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Growing healthy muscles to optimise metabolic health into adult life

Published online by Cambridge University Press:  09 October 2014

S. A. Bayol ,
C. R. Bruce  and
G. D. Wadley
S. A. Bayol*
Affiliation:
School of Exercise and Nutrition Sciences, Centre for Physical Activity and Nutrition Research, Faculty of Health, Deakin University, Melbourne, VIC, Australia
C. R. Bruce
Affiliation:
School of Exercise and Nutrition Sciences, Centre for Physical Activity and Nutrition Research, Faculty of Health, Deakin University, Melbourne, VIC, Australia
G. D. Wadley
Affiliation:
School of Exercise and Nutrition Sciences, Centre for Physical Activity and Nutrition Research, Faculty of Health, Deakin University, Melbourne, VIC, Australia
*
*Address for correspondence: S. A. M. Bayol, School of Exercise and Nutrition Sciences, Centre for Physical Activity and Nutrition Research, Faculty of Health, Deakin University, Melbourne, VIC 3125, Australia. (Email stephanie.bayol@deakin.edu.au)
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Abstract

The importance of skeletal muscle for metabolic health and obesity prevention is gradually gaining recognition. As a result, interventions are being developed to increase or maintain muscle mass and metabolic function in adult and elderly populations. These interventions include exercise, hormonal and nutritional therapies. Nonetheless, growing evidence suggests that maternal malnutrition and obesity during pregnancy and lactation impede skeletal muscle development and growth in the offspring, with long-term functional consequences lasting into adult life. Here we review the role of skeletal muscle in health and obesity, providing an insight into how this tissue develops and discuss evidence that maternal obesity affects its development, growth and function into adult life. Such evidence warrants the need to develop early life interventions to optimise skeletal muscle development and growth in the offspring and thereby maximise metabolic health into adult life.

Keywords

maternal obesitymetabolismskeletal muscle development
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 5 , Issue 6 , December 2014 , pp. 420 - 434
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

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References

1. Gardner, DS, Rhodes, P. Developmental origins of obesity: programming of food intake or physical activity? Adv Exp Med Biol. 2009; 646, 83–93.CrossRefGoogle ScholarPubMed
2. Olefsky, JM. Insulin-stimulated glucose transport minireview series. J Biol Chem. 1999; 274, 1863.CrossRefGoogle ScholarPubMed
3. DeFronzo, RA, Jacot, E, Jequier, E, et al. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes. 1981; 30, 1000–1007.CrossRefGoogle ScholarPubMed
4. DeFronzo, RA, Tripathy, D. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care. 2009; 32(Suppl. 2), S157–S163.Google Scholar
5. Maltin, CA, Delday, MI, Sinclair, KD, Steven, J, Sneddon, AA. Impact of manipulations of myogenesis in utero on the performance of adult skeletal muscle. Reproduction. 2001; 122, 359–374.CrossRefGoogle ScholarPubMed
6. Rehfeldt, C, Fiedler, I, Dietl, G, Ender, K. Myogenesis and postnatal skeletal muscle cell growth as influenced by selection. Livest Prod Sci. 2000; 66, 177–188.Google Scholar
7. Phipps, K, Barker, DJ, Hales, CN, et al. Fetal growth and impaired glucose tolerance in men and women. Diabetologia. 1993; 36, 225–228.CrossRefGoogle ScholarPubMed
8. WHO. Obesity and overweight. Fact sheet number 311. 2013. Retrieved June 2014 from http://www.who.int/mediacentre/factsheets/fs311/en/ Google Scholar
9. ABS. Australian Health Survey: first results, ABS cat. no. 4364.0.55.001 2011–12, Australian Bureau of Statistics, Canberra, 2012.Google Scholar
10. Hammond, RA, Levine, R. The economic impact of obesity in the United States. Diabetes Metab Syndr Obes. 2010; 3, 285–295.CrossRefGoogle ScholarPubMed
11. Muller-Riemenschneider, F, Reinhold, T, Berghofer, A, Willich, SN. Health-economic burden of obesity in Europe. Eur J Epidemiol. 2008; 23, 499–509.Google Scholar
12. Colagiuri, S, Lee, CM, Colagiuri, R, et al. The cost of overweight and obesity in Australia. Med J Aust. 2010; 192, 260–264.Google Scholar
13. Millward, DJ. Energy balance and obesity: a UK perspective on the gluttony v. sloth debate. Nutr Res Rev. 2013; 26, 89–109.Google Scholar
