Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T12:03:43.770Z Has data issue: false hasContentIssue false

Delayed muscle development in small pig fetuses around birth cannot be rectified by maternal early feed restriction and subsequent overfeeding during gestation

Published online by Cambridge University Press:  14 July 2015

M. H. Perruchot*
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France
L. Lefaucheur
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France
I. Louveau
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France
L. Mobuchon
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France
M. F. Palin
Affiliation:
Agriculture and Agri-Food Canada, Dairy and Swine R & D Centre, 2000 College Street, Sherbrooke, Québec J1M 0C8, Canada
C. Farmer
Affiliation:
Agriculture and Agri-Food Canada, Dairy and Swine R & D Centre, 2000 College Street, Sherbrooke, Québec J1M 0C8, Canada
F. Gondret
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France
Get access

Abstract

Intrauterine variations in nutrient allowance can alter body composition and tissue features of the porcine offspring around birth. This study aimed to determine the effects of fetal weight variations between littermates and of maternal dietary regimen during gestation on fetal muscle traits just before birth. Fourteen pregnant gilts were reared under a conventional (control, CTL; n=7) or an experimental (treatment, TRT; n=7) dietary regimen during gestation. The dietary treatment provided 70% of the protein and digestible energy contents of the CTL diet during the first 70 days of gestation and then, 115% of the protein and digestible energy contents up to farrowing. At 110 days of gestation, sows were sacrificed and one fetus having a low (824±140 g) and one having a normal (1218±192 g) BW per litter were sampled. Irrespective of maternal dietary regimen, the longissimus muscle of the small fetuses exhibited higher expression levels of DLK1/Pref1 and NCAM1/CD56, two genes known to be downregulated during normal skeletal muscle development. Expression levels of the embryonic isoform of the myosin heavy chain (MyHC), both at the mRNA and at the protein levels, were also higher in small fetuses. In addition, the ratios of perinatal to embryonic and of adult fast to developmental MyHC isoforms were generally lower in light fetuses compared with their medium-weight littermates. These modifications suggest a delayed myofiber development in spontaneous growth-retarded fetuses. Finally, GLUT1 was expressed to a lesser extent in the muscle of small v. normal fetuses, suggesting decreased ability for glucose uptake in muscle. Initial feed restriction and subsequent overfeeding of sows during gestation led to a lower expression of the myogenic factor MYOD1, a prerequisite for myogenic initiation in skeletal muscle. This maternal strategy was also associated with a lower expression level of insulin-like growth factor 1 receptor (IGFR) but an upregulation of IGF2. This suggests an altered susceptibility of muscle cells to IGFs’ signal in fetuses from treated sows. Altogether, intrauterine growth restriction impaired fetal muscle development, and restricted feeding followed by overfeeding of gestating sows did not allow small fetuses to recover normal contractile and metabolic characteristics.

