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Stage of perinatal development regulates skeletal muscle mitochondrial biogenesis and myogenic regulatory factor genes with little impact of growth restriction or cross-fostering

Published online by Cambridge University Press:  10 November 2011

R. C. Laker
Affiliation:
Department of Physiology, The University of Melbourne, Parkville, Victoria, Australia
G. D. Wadley
Affiliation:
Department of Physiology, The University of Melbourne, Parkville, Victoria, Australia Centre for Physical Activity and Nutrition Research, School of Exercise and Nutrition Sciences, Deakin University, Burwood, Victoria, Australia
G. K. McConell
Affiliation:
Department of Physiology, The University of Melbourne, Parkville, Victoria, Australia Institute of Sport, Exercise and Active Living and the School of Biomedical and Health Sciences, Victoria University, Victoria, Australia
M. E. Wlodek*
Affiliation:
Department of Physiology, The University of Melbourne, Parkville, Victoria, Australia
*
*Author for correspondence: Prof M. E. Wlodek, Department of Physiology, The University of Melbourne, Parkville, Victoria 3010, Australia. (Email m.wlodek@unimelb.edu.au)

Abstract

Foetal growth restriction impairs skeletal muscle development and adult muscle mitochondrial biogenesis. We hypothesized that key genes involved in muscle development and mitochondrial biogenesis would be altered following uteroplacental insufficiency in rat pups, and improving postnatal nutrition by cross-fostering would ameliorate these deficits. Bilateral uterine vessel ligation (Restricted) or sham (Control) surgery was performed on day 18 of gestation. Males and females were investigated at day 20 of gestation (E20), 1 (PN1), 7 (PN7) and 35 (PN35) days postnatally. A separate cohort of Control and Restricted pups were cross-fostered onto a different Control or Restricted mother and examined at PN7. In both sexes, peroxisome proliferator-activated receptor (PPAR)-γ coactivator-1α (PGC-1α), cytochrome c oxidase subunits 3 and 4 (COX III and IV) and myogenic regulatory factor 4 expression increased from late gestation to postnatal life, whereas mitochondrial transcription factor A, myogenic differentiation 1 (MyoD), myogenin and insulin-like growth factor I (IGF-I) decreased. Foetal growth restriction increased MyoD mRNA in females at PN7, whereas in males IGF-I mRNA was higher at E20 and PN1. Cross-fostering Restricted pups onto a Control mother significantly increased COX III mRNA in males and COX IV mRNA in both sexes above controls with little effect on other genes. Developmental age appears to be a major factor regulating skeletal muscle mitochondrial and developmental genes, with growth restriction and cross-fostering having only subtle effects. It therefore appears that reductions in adult mitochondrial biogenesis markers likely develop after weaning.