14. Prentice, AM, Jebb, SA. Obesity in Britain: gluttony or sloth? BMJ. 1995; 311, 437–439.Google Scholar
15. Church, TS, Thomas, DM, Tudor-Locke, C, et al. Trends over 5 decades in U.S. occupation-related physical activity and their associations with obesity. PLoS One. 2011; 6, e19657.Google Scholar
16. Westerterp, KR, Speakman, JR. Physical activity energy expenditure has not declined since the 1980s and matches energy expenditures of wild mammals. Int J Obes (Lond). 2008; 32, 1256–1263.Google Scholar
17. Silventoinen, K, Sans, S, Tolonen, H, et al. Trends in obesity and energy supply in the WHO MONICA Project. Int J Obes Relat Metab Disord. 2004; 28, 710–718.Google Scholar
18. Guthrie, JF, Lin, BH, Frazao, E. Role of food prepared away from home in the American diet, 1977-78 versus 1994-96: changes and consequences. J Nutr Educ Behav. 2002; 34, 140–150.CrossRefGoogle ScholarPubMed
19. Nielsen, SJ, Siega-Riz, AM, Popkin, BM. Trends in energy intake in U.S. between 1977 and 1996: similar shifts seen across age groups. Obes Res. 2002; 10, 370–378.CrossRefGoogle ScholarPubMed
20. Nielsen, SJ, Popkin, BM. Changes in beverage intake between 1977 and 2001. Am J Prev Med. 2004; 27, 205–210.Google Scholar
21. Levine, AS, Kotz, CM, Gosnell, BA. Sugars and fats: the neurobiology of preference. J Nutr. 2003; 133, 831S–834S.Google Scholar
22. Johnson, PM, Kenny, PJ. Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci. 2010; 13, 635–641.Google Scholar
23. Glanz, K, Basil, M, Maibach, E, Goldberg, J, Snyder, D. Why Americans eat what they do: taste, nutrition, cost, convenience, and weight control concerns as influences on food consumption. J Am Diet Assoc. 1998; 98, 1118–1126.Google Scholar
24. Popkin, BM. Global nutrition dynamics: the world is shifting rapidly toward a diet linked with noncommunicable diseases. Am J Clin Nutr. 2006; 84, 289–298.Google Scholar
25. Cordain, L, Eaton, SB, Sebastian, A, et al. Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr. 2005; 81, 341–354.CrossRefGoogle Scholar
26. Atkinson, R. Etiologies of obesity. In The Management of Eating Disorders and Obesity (ed. Goldstein D), 2005; pp 105–118. Humana Press: New Jersey.Google Scholar
27. Oken, E. Maternal and child obesity: the causal link. Obstet Gynecol Clin North Am. 2009; 36, 361–377, iX–X.Google Scholar
28. Poston, L. Maternal obesity, gestational weight gain and diet as determinants of offspring long term health. Best Pract Res Clin Endocrinol Metab. 2012; 26, 627–639.Google Scholar
29. Fall, CH. Evidence for the intra-uterine programming of adiposity in later life. Ann Hum Biol. 2011; 38, 410–428.CrossRefGoogle ScholarPubMed
30. Guelinckx, I, Devlieger, R, Beckers, K, Vansant, G. Maternal obesity: pregnancy complications, gestational weight gain and nutrition. Obes Rev. 2008; 9, 140–150.CrossRefGoogle ScholarPubMed
31. Olson, CM, Strawderman, MS, Dennison, BA. Maternal weight gain during pregnancy and child weight at age 3 years. Matern Child Health J. 2009; 13, 839–846.Google Scholar
32. Crozier, SR, Inskip, HM, Godfrey, KM, et al. Weight gain in pregnancy and childhood body composition: findings from the Southampton Women's Survey. Am J Clin Nutr. 2010; 91, 1745–1751.Google Scholar
33. Reynolds, RM, Osmond, C, Phillips, DI, Godfrey, KM. Maternal BMI, parity, and pregnancy weight gain: influences on offspring adiposity in young adulthood. J Clin Endocrinol Metab. 2010; 95, 5365–5369.CrossRefGoogle ScholarPubMed
34. Wrotniak, BH, Shults, J, Butts, S, Stettler, N. Gestational weight gain and risk of overweight in the offspring at age 7 y in a multicenter, multiethnic cohort study. Am J Clin Nutr. 2008; 87, 1818–1824.CrossRefGoogle Scholar
35. Oken, E, Rifas-Shiman, SL, Field, AE, Frazier, AL, Gillman, MW. Maternal gestational weight gain and offspring weight in adolescence. Obstet Gynecol. 2008; 112, 999–1006.CrossRefGoogle ScholarPubMed
36. Hochner, H, Friedlander, Y, Calderon-Margalit, R, et al. Associations of maternal prepregnancy body mass index and gestational weight gain with adult offspring cardiometabolic risk factors: the Jerusalem Perinatal Family Follow-up Study. Circulation. 2012; 125, 1381–1389.CrossRefGoogle ScholarPubMed
37. Crume, TL, Ogden, LG, Mayer-Davis, EJ, et al. The impact of neonatal breast-feeding on growth trajectories of youth exposed and unexposed to diabetes in utero: the EPOCH Study. Int J Obes (Lond). 2012; 36, 529–534.Google Scholar
38. Arenz, S, Ruckerl, R, Koletzko, B, von Kries, R. Breast-feeding and childhood obesity – a systematic review. Int J Obes Relat Metab Disord. 2004; 28, 1247–1256.CrossRefGoogle ScholarPubMed
