of PGC-1 promoter activity by protein kinase B and the forkhead transcription factor FKHR. Diabetes 2003; 52:642-9.
75. Kitamura T, Kitamura YI, Funahashi Y, Shawber CJ, Castrillon DH, Kollipara R, DePinho RA, Kitajewski J, Accli D. A Foxo/Notch pathway control myogenic differentiation and fibre type specification. J Clin Invest 2007; 117:2477-85.
76. Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T, Mochida K, Hata T, Matsuda J, Aburatani H, Nishino I, Ezaki O. Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, downregulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 2004; 279:41114-23.
77. Yang YJ, Pang WJ, Bai L, Yang GS. Expression of FoxO1 mRNA in muscle tissue of Bamei, Landrace and Landrace x Bamei. Yi Chuan 2008 30:185-9.
78. Allen DL, UntermanTG. Regulation of myostatin expression and myoblast differentiation by FoxO and SMAD transcription factors. Am J Physiol Cell Physiol 2007; 292:188-99.
79. Bois PRJ, Grosveld GC. FKHR (FOXO1a) is required for myotubes fusion of primary mouse myoblasts. The EMBO J 2003; 22:1147-57.
80. Hribal ML, Nakae J, Kitamura T, Shutter JR, Accili D. Regulation of insulin-like growth factor-dependent myoblast differentiation by Foxo forkhead transcription factors. J Cell Biol 2003; 162:535-41.
81. Wu AL, Kim JH, Zhang C, Unterman TG, Chen J. Forkhead Box Protein O1 Negatively Regulates Skeletal Myocyte Differentiation through Degradation of Mammalian Target of Rapamycin Pathway Components. Endocrinology 2008; 149:1407-14.
82. Finck BN, Kelly DP. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest 2006; 116:615-22.
83. Knutti D, Kralli A. PGC-1, a versatile coactivator. Trends Endocrinol Metab 2001; 12:360-5.
84. Chang JH, Lin KH, Shih CH, Chang YJ, Chi HC, Chen SL. Myogenic basic helix-loophelix proteins regulate the expression of peroxisomal proliferator- activated receptor-γ coactivator-1α. Endocrinology 2006; 147:3093-106.
85. Czbryt MP, McAnally J, Fishman GI, Olson EN. Regulation of peroxisome proliferatoractivated receptor γ coactivator 1α (PGC-1α) and mitochondrial function by MEF2 and HDAC5. PNAS 2003; 100:1711-6.
86. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002; 418:797-801.
87. Mortensen OH, Frandsen L, Schjerling P, Nishimura E, Grunnet N. PGC-1alpha and PGC-1beta have both similar and distinct effects on myofiber switching toward an oxidative phenotype. Am J Physiol Endocrinol Metab 2006; 291:807-16.
88. Bayol SA, Simbi BH, Stickland NC. A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 2005; 567:951-61.
89. Singh J, Verma NK, Kansagra SM, Kate BN, Dey CS. Altered PPARgamma expression inhibits myogenic differentiation in C2C12 skeletal muscle cells. Mol Cell Biochem 2007; 294:163-71.
90. Hondares E, Pineda-Torra I, Iglesias R, Staels B, Villarroya F, Giralt M. PPARdelta, but not PPARalpha, activates PGC-1alpha gene transcription in muscle. Biochem Biophys Res Commun 2007; 354:1021-7.
91. Schuler M, Ali F, Chambon C, Duteil D, Bornert JM, Tardivel A, Desvergne B, Wahli W, Chambon P, Metzger D. PGC1alpha expression is controlled in skeletal muscles by PPARbeta, whose ablation results in fiber-type switching, obesity, and type 2 diabetes. Cell Metab 2006; 4:407-14.
92. Gaudel C, Grimaldi PA. Metabolic Functions of Peroxisome Proliferator-Activated Receptor beta/delta in Skeletal Muscle. PPAR Res 2007; 2007:86394.
93. Grimaldi PA. Roles of PPARdelta in the control of muscle development and metabolism. Biochem Soc Trans 2003; 31:1130-2.
94. Luquet S, Lopez-Soriano J, Holst D, Fredenrich A, Melki J, Rassoulzadegan M, Grimaldi PA. Peroxisome proliferator-activated receptor delta controls muscle development and oxidative capability. FASEB J 2003; 17:2299-301.
