Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

In utero effects on livestock muscle development and body composition

John M. Brameld A B and Zoe C. T. R. Daniel A
+ Author Affiliations
- Author Affiliations

A Division of Nutritional Sciences, University of Nottingham, School of Biosciences, Loughborough, LE12 5RD, United Kingdom.

B Corresponding author. Email: john.brameld@nottingham.ac.uk

Australian Journal of Experimental Agriculture 48(7) 921-929 https://doi.org/10.1071/EA08017
Submitted: 7 January 2008  Accepted: 1 April 2008   Published: 20 June 2008

Abstract

This review will focus on the evidence for in utero effects on development of skeletal muscle in farm and laboratory animals, particularly sheep and pigs. We will describe genetic and environmental factors that have been shown to alter the numbers of muscle fibres formed and outline our working hypothesis for the mechanism involved and the critical window during pregnancy when these effects are seen. We will then discuss the long-term consequences in terms of body composition. Although this review concentrates on skeletal muscle development, the mechanism we suggest might be equally applicable to other tissues in the body (e.g. the brain, kidneys or sex organs) and, therefore, impact on their physiological functions.


References


Allen RE, Luiten LS, Dodson MV (1985) Effect of insulin and linoleic acid on satellite cell differentiation. Journal of Animal Science 60, 1571–1579.
CAS | PubMed |
open url image1

Bass JJ , Sharma M , Oldham J , Kambadur R (2000) Muscle growth and genetic regulation. In ‘Ruminant physiology: digestion, metabolism, growth and reproduction’. (Ed. PB Cronje) pp. 227–236. (CABI Publishing: Wallingford, UK)

Bee G (2004) Effect of early gestation feeding, birth weight and gender of progeny on muscle fiber characteristics of pigs at slaughter. Journal of Animal Science 82, 826–836.
CAS | PubMed |
open url image1

Bispham J, Dandrea J, Mostyn A, Brameld JM, Buttery PJ, Stephenson T, Symonds ME (2002) Impact of maternal nutrient restriction in early to mid gestation on leptin, insulin-like growth factor-I (IGF-I) and growth hormone receptor (GHR) mRNA abundance in adipose tissue of the fetal lamb. Early Human Development 68, 135–136. open url image1

Brameld JM (1997) Molecular mechanisms involved in the nutritional and hormonal regulation of growth in pigs. Proceedings of the Nutrition Society 56, 607–619.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Brameld JM, Buttery PJ, Dawson JM, Harper JMM (1998) Nutritional and hormonal control of skeletal muscle cell growth and differentiation. Proceedings of the Nutrition Society 57, 207–217.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Brameld JM, Gilmour RS, Buttery PJ (1999) Glucose and amino acids interact with hormones to control expression of insulin-like growth factor-I (IGF-I) and growth hormone receptor (GHR) mRNA by cultured pig hepatocytes. Journal of Nutrition 129, 1298–1306.
CAS | PubMed |
open url image1

Brameld JM, Mostyn A, Dandrea J, Stephenson TJ, Dawson JM, Buttery PJ, Symonds ME (2000) Maternal nutrition alters expression of insulin-like growth factors in fetal sheep liver and skeletal muscle. Journal of Endocrinology 167(3), 429–437.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Brameld JM, Fahey AJ, Langley-Evans SC, Buttery PJ (2003) Nutritional and hormonal control of muscle growth and fat deposition. Archives of Animal Breeding 46(special issue), 143–156. open url image1

Budge H, Bryce A, Owens JA, Stephenson T, Symonds ME, McMillen IC (2002) Differential effects of nutrient restriction in late gestation and placental restriction throughout gestation on uncoupling protein 1 expression in fetal perirenal adipose tissue. Early Human Development 66, 43. open url image1

Buttery PJ , Brameld JM , Dawson JM (2000) Control and manipulation of hyperplasia and hypertrophy in muscle tissue. In ‘Ruminant physiology: digestion, metabolism, growth and reproduction’. (Ed. PB Cronje) pp. 237–254. (CAB International: Wallingford, UK)

Chang KC (2007) Key signalling factors and pathways in the molecular determination of skeletal muscle phenotype. Animal 1, 681–698.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Daenzer M, Ortmann S, Klaus S, Metges CC (2002) Prenatal high protein exposure decreases energy expenditure and increases adiposity in young rats. Journal of Nutrition 132, 142–144.
CAS | PubMed |
open url image1

