Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-19T10:31:18.074Z Has data issue: false hasContentIssue false
  • English
  • Français

The influence of undernutrition during gestation on skeletal muscle cellularity and on the expression of genes that control muscle growth

Published online by Cambridge University Press:  09 March 2007

Stéphanie Bayol ,
Doiran Jones ,
Geoffrey Goldspink  and
Neil C. Stickland
Stéphanie Bayol*
Affiliation:
The Royal Veterinary College, Royal College Street, London NW1 0TU, UK
Doiran Jones
Affiliation:
Royal Free & University College Medical School, Rowland Hill Street, London NW3 2PF, UK
Geoffrey Goldspink
Affiliation:
Royal Free & University College Medical School, Rowland Hill Street, London NW3 2PF, UK
Neil C. Stickland
Affiliation:
The Royal Veterinary College, Royal College Street, London NW1 0TU, UK
*
*Corresponding author: Dr Stéphanie Bayol, fax +44 20 7388 1027, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

We examined the effects of two levels of gestational undernutrition (50% and 40% of ad libitum) on postnatal growth rate, skeletal muscle cellularity and the expression of genes that control muscle growth, in the offspring at weaning. The results showed that the rat pups born to mothers fed the 50% diet during gestation and a control diet during lactation had an increased postnatal growth rate compared with the pups fed the more restricted diet (40% of ad libitum). Surprisingly, the growth rate of the control group (ad libitum) was intermediate between the 50% and 40% groups. The restricted diets did not alter the number of muscle fibres in the semitendinosus muscle of the offspring but the number of muscle nuclei was reduced by 16% in the 40% group compared with the control group. In the 50% group, the lightest pups at birth (L) had elevated muscle insulin-like growth factor (IGF)-1, IGF binding protein (BP)-5 and proliferating cell nuclear antigen (PCNA) mRNA compared with the L pups from both the control and 40% groups. The heaviest pups at birth (H) in the 50% group had increased levels of IGFBP-4, PCNA and M-cadherin mRNA compared with both the control and 40% groups. Levels of IGF-1 receptor, myostatin and MyoD mRNA did not correlate with postnatal growth. Both H and L pups from the 40% group had reduced muscle IGF-1 mRNA but all other transcripts examined were similar to control levels. The results suggest that the increased postnatal growth rate, which accompanied milder fetal undernutrition (50%), may be due to a more active local muscle IGF system and increased muscle-cell proliferation.

Keywords

GestationUndernutritionSkeletal muscleSatellite cellsInsulin-like growth factor
Type
Research Article
Information
British Journal of Nutrition , Volume 91 , Issue 3 , March 2004 , pp. 331 - 339
Copyright
Copyright © The Nutrition Society 2004