95. Tanaka T, Yamamoto J, Iwasaki S, Asaba H, Hamura H, Ikeda Y, Watanabe M, Magoori K, Ioka RX, Tachibana K, Watanabe Y, Uchiyama Y, Sumi K, Iguchi H, Ito S, Doi T, Hamakubo T, Naito M, Auwerx J, Yanagisawa M, Kodama T, Sakai J. Activation of peroxisome proliferator-activated receptor delta induces fatty acid beta-oxidation in skeletal muscle and attenuates metabolic syndrome. Proc Natl Acad Sci USA 2003; 100:15924-9.
96. Friday BB, Horsley V, Pavlath GK. Calcineurin activity is required for the initiation of skeletal muscle differentiation. J Cell Biol 2000; 149:657-66.
97. Schulz RA, Yutzey KE. Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development. Dev Biol 2004; 266:1-16.
98. Chin ER, Olson EN, Richardson JA, Yang Q, Humphries C, Shelton JM, Wu H, Zhu W, Bassel-Duby R, Williams RS. A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 1998; 12:2499-509.
99. Swoap SJ, Hunter RB, Stevenson EJ, Felton HM, Kansagra NV, Lang JM, Esser KA, Kandarian SC. The calcineurin-NFAT pathway and muscle fiber-type gene expression. Am J Physiol Cell Physiol 2000; 279:915-24.
100. Talmadge RJ, Otis JS, Rittler MR, Garcia ND, Spencer SR, Lees SJ, Naya FJ. Calcineurin activation influences muscle phenotype in a muscle-specific fashion. BMC Cell Biol 2004; 28:5-28.
101. Sakuma K, Nishikawa J, Nakao R, Watanabe K, Totsuka T, Nakano H, Sano M, Yasuhara M. Calcineurin is a potent regulator for skeletal muscle regeneration by association with NFATc1 and GATA-2. Acta Neuropathol 2003; 105:271-80.
102. Bigard X, Sanchez H, Zoll J, Mateo P, Rousseau V, Veksler V, Ventura-Clapier R. Calcineurin Co-regulates contractile and metabolic components of slow muscle phenotype. J Biol Chem 2000; 275:19653-60.
103. da Costa N, Edgar J, Ooi PT, Su Y, Meissner JD, Chang KC. Calcineurin differentially regulates fast myosin heavy chain genes in oxidative muscle fibre type conversion. Cell Tissue Res 2007; 329:515-27.
104. Friday BB, Mitchell PO, Kegley KM, Pavlath GK. Calcineurin initiates skeletal muscle differentiation by activating MEF2 and MyoD. Differentiation 2003; 71:217-27.
105. Oh M, Rybkin II, Copeland V, Czubryt MP, Shelton JM, van Rooij E, Richardson JA, Hill JA, De Windt LJ, Bassel-Duby R, Olson EN, Rothermel BA. Calcineurin is necessary for the maintenance but not embryonic development of slow muscle fibers. Mol Cell Biol 2005; 25:6629-38.
106. Wu H, Rothermel B, Kanatous S, Rosenberg P, Naya FJ, Shelton JM, Hutcheson KA, DiMaio JM, Olson EN, Bassel-Duby R, Williams RS. Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway. EMBO J 2001; 20:6414-23.
107. Beals CR, Sheridan CM, Turek CW, Gardner P, Crabtree GR. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 1997; 275:1930-4.
108. Adachi S, Amasaki Y, Miyatake S, Arai N, Iwata M. Successive expression and activation of NFAT family members during thymocyte differentiation. J Biol Chem 2000; 275:14708-16.
109. Delling U, Tureckova J, Lim HW, De Windt LJ, Rotwein P, Molkentin JD. A calcineurin-NFATc3-dependent pathway regulates skeletal muscle differentiation and slow myosin heavy-chain expression. Mol Cell Biol 2000; 20:6600-11.
110. Kegley KM, Gephart J, Warren GL, Pavlath GK. Altered primary myogenesis in NFATC3(-/-) mice leads to decreased muscle size in the adult. Dev Biol 2001; 232:115-26.
111. Horsley V, Friday BB, Matteson S, Kegley KM, Gephart J, Pavlath GK. Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. J Cell Biol 2001; 153:329-38.