Type
Original Articles
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2011

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References

1. Barker, DJ, Winter, PD, Osmond, C, Margetts, B, Simmonds, SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 2, 577580.CrossRefGoogle ScholarPubMed
2. Barker, DJP, Osmond, C, Golding, J, Kuh, D, Wadsworth, MEJ. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989; 298, 564567.Google Scholar
3. Barker, DJ, Hales, CN, Fall, CH, et al. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia. 1993; 36, 6267.CrossRefGoogle ScholarPubMed
4. Hales, CN, Barker, DJ, Clark, PM, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991; 303, 10191022.Google Scholar
5. Kelley, DE, He, J, Menshikova, EV, Ritov, VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes. 2002; 51, 29442950.Google Scholar
6. Morino, K, Petersen, KF, Dufour, S, et al. Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest. 2005; 115, 35873593.CrossRefGoogle ScholarPubMed
7. Patti, ME. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. PNAS. 2003; 100, 84668471.CrossRefGoogle ScholarPubMed
8. Wadley, GD, Siebel, AL, Cooney, GJ, et al. Uteroplacental insufficiency and reducing litter size alters skeletal muscle mitochondrial biogenesis in a sex specific manner in the adult rat. Am J Physiol. 2008; 294, E861E869.Google Scholar
9. Selak, MA, Storey, BT, Peterside, I, Simmons, RA. Impaired oxidative phosphorylation in skeletal muscle of intrauterine growth-retarded rats. Am J Physiol. 2003; 285, E130E137.Google ScholarPubMed
10. Lane, RH, Maclennan, NK, Daood, MJ, et al. IUGR alters postnatal rat skeletal muscle peroxisome proliferator-activated receptor-g coactivator-1 gene expression in a fiber specific manner. Pediatr Res. 2003; 53, 9941000.Google Scholar
11. Lane, RH, Chandorkar, AK, Flozak, AS, Simmons, RA. Intrauterine growth retardation alters mitochondrial gene expression and function in fetal and juvenile rat skeletal muscle. Pediatr Res. 1998; 43, 563570.CrossRefGoogle ScholarPubMed
12. Hediger, ML, Overpeck, MD, Kuczmarski, RJ, et al. Muscularity and fatness of infants and young children born small- or large-for-gestational age. Pediatrics. 1998; 102, E60E67.CrossRefGoogle ScholarPubMed
13. Kahn, HS, Narayan, KM, Williamson, DF, Valdez, R. Relation of birth weight to lean and fat thigh tissue in young men. Obes Relat Metab Disord. 2000; 24, 667672.Google Scholar
14. Phillips, DIW. Relation of fetal growth to adult muscle mass and glucose tolerance. Diabet Med. 1995; 12, 686690.Google Scholar
15. Sayer, AA, Syddall, HE, Dennison, EM, et al. Birth weight, weight at 1 y of age, and body composition in older men: findings from the Hertfordshire Cohort Study. Am J Clin Nutr. 2004; 80, 199203.CrossRefGoogle ScholarPubMed
16. Sayer, AA, Syddall, HE, Dennison, EM, et al. Grip strength and the metabolic syndrome: findings from the Hertfordshire Cohort Study. Q J Med. 2007; 100, 707713.Google Scholar
17. Kuh, D, Bassey, J, Hardy, R, et al. Birth weight, childhood size, and muscle strength in adult life: evidence from a birth cohort study. Am J Epidemiol. 2002; 156, 627633.Google Scholar
18. Yliharsila, H, Kajantie, E, Osmond, C, et al. Birth size, adult body composition and muscle strength in later life. Int J Obes. 2007; 31, 13921399.CrossRefGoogle ScholarPubMed
19. Jensen, CB, Storgaard, H, Madsbad, S, Richter, EA, Vaag, AA. Altered skeletal muscle fiber composition and size precede whole-body insulin resistance in young men with low birth weight. J Clin Endocrinol Metab. 2007; 92, 15301534.CrossRefGoogle ScholarPubMed
20. Ward, SS, Stickland, NC. Why are slow and fast muscles differentially affected during prenatal undernutrition? Muscle Nerve. 1991; 14, 259267.Google Scholar
21. 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, 12851292.CrossRefGoogle ScholarPubMed
22. Wilson, SJ, Ross, JJ, Harris, AJ. A critical period for formation of secondary myotubes defined by prenatal undernourishment in rats. Development. 1988; 102, 815821.Google Scholar