References

Allen, RE, Sheehan, SM, Taylor, RG, Kendall, TL & Rice, GM (1995) Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 165, 307–312.CrossRefGoogle ScholarPubMed
Barker, DJ, Gluckman, PD, Godfrey, KM, Harding, JE, Owens, JA & Robinson, JS (1993) Fetal nutrition and cardiovascular disease in adult life. Lancet 341, 938–941.CrossRefGoogle ScholarPubMed
Barker, DJ, Hales, CN, Fall, CH, Osmond, C, Phipps, K & Clark, PM (1993) Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62–67.CrossRefGoogle ScholarPubMed
Barton-Davis, ER, Shoturma, DI & Sweeney, HL (1999) Contribution of satellite cells to IGF-I induced hypertrophy of skeletal muscle. Acta Physiol Scand 167, 301–305.CrossRefGoogle ScholarPubMed
Bedi, KS, Birzgalis, AR, Mahon, M, Smart, JL & Wareham, AC (1982) Early life undernutrition in rats. 1. Quantitative histology of skeletal muscles from underfed young and refed adult animals. Br J Nutr 47, 417–431.CrossRefGoogle Scholar
Bravo, R, Frank, R, Blundell, PA & Macdonald-Bravo, H (1987) Cyclin/PCNA is the auxiliary protein of DNA polymerase-delta. Nature 326, 515–517.CrossRefGoogle ScholarPubMed
Clelland, AK (2001) Intra-litter variation in early porcine muscle development. PhD thesis. University of London, UK.Google Scholar
Clemmons, DR & Van Wyk, JJ (1981) Somatomedin-C and platelet-derived growth factor stimulate human fibroblast replication. J Cell Physiol 106, 361–367.CrossRefGoogle ScholarPubMed
Coleman, ME, DeMayo, F, Yin, KC, Lee, HM, Geske, R, Montgomery, C & Schwartz, RJ (1995) Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J Biol Chem 270, 12109–12116.CrossRefGoogle ScholarPubMed
Condon, K, Silberstein, L, Blau, HM & Thompson, WJ (1990) Development of muscle fibre types in the prenatal rat hindlimb. Dev Biol 138, 256–274.CrossRefGoogle ScholarPubMed
Cornelison, DD & Wold, BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191, 270–283.CrossRefGoogle ScholarPubMed
Donalies, M, Cramer, M, Ringwald, M & Starzinski-Powitz, A (1991) Expression of M-cadherin, a member of the cadherin multigene family, correlates with differentiation of skeletal muscle cells. Proc Natl Acad Sci USA 88, 8024–8028.CrossRefGoogle ScholarPubMed
Dwyer, CM, Madgwick, AJ, Ward, SS & Stickland, NC (1995) Effect of maternal undernutrition in early gestation on the development of fetal myofibres in the guinea-pig. Reprod Fertil Dev 7, 1285–1292.CrossRefGoogle ScholarPubMed
Dwyer, CM & Stickland, NC (1992) The effects of maternal undernutrition on maternal and fetal serum insulin-like growth factors, thyroid hormones and cortisol in the guinea pig. J Dev Physiol 18, 303–313.Google ScholarPubMed
Dwyer, CM, Stickland, NC & Fletcher, JM (1994) The influence of maternal nutrition on muscle fiber number development in the porcine foetus and on subsequent postnatal growth. J Anim Sci 72, 911–917.CrossRefGoogle ScholarPubMed
Ewton, DZ, Coolican, SA, Mohan, S, Chernausek, SD & Florini, JR (1998) Modulation of insulin-like growth factor binding protein (IGFBP)-4 and IGFBP-5: a dual role for IGFBP-5. J Cell Phys 177, 47–57.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Ewton, DZ & Florini, JR (1995) IGF binding proteins-4, -5 and -6 may play specialized roles during L6 myoblast proliferation and differentiation. J Endocrinol 144, 539–553.CrossRefGoogle ScholarPubMed
Florini, JR, Ewton, DZ & Coolican, SA (1996) Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev 17, 481–517.Google ScholarPubMed
Goldspink, DF, Cox, VM, Smith, SK, Eaves, LA, Osbaldeston, NJ, Lee, DM & Mantle, D (1995) Muscle growth in response to mechanical stimuli. Am J Physiol 268, E288–E297.Google ScholarPubMed
Greenwood, PL, Slepetis, RM, Hermanson, JW & Bell, AW (1999) Intrauterine growth retardation is associated with reduced cell cycle activity, but not myofibre number, in ovine fetal muscle. Reprod Fertil Dev 11, 281–291.CrossRefGoogle Scholar
Grounds, MD, Garrett, KL, Lai, MC, Wright, WE & Beilharz, MW (1992) Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res 267, 99–104.CrossRefGoogle ScholarPubMed