39. Tounian, P. Programming towards childhood obesity. Ann Nutr Metab. 2011; 58(Suppl. 2), 30–41.Google Scholar
40. Fields, DA, Demerath, EW. Relationship of insulin, glucose, leptin, IL-6 and TNF-alpha in human breast milk with infant growth and body composition. Pediatr Obes. 2012; 7, 304–312.CrossRefGoogle ScholarPubMed
41. Makela, J, Linderborg, K, Niinikoski, H, Yang, B, Lagstrom, H. Breast milk fatty acid composition differs between overweight and normal weight women: the STEPS Study. Eur J Nutr. 2013; 52, 727–735.CrossRefGoogle ScholarPubMed
42. Fahrenkrog, S, Harder, T, Stolaczyk, E, et al. Cross-fostering to diabetic rat dams affects early development of mediobasal hypothalamic nuclei regulating food intake, body weight, and metabolism. J Nutr. 2004; 134, 648–654.Google Scholar
43. Plagemann, A, Harder, T, Franke, K, Kohlhoff, R. Long-term impact of neonatal breast-feeding on body weight and glucose tolerance in children of diabetic mothers. Diabetes Care. 2002; 25, 16–22.Google Scholar
44. Bayol, SA, Farrington, SJ, Stickland, NC. A maternal ‘junk food’ diet in pregnancy and lactation promotes an exacerbated taste for ‘junk food’ and a greater propensity for obesity in rat offspring. Br J Nutr. 2007; 98, 843–851.CrossRefGoogle Scholar
45. Ong, ZY, Muhlhausler, BS. Maternal ‘junk-food’ feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring. FASEB J. 2011; 25, 2167–2179.CrossRefGoogle ScholarPubMed
46. Bayol, SA, Simbi, BH, Bertrand, JA, Stickland, NC. Offspring from mothers fed a ‘junk food’ diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females. J Physiol. 2008; 586, 3219–3230.Google Scholar
47. Bayol, SA, Simbi, BH, Fowkes, RC, Stickland, NC. A maternal ‘junk food’ diet in pregnancy and lactation promotes nonalcoholic fatty liver disease in rat offspring. Endocrinology. 2010; 151, 1451–1461.CrossRefGoogle ScholarPubMed
48. Samuelsson, AM, Matthews, PA, Argenton, M, 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. 2008; 51, 383–392.CrossRefGoogle ScholarPubMed
49. Howie, GJ, Sloboda, DM, Reynolds, CM, Vickers, MH. Timing of maternal exposure to a high fat diet and development of obesity and hyperinsulinemia in male rat offspring: same metabolic phenotype, different developmental pathways? J Nutr Metab. 2013; 2013, 517384.CrossRefGoogle ScholarPubMed
50. Cameron, AJ, Welborn, TA, Zimmet, PZ, et al. Overweight and obesity in Australia: the 1999–2000 Australian Diabetes, Obesity and Lifestyle Study (AusDiab). Med J Aust. 2003; 178, 427–432.Google Scholar
51. Laws, P, Hilder, L. Australia’s mothers and babies 2006. 2008. Unit ANPS: Sydney.Google Scholar
52. de Jersey, SJ, Nicholson, JM, Callaway, LK, Daniels, LA. A prospective study of pregnancy weight gain in Australian women. Aust N Z J Obstet Gynaecol. 2012; 52, 545–551.Google Scholar
53. Armitage, JA, Poston, L, Taylor, PD. Developmental origins of obesity and the metabolic syndrome: the role of maternal obesity. Front Horm Res. 2008; 36, 73–84.Google Scholar
54. Wolfe, RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr. 2006; 84, 475–482.Google Scholar
55. McCarthy, HD. Measuring growth and obesity across childhood and adolescence. Proc Nutr Soc. 2014; 73, 210–217.Google Scholar
56. Benson, AC, Torode, ME, Singh, MA. Muscular strength and cardiorespiratory fitness is associated with higher insulin sensitivity in children and adolescents. Int J Pediatr Obes. 2006; 1, 222–231.CrossRefGoogle ScholarPubMed
57. Dodson, S, Baracos, VE, Jatoi, A, et al. Muscle wasting in cancer cachexia: clinical implications, diagnosis, and emerging treatment strategies. Annu Rev Med. 2011; 62, 265–279.CrossRefGoogle ScholarPubMed
58. Leenders, M, Verdijk, LB, van der Hoeven, L, et al. Patients with type 2 diabetes show a greater decline in muscle mass, muscle strength, and functional capacity with aging. J Am Med Dir Assoc. 2013; 14, 585–592.Google Scholar
59. Kadar, L, Albertsson, M, Areberg, J, Landberg, T, Mattsson, S. The prognostic value of body protein in patients with lung cancer. Ann N Y Acad Sci. 2000; 904, 584–591.CrossRefGoogle ScholarPubMed
60. Artero, EG, Lee, DC, Lavie, CJ, et al. Effects of muscular strength on cardiovascular risk factors and prognosis. J Cardiopulm Rehabil Prev. 2012; 32, 351–358.CrossRefGoogle ScholarPubMed
61. Srikanthan, P, Karlamangla, AS. Muscle mass index as a predictor of longevity in older-adults. Am J Med. 2014; 127, 547–553.Google Scholar