Daniel ZCTR, Brameld JM, Craigon J, Scollan N, Buttery PJ (2007) Effect of maternal dietary restriction on lamb carcass characteristics and muscle fiber composition. Journal of Animal Science 85, 1565–1576.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Dwyer CM, Stickland NC, Fletcher JM (1994) The influence of maternal nutrition on muscle fiber number development in the porcine fetus and on subsequent postnatal growth. Journal of Animal Science 72, 911–917.
CAS | PubMed |
open url image1

Dwyer CM, Madgwick AJA, Ward SS, Strickland NC (1995) Effect of maternal undernutrition in early gestation on the development of fetal myofibres in the guinea‐pig. Reproduction, Fertility and Development 7, 1285–1292.
CAS | Crossref |
open url image1

Fahey AJ, Brameld JM, Parr T, Buttery PJ (2005a) Ontogeny of factors associated with proliferation and differentiation of muscle in the ovine fetus. Journal of Animal Science 83, 2330–2338.
CAS | PubMed |
open url image1

Fahey AJ, Brameld JM, Parr T, Buttery PJ (2005b) The effect of maternal under-nutrition before muscle differentiation on the muscle fiber development of the newborn lamb. Journal of Animal Science 83, 2564–2571.
CAS | PubMed |
open url image1

Fiorotto ML, Davis TA, Schoknecht P, Mersmann HJ, Pond WG (1995) Both maternal over- and under-nutrition during gestation increase the adiposity of young progeny in rats. Obesity Research 3(2), 131–141.
CAS | PubMed |
open url image1

Florini JR, Ewton DZ, Coolican SA (1996) Growth hormone and the insulin-like growth factor system in myogenesis. Endocrine Reviews 17, 481–517.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ford SP, Hess BW, Schwope MM, Nijland MJ, Gilbert JS, Vonnahme KA, Means WJ, Han H, Nathanielsz PW (2007) Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. Journal of Animal Science 85, 1285–1294.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gagniere H, Picard B, Geay Y (1999) Contractile differentiation of foetal cattle muscles: intermuscular variability. Reproduction, Nutrition, Development 39, 637–655.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gatford KL, Ekert JE, Blackmore K, De Blasio MJ, Boyce JM, Owens JA, Campbell RG, Owens PC (2003) Variable maternal nutrition and growth hormone treatment in the second quarter of pregnancy in pigs alter semitendinosus muscle in adolescent progeny. British Journal of Nutrition 90, 283–293.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gerrard DE, Grant AL (1994) Insulin-like growth factor-II expression in developing skeletal muscle of double muscled and normal cattle. Domestic Animal Endocrinology 11, 339–347.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gondret F, Lefaucheur L, Juin H, Louveau I, Lebret B (2006) Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs. Journal of Animal Science 84, 93–103.
CAS | PubMed |
open url image1

Gopalakrishnan G, Rhind SM, Stephenson T, Kyle CE, Brooks AN, Rae MT, Symonds ME (2001) Effect of maternal nutrient restriction at defined periods in early to mid gestation on placento-fetal, kidney and adipose tissue weights at 110 days gestation in sheep. Early Human Development 63, 58–59. open url image1

Hurley MS, Flux C, Salter AM, Brameld JM (2006) Effects of fatty acids on skeletal muscle cell differentiation in vitro. British Journal of Nutrition 95, 623–630.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Jiang YL, Li N, Fan XZ, Xiao LR, Xiang RL, Hu XX, Du LX, Wu CX (2002a) Associations of T -> A mutation in the promoter region of myostatin gene with birth weight in Yorkshire pigs. Asian-Australasian Journal of Animal Sciences 15, 1543–1545.
CAS |
open url image1

Jiang YL, Li N, Plastow G, Liu ZL, Hu XX, Wu CX (2002b) Identification of three SNPs in the porcine myostatin gene (MSTN). Animal Biotechnology 13, 173–178.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lefaucheur L, Edom F, Ecolan P, Butler-Browne GS (1995) Pattern of muscle fiber type formation in the pig. Developmental Dynamics 203, 27–41.
CAS |
open url image1

Mallinson JE, Sculley DV, Craigon J, Plant R, Langley-Evans SC, Brameld JM (2007) Fetal exposure to a maternal low-protein diet during mid-gestation results in muscle-specific effects on fibre type composition in young rats. British Journal of Nutrition 98, 292–299.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Maltin CA, Delday MI, Sinclair KD, Steven J, Sneddon AA (2001) Impact of manipulations of myogenesis in utero on the performance of adult skeletal muscle. Reproduction (Cambridge, England) 122, 359–374.
CAS | PubMed |
open url image1