112. Friday BB, Pavlath GK. A calcineurin- and NFAT-dependent pathway regulates Myf5 gene expression in skeletal muscle reserve cells. J Cell Sci 2000; 114:303-10.
113. Serrano AL, Murgia M, Pallafacchina G, Calabria E, Coniglio P, Lømo T, Schiaffino S. Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growth. Proc Natl Acad Sci USA 2001; 98:13108-13.
114. Hughes DS, Schade RR, Ontell M. Ablation of the fetal mouse spinal cord: the effect on soleus muscle cytoarchitecture. Dev Dyn 1992; 193:164-74.
115. Madhavan R, Zhao XT, Chan F, Wu Z, Peng HB. The involvement of calcineurin in acetylcholine receptor redistribution in muscle. Mol Cell Neurosci 2003; 23:587-99.
116. Rehfeldt C, Kuhn G. Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J Anim Sci 2006; 84:113-23.
117. Quigley SP, Kleemann DO, Kakar MA, Owens JA, Nattrass GS, Maddocks S, Walker SK. Myogenesis in sheep is altered by maternal feed intake during the peri-conception period. Anim Reprod Sci 2005; 87:241-51.
118. Maxfield EK, Sinclair KD, Broadbent PJ, McEvoy TG, Robinson JJ, Maltin CA. Shortterm culture of ovine embryos modifies fetal myogenesis. Am J Physiol 1998; 274:1121-3.
119. Maxfield EK, Sinclair KD, Dunne LD, Broadbent PJ, Robinson JJ, Stewart E, Kyle DG, Maltin CA. Temporary exposure of ovine embryos to an advanced uterine environment does not affect fetal weight but alters fetal muscle development. Biol Reprod 1998; 59:321-5.
120. Zhu MJ, Ford SP, Means WJ, Hess BW, Nathanielsz PW, Du M. Maternal nutrient restriction affects properties of skeletal muscle in offspring. J Physiol 2006; 575:241-50.
121. Ford SP, Hess BW, Schwope MM, Nijland MJ, Gilbert JS, Vonnahme KA, Means WJ, Han H, Nathanielsz PW. Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. J Anim Sci 2007; 85:1285-94.
122. Fahey AJ, Brameld JM, Parr T, Buttery PJ. The effect of maternal undernutrition before muscle differentiation on the muscle fiber development of the newborn lamb. J Anim Sci 2005; 83:2564-71.
123. Daniel ZC, Brameld JM, Craigon J, Scollan ND, Buttery PJ. Effect of maternal dietary restriction during pregnancy on lamb carcass characteristics and muscle fiber composition. J Anim Sci 2007; 85:1565-76.
124. Tollefsen SE, Lajara R, McCusker RH, Clemmons DR, Rotwein P. Insulin-like growth factors (IGF) in muscle development. Expression of IGF-I, the IGF-I receptor, and an IGF binding protein during myoblast differentiation. J Biol Chem 1989; 264:13810-7.
125. 2+- dependent calcineurin signalling pathway. Nature 1999; 400:576-81.
126. Espinosa A, Estrada M, Jaimovich E. IGF-I and insulin induce different intracellular calcium signals in skeletal muscle cells. J Endocrinol 2004; 182:339-52.
127. Osgerby JC, Wathes DC, Howard D, Gadd TS. The effect of maternal undernutrition on the placental growth trajectory and the uterine insulin-like growth factor axis in the pregnant ewe. J Endocrinol 2004; 182:89-103.
128. Heasman L, Brameld J, Mostvn A, Budge H, Dawson J, Buttery P, Stephenson T, Symonds ME. Maternal nutrient restriction during early to mid gestation alters the relationship between insulin-like growth factor I and bodyweight at term in fetal sheep. Reprod Fertil Dev 2000; 12:345-50.
129. Brameld JM, Mostyn A, Dandrea J, Stephenson TJ, Dawson JM, Buttery PJ, Symonds ME. Maternal nutrition alters the expression of insulin-like growth factors in fetal sheep liver and skeletal muscle. J Endocrinol 2000; 167:429-37.