62. Narici, MV, Maffulli, N. Sarcopenia: characteristics, mechanisms and functional significance. Br Med Bull. 2010; 95, 139–159.CrossRefGoogle ScholarPubMed
63. Hegarty, BD, Furler, SM, Ye, J, Cooney, GJ, Kraegen, EW. The role of intramuscular lipid in insulin resistance. Acta Physiol Scand. 2003; 178, 373–383.Google Scholar
64. Choi, KM. Sarcopenia and sarcopenic obesity. Endocrinol Metab (Seoul). 2013; 28, 86–89.CrossRefGoogle ScholarPubMed
65. Muller, MJ, Lagerpusch, M, Enderle, J, et al. Beyond the body mass index: tracking body composition in the pathogenesis of obesity and the metabolic syndrome. Obes Rev. 2012; 13(Suppl. 2), 6–13.Google Scholar
66. Zamboni, M, Mazzali, G, Fantin, F, Rossi, A, Di Francesco, V. Sarcopenic obesity: a new category of obesity in the elderly. Nutr Metab Cardiovasc Dis. 2008; 18, 388–395.Google Scholar
67. Bollheimer, LC, Buettner, R, Pongratz, G, et al. Sarcopenia in the aging high-fat fed rat: a pilot study for modeling sarcopenic obesity in rodents. Biogerontology. 2012; 13, 609–620.Google Scholar
68. Steene-Johannessen, J, Anderssen, SA, Kolle, E, Andersen, LB. Low muscle fitness is associated with metabolic risk in youth. Med Sci Sports Exerc. 2009; 41, 1361–1367.Google Scholar
69. Artero, EG, Ruiz, JR, Ortega, FB, et al. Muscular and cardiorespiratory fitness are independently associated with metabolic risk in adolescents: the HELENA study. Pediatr Diabetes. 2011; 12, 704–712.Google Scholar
70. Garcia-Artero, E, Ortega, FB, Ruiz, JR, et al. [Lipid and metabolic profiles in adolescents are affected more by physical fitness than physical activity (AVENA study)]. Rev Esp Cardiol. 2007; 60, 581–588.Google Scholar
71. Janz, KF, Dawson, JD, Mahoney, LT. Increases in physical fitness during childhood improve cardiovascular health during adolescence: the Muscatine Study. Int J Sports Med. 2002; 23(Suppl. 1), S15–S21.CrossRefGoogle ScholarPubMed
72. Farr, JN, Van Loan, MD, Lohman, TG, Going, SB. Lower physical activity is associated with skeletal muscle fat content in girls. Med Sci Sports Exerc. 2012; 44, 1375–1381.CrossRefGoogle ScholarPubMed
73. Fernandes, RA, Zanesco, A. Early physical activity promotes lower prevalence of chronic diseases in adulthood. Hypertens Res. 2010; 33, 926–931.Google Scholar
74. Ravussin, E, Lillioja, S, Anderson, TE, Christin, L, Bogardus, C. Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Invest. 1986; 78, 1568–1578.CrossRefGoogle ScholarPubMed
75. Zurlo, F, Larson, K, Bogardus, C, Ravussin, E. Skeletal muscle metabolism is a major determinant of resting energy expenditure. J Clin Invest. 1990; 86, 1423–1427.CrossRefGoogle Scholar
76. Guillet, C, Masgrau, A, Walrand, S, Boirie, Y. Impaired protein metabolism: interlinks between obesity, insulin resistance and inflammation. Obes Rev. 2012; 13(Suppl. 2), 51–57.Google Scholar
77. Forbes, GB, Welle, SL. Lean body mass in obesity. Int J Obes. 1983; 7, 99–107.Google Scholar
78. Lafortuna, CL, Maffiuletti, NA, Agosti, F, Sartorio, A. Gender variations of body composition, muscle strength and power output in morbid obesity. Int J Obes (Lond). 2005; 29, 833–841.Google Scholar
79. Auyeung, TW, Lee, JS, Leung, J, Kwok, T, Woo, J. Adiposity to muscle ratio predicts incident physical limitation in a cohort of 3,153 older adults – an alternative measurement of sarcopenia and sarcopenic obesity. Age (Dordr). 2013; 35, 1377–1385.Google Scholar
80. Hulens, M, Vansant, G, Lysens, R, et al. Study of differences in peripheral muscle strength of lean versus obese women: an allometric approach. Int J Obes Relat Metab Disord. 2001; 25, 676–681.Google Scholar
81. Goodpaster, BH, Thaete, FL, Kelley, DE. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr. 2000; 71, 885–892.CrossRefGoogle ScholarPubMed
82. Hilton, TN, Tuttle, LJ, Bohnert, KL, Mueller, MJ, Sinacore, DR. Excessive adipose tissue infiltration in skeletal muscle in individuals with obesity, diabetes mellitus, and peripheral neuropathy: association with performance and function. Phys Ther. 2008; 88, 1336–1344.Google Scholar
83. Lee, S, Kim, Y, White, DA, Kuk, JL, Arslanian, S. Relationships between insulin sensitivity, skeletal muscle mass and muscle quality in obese adolescent boys. Eur J Clin Nutr. 2012; 66, 1366–1368.Google Scholar
84. Stickland, NC, Batt, RA, Crook, AR, Sutton, CM. Inability of muscles in the obese mouse (ob/ob) to respond to changes in body weight and activity. J Anat. 1994; 184(Pt 3), 527–533.Google ScholarPubMed