McPherron AC, Lawler AM, Lee SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-β superfamily member. Nature 387, 83–90.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Musser RE, Goodband RD, Tokach MD, Owen KQ, Nelssen JL, Blum SA, Dritz SS, Civis CA (1999) Effects of L-carnitine fed during gestation and lactation on sow and litter performance. Journal of Animal Science 77, 3289–3295.
CAS | PubMed |
open url image1

Musser RE, Goodband RD, Owen KQ, Davis DL, Tokach MD, Dritz SS, Nelssen JL (2001) Determining the effect of increasing L-carnitine additions on sow performance and muscle fiber development of the offspring. Journal of Animal Science 79(Supp. 1), 65. open url image1

Nissen PM, Danielsen VO, Jorgensen PF, Oksbjerg N (2003) Increased maternal nutrition of sows has no beneficial effects on muscle fiber number or postnatal growth and has no impact on the meat quality of the offspring. Journal of Animal Science 81, 3018–3027.
CAS | PubMed |
open url image1

Nordby DJ, Field RA, Riley ML, Kercher CJ (1987) Effects of maternal undernutrition during early pregnancy on growth, muscle cellularity, fiber type and carcass composition in lambs. Journal of Animal Science 64, 1419–1427.
CAS | PubMed |
open url image1

Picard B, Lefaucheur L, Berri C, Duclos MJ (2002) Muscle fibre ontogenesis in farm animal species. Reproduction, Nutrition, Development 42, 415–431.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Powell SE, Aberle ED (1981) Skeletal muscle and adipose tissue cellularity in runt and normal birth weight swine. Journal of Animal Science 52, 748–756.
CAS | PubMed |
open url image1

Quigley SP, Kleemann DO, Kakar MA, Owens JA, Nattrass GS, Maddocks S, Walker SK (2005) Myogenesis in sheep is altered by maternal feed intake during the peri-conception period. Animal Reproduction Science 87, 241–251.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rehfeldt C, Kuhn G (2006) Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. Journal of Animal Science 84(E. suppl.), E113–E123.
PubMed |
open url image1

Rehfeldt C, Fiedler I, Weikard R, Kanitz E, Ender K (1993) It is possible to increase skeletal muscle fibre number in utero. Bioscience Reports 13, 213–220.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rehfeldt C, Kuhn G, Vanselow J, Furbass R, Fiedler I, Nurnberg G, Clelland AK, Stickland NC, Ender K (2001) Maternal treatment with somatotropin during early gestation affects basic events of myogenesis in pigs. Cell and Tissue Research 306, 429–440.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rehfeldt C, Kuhn G, Ender K (2002) Effects of exogenous somatotropin during early gestation on postnatal development of muscle fibers in pigs. Journal of Animal Science 80(Suppl. 1), 209. open url image1

Smith JA, Lewis AM, Wiener P, Williams JL (2000) Genetic variation in the bovine myostatin gene in UK beef cattle: allele frequencies and haplotype analysis in the South Devon. Animal Genetics 31, 306–309.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Stubbs AK, Wheelhouse NM, Lomax MA, Hazlerigg DG (2002) Nutrient-hormone interaction in the ovine liver: methionine supply selectively modulates growth hormone-induced IGF-1 gene expression. Journal of Endocrinology 174, 335–341.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Tilley RE, McNeil CJ, Ashworth CJ, Page KR, McArdle HJ (2007) Altered muscle development and expression of the insulin-like growth factor system in growth retarded fetal pigs. Domestic Animal Endocrinology 32, 167–177.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD (2000) Fetal origins of hyperphagia, obesity and hypertension and its postnatal amplifications by hypercaloric nutrition. American Journal of Physiology 279, E83–E87.
CAS | PubMed |
open url image1

Wheelhouse NM, Stubbs AK, Lomax MA, MacRae JC, Hazlerigg DG (1999) Growth hormone and amino acid supply interact synergistically to control insulin-like growth factor-I production and gene expression in cultured ovine hepatocytes. Journal of Endocrinology 163, 353–361.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
CAS | PubMed |
open url image1

Wilson SJ, McEwan JC, Sheard PW, Harris AJ (1992) Early stages of myogenesis in a large mammal: formation of successive generations of myotubes in sheep tibialis cranialis muscle. Journal of Muscle Research and Cell Motility 13, 534–550.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Zhu MJ, Ford SP, Nathanielsz PW, Du M (2004) Effect of maternal nutrient restriction in sheep on the development of fetal skeletal muscle. Biology of Reproduction 71, 1968–1973.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Zhu MJ, Ford SP, Means WJ, Hess BW, Nathanielsz PW, Du M (2006) Maternal nutrient restriction affects properties of skeletal muscle in offspring. Journal of Physiology 575, 241–250.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1