23. Alves, PA, Damasco, AR, Pai, VD. The effects of prenatal and postnatal malnutrition on the morphology, differentiation, and metabolism of skeletal striated muscle tissue in rats. J de Pediatr. 2008; 84, 264271.Google Scholar
24. 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, 23712379.CrossRefGoogle ScholarPubMed
25. Prakash, YS, Fournier, M, Sieck, GC. Effects of prenatal undernutrition on developing rat diaphragm. J Appl Physiol. 1993; 75, 10441052.CrossRefGoogle ScholarPubMed
26. Harris, AJ, Duxson, MJ, Fitzsimons, RB, Rieger, F. Myonuclear bithdates distinguish the origins of primary and secondary myotubes in embryonic mammalian skeletal muscles. Development. 1989; 107, 771784.Google Scholar
27. Thompson, WJ, Condon, K, Astrow, SH. The origin and selective innvervation of early muscle fiber types in the rat. J Neurobiol. 1990; 21, 212222.Google Scholar
28. Zhang, M, McLennan, IS. During secondary myotube formation, primary myotubes preferentially absorb new nuclei at their ends. Dev Dyn. 1995; 204, 168177.CrossRefGoogle ScholarPubMed
29. Braun, T, Arnold, HH. Inactivation of Myf-6 and Myf-5 genes in mice leads to alterations in skeletal muscle development. EMBO J. 1995; 14, 11761186.Google Scholar
30. Gerhart, J, Elder, J, Neely, C, et al. MyoD-positive epiblast cells regulate skeletal muscle differentiation in the embryo. J Cell Biol. 2006; 175, 283292.Google Scholar
31. Hasty, P, Bradley, A, Morris, JH, et al. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature. 1993; 364, 501506.Google Scholar
32. Kassar-Duchossoy, LK, Gayraud-Morel, B, Gomes, D, et al. Mrf4 determines skeletal muscle identity in Myf5: Myod double-mutant mice. Nature. 2004; 431, 466471.CrossRefGoogle ScholarPubMed
33. Cossu, G, Kelly, R, Tajbakhsh, S, et al. Activation of different myogenic pathways: Myf-5 is induced by the neural tube and MyoD by the dorsal ectoderm in mouse paraxial mesoderm. Development. 1996; 122, 429437.Google Scholar
34. Tajbakhsh, S, Rocancourt, D, Cossu, G, Buckingham, M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell. 1997; 89, 127138.Google Scholar
35. Rawls, A, Morris, JH, Rudnicki, M, et al. Myogenin's functions do not overlap with those of MyoD or Myf-5 during mouse embryogenesis. Dev Biol. 1995; 172, 3750.Google Scholar
36. Baker, J, Liu, JP, Robertson, EJ, Efstratiadis, A. Role of insulin-like growth factors in embryonic and postnatal growth. Cell. 1993; 75, 7382.CrossRefGoogle ScholarPubMed
37. Liu, JP, Baker, J, Perkins, AS, Robertson, EJ, Efstratiadis, A. Mice carrying null mutations of the genes encoding insulin-like growth factor 1 (Igf-1) and type 1 IGF receptor (Igf1r). Cell. 1993; 75, 5972.Google ScholarPubMed
38. Powell-Braxton, L, Hollingshead, P, Warburton, C, et al. IGF-1 is required for normal embryonic growth in mice. Genes Dev. 1993; 12B, 26092617.Google Scholar
39. Coolican, SA, Samuel, DS, Ewton, DZ, McWade, FJ, Florini, JR. The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signalling pathways. J Biol Chem. 1997; 272, 66536662.CrossRefGoogle Scholar
40. Wlodek, ME, Lorenc, U, O'Dowd, R, et al. Uteroplacental insufficiency impairs mammary function, milk intake and postnatal growth. Pediatr Res. 2003; 53, 36A.Google Scholar
41. O'Dowd, R, Kent, JC, Moseley, JM, Wlodek, ME. Effects of uteroplacental insufficiency and reducing litter size on maternal mammary function and postnatal offspring growth. Am J Physiol. 2008; 294, R539R548.Google ScholarPubMed
42. Eriksson, JG. Early growth, and coronary heart disease and type 2 diabetes: experiences from the Helsinki birth cohort studies. Int J Obes. 2006; 30 (Suppl. 4), S18S22.Google Scholar
43. Eriksson, JG, Osmond, C, Kajantie, E, Forsén, TJ, Barker, DJP. Patterns of growth among children who later develop type 2 diabetes or its risk factors. Diabetologia. 2006; 49, 28532858.CrossRefGoogle ScholarPubMed
44. Forsén, T, Eriksson, J, Tuomilehto, J, et al. The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med. 2000; 133, 176182.Google Scholar
45. Siebel, AL, Mibus, A, De Blasio, MJ, et al. Improved lactational nutrition and postnatal growth ameliorates impairment of glucose tolerance by uteroplacental insufficiency in male rat offspring. Endocrinology. 2008; 149, 30673076.Google Scholar