85. Durschlag, RP, Layman, DK. Skeletal muscle growth in lean and obese Zucker rats. Growth. 1983; 47, 282–291.Google ScholarPubMed
86. Kemp, JG, Blazev, R, Stephenson, DG, Stephenson, GM. Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int J Obes (Lond). 2009; 33, 831–841.Google Scholar
87. Adechian, S, Giardina, S, Remond, D, et al. Excessive energy intake does not modify fed-state tissue protein synthesis rates in adult rats. Obesity (Silver Spring). 2009; 17, 1348–1355.Google Scholar
88. Suga, T, Kinugawa, S, Takada, S, et al. Combination of exercise training and diet restriction normalizes limited exercise capacity and impaired skeletal muscle function in diet-induced diabetic mice. Endocrinology. 2014; 155, 68–80.Google Scholar
89. Sishi, B, Loos, B, Ellis, B, et al. Diet-induced obesity alters signalling pathways and induces atrophy and apoptosis in skeletal muscle in a prediabetic rat model. Exp Physiol. 2011; 96, 179–193.CrossRefGoogle Scholar
90. Masgrau, A, Mishellany-Dutour, A, Murakami, H, et al. Time-course changes of muscle protein synthesis associated with obesity-induced lipotoxicity. J Physiol. 2012; 590(Pt 20), 5199–5210.Google Scholar
91. Tanner, CJ, Barakat, HA, Dohm, GL, et al. Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab. 2002; 282, E1191–E1196.Google Scholar
92. Hickey, MS, Carey, JO, Azevedo, JL, et al. Skeletal muscle fiber composition is related to adiposity and in vitro glucose transport rate in humans. Am J Physiol. 1995; 268(3 Pt 1), E453–E457.Google Scholar
93. Abou Mrad, J, Yakubu, F, Lin, D, et al. Skeletal muscle composition in dietary obesity-susceptible and dietary obesity-resistant rats. Am J Physiol. 1992; 262(4 Pt 2), R684–R688.Google Scholar
94. Helge, JW, Fraser, AM, Kriketos, AD, et al. Interrelationships between muscle fibre type, substrate oxidation and body fat. Int J Obes Relat Metab Disord. 1999; 23, 986–991.Google Scholar
95. Wade, AJ, Marbut, MM, Round, JM. Muscle fibre type and aetiology of obesity. Lancet. 1990; 335, 805–808.Google Scholar
96. Cherrington, AD. Banting lecture 1997. Control of glucose uptake and release by the liver in vivo . Diabetes. 1999; 48, 1198–1214.Google Scholar
97. Shrayyef, MZ, Gerich, JE. Normal glucose homeostasis. In Principles of Diabetes Mellitus (ed. Poretsky L), 2010; pp 19–35. Springer: New York, Dordrecht, Heidelberg, London.Google Scholar
98. Kelley, D, Mitrakou, A, Marsh, H, et al. Skeletal muscle glycolysis, oxidation, and storage of an oral glucose load. J Clin Invest. 1988; 81, 1563–1571.Google Scholar
99. Basu, A, Dalla Man, C, Basu, R, et al. Effects of type 2 diabetes on insulin secretion, insulin action, glucose effectiveness, and postprandial glucose metabolism. Diabetes Care. 2009; 32, 866–872.Google Scholar
100. Gerich, JE, Mitrakou, A, Kelley, D, et al. Contribution of impaired muscle glucose clearance to reduced postabsorptive systemic glucose clearance in NIDDM. Diabetes. 1990; 39, 211–216.Google Scholar
101. Carey, PE, Halliday, J, Snaar, JE, Morris, PG, Taylor, R. Direct assessment of muscle glycogen storage after mixed meals in normal and type 2 diabetic subjects. Am J Physiol Endocrinol Metab. 2003; 284, E688–E694.Google Scholar
102. Shaw, CS, Clark, J, Wagenmakers, AJ. The effect of exercise and nutrition on intramuscular fat metabolism and insulin sensitivity. Annu Rev Nutr. 2010; 30, 13–34.Google Scholar
103. Consitt, LA, Bell, JA, Houmard, JA. Intramuscular lipid metabolism, insulin action, and obesity. IUBMB Life. 2009; 61, 47–55.Google Scholar
104. Coen, PM, Goodpaster, BH. Role of intramyocelluar lipids in human health. Trends Endocrinol Metab. 2012; 23, 391–398.Google Scholar
105. Bismuth, K, Relaix, F. Genetic regulation of skeletal muscle development. Exp Cell Res. 2010; 316, 3081–3086.Google Scholar
106. Buckingham, M, Bajard, L, Chang, T, et al. The formation of skeletal muscle: from somite to limb. J Anat. 2003; 202, 59–68.CrossRefGoogle ScholarPubMed
107. Olsen, BR, Reginato, AM, Wang, W. Bone development. Annu Rev Cell Dev Biol. 2000; 16, 191–220.Google Scholar
108. Buckingham, M, Vincent, SD. Distinct and dynamic myogenic populations in the vertebrate embryo. Curr Opin Genet Dev. 2009; 19, 444–453.CrossRefGoogle ScholarPubMed
109. Aziz, A, Miyake, T, Engleka, KA, Epstein, JA, McDermott, JC. Menin expression modulates mesenchymal cell commitment to the myogenic and osteogenic lineages. Dev Biol. 2009; 332, 116–130.CrossRefGoogle Scholar