130. Dong F, Ford SP, Fang CX, Nijland MJ, Nathanielsz PW, Ren J. Maternal nutrient restriction during early to mid gestation upregulates cardiac insulin-like growth factor (IGF) receptors associated with enlarged ventricular size in fetal sheep. Growth Horm IGF Res 2005; 15:291-9.
131. Merrick D, Ting T, Stadler LK, Smith J. A role for Insulin-like growth factor 2 in specification of the fast skeletal muscle fibre. BMC Dev Biol 2007; 7:65.
132. Whipple G, Koohmaraie M. Effects of lamb age, muscle type and 24 hour activity of endogenous proteinases on post-mortem proteolysis. J. Anim Sci 1992; 70:798-804.
133. Kocamis H, Gahr SA, Batelli L, Hubbs AF, Killefer J. IGF-I, IGF-II, and IGF-receptor-1 transcript and IGF-II protein expression in myostatin knockout mice tissues. Muscle Nerve 2002; 26:55-63.
134. Yamaguchi A, Fujikawa T, Tateoka M, Soya H, Sakuma K, Sugiura T, Morita I, Ikeda Y, Hirai T. The expression of IGF-I and myostatin mRNAs in skeletal muscle of hypophysectomized and underfed rats during postnatal growth. Acta Physiol (Oxf) 2006; 186:291-300.
135. Rosenthal SM, Hsiao D, Silverman LA. An insulin-like growth factor-II (IGF-II) analog with highly selective affinity for IGF-II receptors stimulates differentiation, but not IGF-I receptor downregulation in muscle cells. Endocrinology 1994; 135:38-44.
136. Florini JR, Ewton DZ, Coolican SA. Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev 1996; 17:481-517.
137. Machida S, Spangenburg EE, Booth FW. Forkhead transcription factor FoxO1 transduces insulin-like growth factor's signal to p27Kip1 in primary skeletal muscle satellite cells. J Cell Physiol 2003; 196:523-31.
138. Spangenburg EE, Bowles DK, Booth FW. Insulin-like growth factor-induced transcriptional activity of the skeletal alpha-actin gene is regulated by signaling mechanisms linked to voltage-gated calcium channels during myoblast differentiation. Endocrinology 2004; 145:2054-63.
139. Alfieri CM, Evans-Anderson HJ, Yutzey KE. Developmental regulation of the mouse IGF-I exon 1 promoter region by calcineurin activation of NFAT in skeletal muscle. Am J Physiol Cell Physiol 2007; 292:1887-94.
140. Ni YG, Wang N, Cao DJ, Sachan N, Morris DJ, Gerard RD, Kuro-O M, Rothermel BA, Hill JA. FoxO transcription factors activate Akt and attenuate insulin signaling in heart by inhibiting protein phosphatases. Proc Natl Acad Sci USA 2007; 104:20517-22.
141. Dwyer CM, Madgwick AJ, Ward SS, Stickland NC. Effect of maternal undernutrition in early gestation on the development of fetal myofibres in the guinea-pig. Reprod Fertil Dev 1995; 7:1285-92.
142. Wilson SJ, Ross JJ, Harris AJ. A critical period for formation of secondary myotubes defined by prenatal undernourishment in rats. Development 1988; 102:815-21.
143. Moughan PJ, Jacobson LH, Morel PC. A genetic upper limit to whole-body protein deposition in a strain of growing pigs. J Anim Sci 2006; 84:3301-9.
144. Gardner DS, Buttery PJ, Daniel Z, Symonds ME. Factors affecting birth weight in sheep: maternal environment. Reproduction 2007; 133:297-307.
145. Bee G. Effect of early gestation feeding, birth weight, and gender of progeny on muscle fiber characteristics of pigs at slaughter. J Anim Sci 2004; 82:826-36.
146. Wells JC, Chomtho S, Fewtrell MS. Programming of body composition by early growth and nutrition. Proc Nutr Soc 2007; 66:423-34.
147. Muaku SM, Thissen JP, Gerard G, Ketelslegers JM, Maiter D. Postnatal catch-up growth induced by growth hormone and insulin-like growth factor-I in rats with intrauterine growth retardation caused by maternal protein malnutrition. Pediatr Res 1997; 42:370-7.
148. Maltin CA, Steven J, Warkup CC. Assay for Duroc Muscle fibre type. International application published under the patent cooperation treaty (PCT) 1998; WO 98/15837.