Hameed, M, Orrell, RW, Cobbold, M, Goldspink, G & Harridge, SD (2003) Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance exercise. J Physiol 547, 247–254.CrossRefGoogle Scholar
Hawke, TJ & Garry, DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91, 534–551.CrossRefGoogle ScholarPubMed
Jaskulski, D, deRiel, JK, Mercer, WE, Calabretta, B & Baserga, R (1988) Inhibition of cellular proliferation by antisense oligodeoxynucleotides to PCNA cyclin. Science 240, 1544–1546.CrossRefGoogle ScholarPubMed
Johnson, SE & Allen, RE (1993) Proliferating cell nuclear antigen (PCNA) is expressed in activated rat skeletal muscle satellite cells. J Cell Physiol 154, 39–43.CrossRefGoogle ScholarPubMed
McPherron, AC & Lee, SJ (1997) Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94, 12457–12461.CrossRefGoogle ScholarPubMed
Matsumura, Y, Domeki, M, Sugahara, K, Kubo, T, Roberts, CT Jr, LeRoith, D & Kato, H (1996) Nutritional regulation of insulin-like growth factor-I receptor mRNA levels in growing chickens. Biosci Biotechnol Biochem 60, 979–982.CrossRefGoogle ScholarPubMed
Melone, MA, Peluso, G, Galderisi, U, Petillo, O & Cotrufo, R (2000) Increased expression of IGF-binding protein-5 in Duchenne muscular dystrophy (DMD) fibroblasts correlates with the fibroblast-induced downregulation of DMD myoblast growth: an in vitro analysis. J Cell Physiol 185, 143–153.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Mi, J, Law, C, Zhang, KL, Osmond, C, Stein, C & Barker, D (2000) Effects of infant birthweight and maternal body mass index in pregnancy on components of the insulin resistance syndrome in China. Ann Intern Med 132, 253–260.CrossRefGoogle ScholarPubMed
Mitchell, PJ, Johnson, SE & Hannon, K (2002) Insulin-like growth factor I stimulates myoblast expansion and myofiber development in the limb. Dev Dyn 223, 12–23.CrossRefGoogle ScholarPubMed
Owino, V, Yang, SY & Goldspink, G (2001) Age-related loss of skeletal muscle function and the inability to express the autocrine form of insulin-like growth factor-1 (MGF) in response to mechanical overload. FEBS Lett 505, 259–263.CrossRefGoogle ScholarPubMed
Powell-Braxton, L, Hollingshead, P, Warburton, C, Dowd, M, Pitts-Meek, S, Dalton, D, Gillett, N & Stewart, TA (1993) IGF-I is required for normal embryonic growth in mice. Genes Dev 7, 2609–2617.CrossRefGoogle ScholarPubMed
Rayne, J & Crawford, GN (1975) Increase in fibre numbers of the rat pterygoid muscles during postnatal growth. J Anat 119, 347–357.Google ScholarPubMed
Saintonge, J & Rosso, P (1981) Placental blood flow and transfer of nutrient analogs in large, average, and small guinea pig littermates. Pediatr Res 15, 152–156.CrossRefGoogle ScholarPubMed
Sjögren, K, Liu, JL & Blad, K (1999) Liver-derived insulin-like growth factor I (IGF-I) is the principal source of IGF-I in blood but is not required for postnatal body growth in mice. Proc Natl Acad Sci USA 96, 7088–7092.CrossRefGoogle Scholar
Tomita, M, Shimokawa, I, Higami, Y, Yanagihara-Outa, K, Kawahara, T, Tanaka, K, Ikeda, T & Shindo, H (2001) Modulation by dietary restriction in gene expression related to insulin-like growth factor-1 in rat muscle. Aging 13, 273–281.Google ScholarPubMed
Ward, SS & Stickland, NC (1991) Why are slow and fast muscles differentially affected during prenatal undernutrition?. Muscle Nerve 14, 259–267.CrossRefGoogle ScholarPubMed
Wilson, SJ, Ross, JJ & Harris, AJ (1988) A critical period for formation of secondary myotubes defined by prenatal undernourishment in rats. Development 102, 815–821.CrossRefGoogle ScholarPubMed
Yakar, S, Liu, JL, Stannard, B, Butler, A, Accili, D, Sauer, B & LeRoith, D (1999) Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc Natl Acad Sci USA 96, 7324–7329.CrossRefGoogle ScholarPubMed
Yang, H, Alnaqeeb, M, Simpson, H & Goldspink, G (1997) Changes in muscle fibre type, muscle mass and IGF-I gene expression in rabbit skeletal muscle subjected to stretch. J Anat 190, 613–622.CrossRefGoogle ScholarPubMed