110. Seale, P, Bjork, B, Yang, W, et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature. 2008; 454, 961–967.Google Scholar
111. Berard, J, Kalbe, C, Losel, D, Tuchscherer, A, Rehfeldt, C. Potential sources of early-postnatal increase in myofibre number in pig skeletal muscle. Histochem Cell Biol. 2011; 136 217–225.CrossRefGoogle ScholarPubMed
112. Standring, S, Borley, N, Collins, P, et al. Functional anatomy of the musculoskeletal system. In Gray’s Anatomy. (eds. Standring, Susan and Elsevier Limited), 2008; pp. 81–126. Churchill Livingstone: Edinburgh, UK.Google Scholar
113. Wigmore, PM, Dunglison, GF. The generation of fiber diversity during myogenesis. Int J Dev Biol. 1998; 42, 117–125.Google Scholar
114. Barbet, JP, Thornell, LE, Butler-Browne, GS. Immunocytochemical characterisation of two generations of fibers during the development of the human quadriceps muscle. Mech Dev. 1991; 35, 3–11.Google Scholar
115. Ross, JJ, Duxson, MJ, Harris, AJ. Formation of primary and secondary myotubes in rat lumbrical muscles. Development. 1987; 100, 383–394.Google Scholar
116. Ontell, M, Bourke, D, Hughes, D. Cytoarchitecture of the fetal murine soleus muscle. Am J Anat. 1988; 181, 267–278.Google Scholar
117. Duxson, MJ, Usson, Y, Harris, AJ. The origin of secondary myotubes in mammalian skeletal muscles: ultrastructural studies. Development. 1989; 107, 743–750.Google Scholar
118. White, RB, Bierinx, AS, Gnocchi, VF, Zammit, PS. Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev Biol. 2010; 10, 21.CrossRefGoogle ScholarPubMed
119. Stickland, NC. Muscle development in the human fetus as exemplified by m. sartorius: a quantitative study. J Anat. 1981; 132(Pt 4), 557–579.Google Scholar
120. Schiaffino, S, Dyar, KA, Ciciliot, S, Blaauw, B, Sandri, M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. 2013; 280, 4294–4314.Google Scholar
121. Partridge, T. Developmental biology: Skeletal muscle comes of age. Nature. 2009; 460, 584–585.Google Scholar
122. Brack, AS, Rando, TA. Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell. 2012; 10, 504–514.Google Scholar
123. McCarthy, JJ, Mula, J, Miyazaki, M, et al. Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development. 2011; 138, 3657–3666.Google Scholar
124. Partridge, TA. The mdx mouse model as a surrogate for Duchenne muscular dystrophy. FEBS J. 2013; 280, 4177–4186.Google Scholar
125. Mavalli, MD, DiGirolamo, DJ, Fan, Y, et al. Distinct growth hormone receptor signaling modes regulate skeletal muscle development and insulin sensitivity in mice. J Clin Invest. 2010; 120, 4007–4020.Google Scholar
126. Matsakas, A, Otto, A, Elashry, MI, Brown, SC, Patel, K. Altered primary and secondary myogenesis in the myostatin-null mouse. Rejuvenation Res. 2010; 13, 717–727.Google Scholar
127. Judson, RN, Zhang, RH, Rossi, FM. Tissue-resident mesenchymal stem/progenitor cells in skeletal muscle: collaborators or saboteurs? FEBS J. 2013; 280, 4100–4108.Google Scholar
128. Uezumi, A, Ikemoto-Uezumi, M, Tsuchida, K. Roles of nonmyogenic mesenchymal progenitors in pathogenesis and regeneration of skeletal muscle. Front Physiol. 2014; 5, 68.Google Scholar
129. Sayer, AA, Syddall, H, Martin, H, et al. The developmental origins of sarcopenia. J Nutr Health Aging. 2008; 12, 427–432.Google Scholar
130. Brown, L. Endocrine regulation of fetal skeletal muscle growth: impact on future metabolic health. J Endocrinol. 2014; 221, R13–R29.CrossRefGoogle ScholarPubMed
131. Bedi, KS, Birzgalis, AR, Mahon, M, Smart, JL, Wareham, AC. Early life undernutrition in rats. 1. Quantitative histology of skeletal muscles from underfed young and refed adult animals. Br J Nutr. 1982; 47, 417–431.Google Scholar
132. Wilson, SJ, Ross, JJ, Harris, AJ. A critical period for formation of secondary myotubes defined by prenatal undernourishment in rats. Development. 1988; 102, 815–821.Google Scholar
133. 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, 1285–1292.Google Scholar
134. Dwyer, CM, Stickland, NC, Fletcher, JM. The influence of maternal nutrition on muscle fiber number development in the porcine fetus and on subsequent postnatal growth. J Anim Sci. 1994; 72, 911–917.CrossRefGoogle ScholarPubMed
135. Montgomery, RD. Muscle morphology in infantile protein malnutrition. J Clin Pathol. 1962; 15, 511–521.Google Scholar
136. Dwyer, CM, Fletcher, JM, Stickland, NC. Muscle cellularity and postnatal growth in the pig. J Anim Sci. 1993; 71, 3339–3343.Google Scholar