46. Siebel, AL, Gallo, LA, Guan, TC, Owens, JA, Wlodek, ME. Cross-fostering and improved lactation ameliorates deficits in endocrine pancreatic morphology in growth restricted adult male rat offspring. J Dev Origin Health Dis. 2010; 1, 234244.Google Scholar
47. Owens, JA, Thavaneswaran, P, De Blasio, MJ, et al. Sex-specific effects of placental restriction on components of the metabolic syndrome in young adult sheep. Am J Physiol. 2007; 292, E1879E1889.Google Scholar
48. Gatford, KL, Mohammad, SNB, Harland, ML, et al. Impaired B-Cell function and inadequate compensatory increases in B-cell mass following intrauterine growth restriction in sheep. Endocrinology. 2008; 149, 51185127.CrossRefGoogle Scholar
49. Owens, JA, Gatford, KL, De Blasio, MJ, et al. Restriction of placental growth in sheep impairs insulin secretion but not sensitivity before birth. J Physiol. 2007; 584(Pt 3), 935949.CrossRefGoogle Scholar
50. Wlodek, ME, Westcott, KT, O'Dowd, R, et al. Uteroplacental restriction in the rat impairs fetal growth in association with alterations in placental growth factors including PTHrP. Am J Physiol. 2005; 288, R1620R1627.Google ScholarPubMed
51. Wlodek, ME, Mibus, A, Tan, A, et al. Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat. J Am Soc Nephrol. 2007; 18, 16881696.CrossRefGoogle ScholarPubMed
52. Vodstrcil, LA, Wlodek, ME, Parry, LJ. Effects of uteroplacental restriction on the relaxin-family receptors, Lgr7 and Lgr8, in the uterus of late pregnant rats. Reprod Fertil Dev. 2007; 19, 530538.CrossRefGoogle ScholarPubMed
53. Colling-Saltin, A-S. Some quantitative biochemical evaluations of developing skeletal muscles in the human foetus. J Neurol Sci. 1978; 39, 187198.CrossRefGoogle ScholarPubMed
54. Novak, E, Drummond, GI, Skala, J, Hahn, P. Developmental changes in cyclic AMP, protein kinase, phosphorylase kinase, and phosphorylase in liver, heart, and skeletal muscle of the rat. Arch Biochem Biophys. 1972; 150, 511518.CrossRefGoogle ScholarPubMed
55. Glatz, JFC, Veerkamp, JH. Postnatal development of palmitate oxidation and mitochondrial enzyme activities in rat cardiac and skeletal muscle. Biochimica et Biophysica Acta. 1982; 711, 327335.CrossRefGoogle ScholarPubMed
56. Kang, D, Kim, SH, Hamasaki, N. Mitochondrial transcription factor A (TFAM): roles in maintenance of MtDNA and cellular functions. Mitochondrion. 2007; 7, 3944.Google Scholar
57. Nabeshima, Y, Hanaoka, K, Hayasaka, M, et al. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature. 1993; 365, 532535.Google Scholar
58. Rudnicki, MA, Braun, T, Hinuma, S, Jaenisch, R. Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell. 1992; 71, 383390.Google Scholar
59. Rudnicki, MA, Schnegelsberg, PN, Stead, RH, et al. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell. 1993; 75, 13511359.CrossRefGoogle ScholarPubMed
60. O'Hagan, KA, Cocchiglia, S, Zhdanov, AV, et al. PGC-1alpha is coupled to HIF-1alpha-dependent gene expression by increasing mitochondrial oxygen consumption in skeletal muscle cells. Proc Natl Acad Sci USA. 2009; 106, 21882193.CrossRefGoogle ScholarPubMed
61. Brameld, JM, Mostyn, A, Dandrea, J, et al. Maternal nutrition alters the expression of insulin-like growth factors in fetal sheep liver and skeletal muscle. J Endocrinol. 2000; 167, 429437.CrossRefGoogle ScholarPubMed
62. Kind, KL, Owens, JA, Robinson, JS, et al. Effect of restriction of placental growth on expression of IGFs in fetal sheep: relationship to fetal growth, circulating IGFs and binding proteins. J Endocrinol. 1995; 146, 2334.Google Scholar
63. O'Dowd, R, Siebel, AL, Wlodek, ME. Cross-fostering a pup born small onto a mother with normal lactation improves postnatal growth by altering alveolar area, milk production and milk protein gene expression. J Soc Gynecol Invest. 2006; 13, 185A.Google Scholar
64. Siebel, AL, Westcott, KT, Mibus, AL, et al. Growth-restricted male offspring show marked hyperglycaemia in response to a glucose load, which can be improved by restoring lactational nutrition. J Paediatr Child Health. 2007; 43, A74.Google Scholar