137. Stickland, NC, Handel, SE. The numbers and types of muscle fibres in large and small breeds of pigs. J Anat. 1986; 147, 181–189.Google Scholar
138. Paredes, SP, Kalbe, C, Jansman, AJ, et al. Predicted high-performing piglets exhibit more and larger skeletal muscle fibers. J Anim Sci. 2013; 91, 5589–5598.Google Scholar
139. Mallinson, JE, Sculley, DV, Craigon, J, et al. Fetal exposure to a maternal low-protein diet during mid-gestation results in muscle-specific effects on fibre type composition in young rats. Br J Nutr. 2007; 98, 292–299.Google Scholar
140. Costello, PM, Rowlerson, A, Astaman, NA, et al. Peri-implantation and late gestation maternal undernutrition differentially affect fetal sheep skeletal muscle development. J Physiol. 2008; 586, 2371–2379.Google Scholar
141. Huber, K, Miles, JL, Norman, AM, et al. Prenatally induced changes in muscle structure and metabolic function facilitate exercise-induced obesity prevention. Endocrinology. 2009; 150, 4135–4144.Google Scholar
142. Muhlhausler, BS, Duffield, JA, Ozanne, SE, et al. The transition from fetal growth restriction to accelerated postnatal growth: a potential role for insulin signalling in skeletal muscle. J Physiol. 2009; 587(Pt 17), 4199–4211.Google Scholar
143. Bayol, SA, Macharia, R, Farrington, SJ, Simbi, BH, Stickland, NC. Evidence that a maternal ‘junk food’ diet during pregnancy and lactation can reduce muscle force in offspring. Eur J Nutr. 2009; 48, 62–65.Google Scholar
144. Samuelsson, AM, Matthews, PA, Jansen, E, Taylor, PD, Poston, L. Sucrose feeding in mouse pregnancy leads to hypertension, and sex-linked obesity and insulin resistance in female offspring. Front Physiol. 2013; 4, 14.Google Scholar
145. Tong, JF, Yan, X, Zhu, MJ, et al. Maternal obesity downregulates myogenesis and beta-catenin signaling in fetal skeletal muscle. Am J Physiol Endocrinol Metab. 2009; 296, E917–E924.Google Scholar
146. Yan, X, Huang, Y, Zhao, JX, et al. Maternal obesity-impaired insulin signaling in sheep and induced lipid accumulation and fibrosis in skeletal muscle of offspring. Biol Reprod. 2011; 85, 172–178.Google Scholar
147. Huang, Y, Zhao, JX, Yan, X, et al. Maternal obesity enhances collagen accumulation and cross-linking in skeletal muscle of ovine offspring. PLoS One. 2012; 7, e31691.CrossRefGoogle ScholarPubMed
148. Purslow, PP. Muscle fascia and force transmission. J Bodyw Mov Ther. 2010; 14, 411–417.Google Scholar
149. Brack, AS, Conboy, MJ, Roy, S, et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science. 2007; 317, 807–810.Google Scholar
150. Bailey, AJ, Paul, RG, Knott, L. Mechanisms of maturation and ageing of collagen. Mech Ageing Dev. 1998; 106, 1–56.Google Scholar
151. Lahoute, C, Sotiropoulos, A, Favier, M, et al. Premature aging in skeletal muscle lacking serum response factor. PLoS One. 2008; 3, e3910.CrossRefGoogle ScholarPubMed
152. Beggs, ML, Nagarajan, R, Taylor-Jones, JM, et al. Alterations in the TGFbeta signaling pathway in myogenic progenitors with age. Aging Cell. 2004; 3, 353–361.Google Scholar
153. Goldspink, G, Fernandes, K, Williams, PE, Wells, DJ. Age-related changes in collagen gene expression in the muscles of mdx dystrophic and normal mice. Neuromuscul Disord. 1994; 4, 183–191.Google Scholar
154. Du, M, Yan, X, Tong, JF, Zhao, J, Zhu, MJ. Maternal obesity, inflammation, and fetal skeletal muscle development. Biol Reprod. 2010; 82, 4–12.Google Scholar
155. 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(Pt 3), 951–961.CrossRefGoogle ScholarPubMed
156. Uezumi, A, Fukada, S, Yamamoto, N, Takeda, S, Tsuchida, K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol. 2010; 12, 143–152.Google Scholar
157. Aguiari, P, Leo, S, Zavan, B, et al. High glucose induces adipogenic differentiation of muscle-derived stem cells. Proc Natl Acad Sci U S A. 2008; 105, 1226–1231.Google Scholar
158. Tamilarasan, KP, Temmel, H, Das, SK, et al. Skeletal muscle damage and impaired regeneration due to LPL-mediated lipotoxicity. Cell Death Dis. 2012; 3, e354.Google Scholar
159. Mebarek, S, Komati, H, Naro, F, et al. Inhibition of de novo ceramide synthesis upregulates phospholipase D and enhances myogenic differentiation. J Cell Sci. 2007; 120(Pt 3), 407–416.Google Scholar
160. Turpin, SM, Lancaster, GI, Darby, I, Febbraio, MA, Watt, MJ. Apoptosis in skeletal muscle myotubes is induced by ceramides and is positively related to insulin resistance. Am J Physiol Endocrinol Metab. 2006; 291, E1341–E1350.Google Scholar
161. Henique, C, Mansouri, A, Fumey, G, et al. Increased mitochondrial fatty acid oxidation is sufficient to protect skeletal muscle cells from palmitate-induced apoptosis. J Biol Chem. 2010; 285, 36818–36827.Google Scholar
162. Akhmedov, D, Berdeaux, R. The effects of obesity on skeletal muscle regeneration. Front Physiol. 2013; 4, 371.Google Scholar
163. Charge, SB, Rudnicki, MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004; 84, 209–238.Google Scholar
164. Hu, Z, Wang, H, Lee, IH, et al. PTEN inhibition improves muscle regeneration in mice fed a high-fat diet. Diabetes. 2010; 59, 1312–1320.Google Scholar
165. Woo, M, Isganaitis, E, Cerletti, M, et al. Early life nutrition modulates muscle stem cell number: implications for muscle mass and repair. Stem Cells Dev. 2011; 20, 1763–1769.Google Scholar
166. Park, KW, Halperin, DS, Tontonoz, P. Before they were fat: adipocyte progenitors. Cell Metab. 2008; 8, 454–457.Google Scholar
167. Latouche, C, Heywood, SE, Henry, SL, et al. Maternal overnutrition program changes in skeletal muscle gene expression associated with insulin resistance and reduction in oxidative phosphorylation enzymes in adult male rat offspring. J Nutr. 2013; 144, 237–244.Google Scholar
168. Simar, D, Chen, H, Lambert, K, Mercier, J, Morris, MJ. Interaction between maternal obesity and post-natal over-nutrition on skeletal muscle metabolism. Nutr Metab Cardiovasc Dis. 2012; 22, 269–276.Google Scholar
169. Gatford, KL, Kaur, G, Falcao-Tebas, F, et al. Exercise as an intervention to improve metabolic outcomes after intrauterine growth restriction. Am J Physiol Endocrinol Metab. 2014; 306, E999–E1012.Google Scholar
170. Caruso, V, Bahari, H, Morris, MJ. The beneficial effects of early short-term exercise in the offspring of obese mothers are accompanied by alterations in the hypothalamic gene expression of appetite regulators and FTO (fat mass and obesity associated) gene. J Neuroendocrinol. 2013; 25, 742–752.Google Scholar
171. Bahari, H, Caruso, V, Morris, MJ. Late-onset exercise in female rat offspring ameliorates the detrimental metabolic impact of maternal obesity. Endocrinology. 2013; 154, 3610–3621.Google Scholar
172. Nathanielsz, PW, Ford, SP, Long, NM, et al. Interventions to prevent adverse fetal programming due to maternal obesity during pregnancy. Nutr Rev. 2013; 71(Suppl. 1), S78–S87.CrossRefGoogle ScholarPubMed
173. Tong, JF, Yan, X, Zhao, JX, et al. Metformin mitigates the impaired development of skeletal muscle in the offspring of obese mice. Nutr Diabetes. 2011; 1, e7.Google Scholar
174. McCarthy, HD, Samani-Radia, D, Jebb, SA, Prentice, AM. Skeletal muscle mass reference curves for children and adolescents. Pediatr Obes. 2013; 9, 249–259.Google Scholar
175. Gale, CR, Javaid, MK, Robinson, SM, et al. Maternal size in pregnancy and body composition in children. J Clin Endocrinol Metab. 2007; 92, 3904–3911.Google Scholar
176. Hull, HR, Dinger, MK, Knehans, AW, Thompson, DM, Fields, DA. Impact of maternal body mass index on neonate birthweight and body composition. Am J Obstet Gynecol. 2008; 198, e411–e416.Google Scholar
177. Ruager-Martin, R, Thomas, EL, Uthaya, S, Bell, JD, Modi, N. Effect of maternal obesity on newborn body composition. Neonat Soc Abstr. 2009; Available at http://www.neonatalsociety.ac.uk/abstracts/ruagermartinr_2009_maternalobesitynewbornbody.shtml Google Scholar
178. Sewell, MF, Huston-Presley, L, Super, DM, Catalano, P. Increased neonatal fat mass, not lean body mass, is associated with maternal obesity. Am J Obstet Gynecol. 2006; 195, 1100–1103.Google Scholar
179. Ode, KL, Gray, HL, Ramel, SE, Georgieff, MK, Demerath, EW. Decelerated early growth in infants of overweight and obese mothers. J Pediatr. 2012; 161, 1028–1034.Google Scholar
180. van den Ham, EC, Kooman, JP, Christiaans, MH, et al. Body composition in renal transplant patients: bioimpedance analysis compared to isotope dilution, dual energy X-ray absorptiometry, and anthropometry. J Am Soc Nephrol. 1999; 10, 1067–1079.Google Scholar
181. Provyn, S, Clarys, JP, Wallace, J, Scafoglieri, A, Reilly, T. Quality control, accuracy, and prediction capacity of dual energy X-ray absorptiometry variables and data acquisition. J Physiol Anthropol. 2008; 27, 317–323.Google Scholar
182. Rutten, EP, Spruit, MA, Wouters, EF. Critical view on diagnosing muscle wasting by single-frequency bio-electrical impedance in COPD. Respir Med. 2010; 104, 91–98.Google Scholar