Type
Research Article
Copyright
© The Animal Consortium 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andersen, DC, Schrøder, HD and Jensen, CH 2008. Non-cultured adipose-derived CD45- side population cells are enriched for progenitors that give rise to myofibres in vivo. Experimental Cell Research 314, 29512964.Google Scholar
Bérard, J, Pardo, CE, Béthaz, S, Kreuzer, M and Bee, G 2010. Intrauterine crowding decreases average birth weight and affects muscle fiber hyperplasia in piglets. Journal of Animal Science 88, 32423250.Google Scholar
Bérard, J, Kalbe, C, Lösel, D, Tuchscherer, A and Rehfeldt, C 2011. Potential sources of early-postnatal increase in myofibre number in pig skeletal muscle. Histochemistry and Cellular Biology 136, 217225.Google Scholar
Brown, LD 2014. Endocrine regulation of fetal skeletal muscle growth: impact on future metabolic health. Journal of Endocrinology 221, R13R29.Google Scholar
Cerisuelo, A, Baucells, MD, Gasa, J, Coma, D, Carrión, D, Chapinal, N and Sala, R 2009. Increased sow nutrition during midgestation affects muscle fiber development and meat quality, with no consequences on growth performance. Journal of Animal Science 87, 729739.Google Scholar
de Zegher, F, Díaz, M, Sebastiani, G, Martín-Ancel, A, Sánchez-Infantes, D, López-Bermejo, A and Ibáñez, L 2012. Abundance of circulating preadipocyte factor 1 in early life. Diabetes Care 35, 848849.Google Scholar
Farmer, C, Palin, MF and Martel-Kennes, Y 2014. Impact of diet deprivation and subsequent overallowance during gestation on mammary gland development and lactation performance. Journal of Animal Science 92, 141151.Google Scholar
Foxcroft, GR, Dixon, WT, Novak, S, Putman, CT, Town, SC and Vinsky, MDA 2006. The biological basis for prenatal programming of postnatal performance in pigs. Journal of Animal Science 84, E105E122.Google Scholar
Gaster, M, Handberg, A, Beck-Nielsen, H and Schroeder, HD 2000. Glucose transporter expression in human skeletal muscle fibers. American Journal of Physiology Endocrinolology and Metabolism 279, 529538.CrossRefGoogle ScholarPubMed
Gondret, F, Perruchot, MH, Tacher, S, Bérard, J and Bee, G 2011. Differential gene expressions in subcutaneous adipose tissue pointed to a delayed adipocytic differentiation in small pig fetuses compared to their heavier siblings. Differentiation 81, 253260.Google Scholar
Gondret, F, Père, MC, Tacher, S, Daré, S, Trefeu, C, Le Huërou-Luron, I and Louveau, I 2013. Spontaneous intra-uterine growth restriction modulates the endocrine status and the developmental expression of genes in porcine fetal and neonatal adipose tissue. General and Comparative Endocrinology 194, 208216.Google Scholar
Karunaratne, JF, Bayol, SA, Ashton, CJ, Simbi, BH and Stickland, NC 2009. Potential molecular mechanisms for the prenatal compartmentalization of muscle and connective tissue in pigs. Differentiation 77, 290297.Google Scholar
Lefaucheur, L, Milan, D, Ecolan, P and Le Callenec, C 2004. Myosin heavy chain composition of different skeletal muscles in Large White and Meishan pigs. Journal of Muscle Research and Cell Motility 82, 19311941.Google ScholarPubMed
Lefaucheur, L, Ecolan, P, Lossec, G, Gabillard, JC, Butler-Browne, GS and Herpin, P 2001. Influence of early postnatal cold exposure on myofiber maturation in pig skeletal muscle. Journal of Muscle Research and Cell Motilility 22, 439452.Google Scholar
Louveau, I, Combes, S, Cochard, A and Bonneau, M 1996. Developmental changes in insulin-like growth factor-I (IGF-I) receptor levels and plasma IGF-I concentrations in large white and Meishan pigs. General and Comparative Endocrinology 104, 2936.Google Scholar
Markham, TC, Latorre, RM, Lawlor, PG, Ashton, CJ, McNamara, LB, Natter, R, Rowlerson, A and Stickland, NC 2009. Developmental programming of skeletal muscle phenotype/metabolism. Animal 3, 10011012.Google Scholar
McNamara, LB, Giblin, L, Markham, T, Stickland, NC, Berry, DP, O’Reilly, JJ, Lynch, PB, Kerry, JP and Lawlor, PG 2011. Nutritional intervention during gestation alters growth, body composition and gene expression patterns in skeletal muscle of pig offspring. Animal 5, 11951206.Google Scholar
Nissen, PM, Danielsen, VO, Jorgensen, PF and 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, 30183027.Google Scholar
Oczkowicz, M, Piestrzyska-Kajtoch, A, Piórkowska, K, Rejduch, B and Rózycki, M 2010. Expression of DLK1 and MEG3 genes in porcine tissues during postnatal development. Genetics and Molecular Biology 33, 790794.Google Scholar
Oksbjerg, N, Gondret, F and Vestergaard, M 2004. Basic principles of muscle development and growth in meat-producing mammals as affected by the insulin-like growth factor (IGF) system. Domestic Animal Endocrinology 27, 219240.Google Scholar
Patruno, M, Caliaro, F, Maccatrozzo, L, Sacchetto, R, Martinello, T, Toniolo, L, Reggiani, C and Mascarello, F 2008. Myostatin shows a specific expression pattern in pig skeletal and extraocular muscles during pre- and post-natal growth. Differentiation 76, 168181.Google Scholar
Peault, B, Rudnicki, M, Torrente, Y, Cossu, G, Tremblay, JP, Partridge, T, Gussoni, E, Kunkel, LM and Huard, J 2007. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Molecular Therapy 15, 867877.CrossRefGoogle ScholarPubMed
Perruchot, MH, Ecolan, P, Sorensen, IL, Oksbjerg, N and Lefaucheur, L 2012. In vitro characterization of proliferation and differentiation of pig satellite cells. Differentiation 84, 322329.Google Scholar
Perruchot, MH, Lefaucheur, L, Barreau, C, Casteilla, L and Louveau, I 2013. Age-related changes in the features of porcine adult stem cells isolated from adipose tissue and skeletal muscle. American Journal of Physiology-Cell Physiology 305, C728C738.Google Scholar
Rehfeldt, C, Lefaucheur, L, Block, J, Stabenow, B, Pfuhl, R, Otten, W, Metges, CC and Kalbe, C 2012. Limited and excess protein intake of pregnant gilts differently affects body composition and cellularity of skeletal muscle and subcutaneous adipose tissue of newborn and weanling piglets. European Journal of Nutrition 51, 151165.Google Scholar
Rehfeldt, C, Te Pas, MF, Wimmers, K, Brameld, JM, Nissen, PM, Berri, C, Valente, LM, Power, DM, Picard, B, Stickland, NC and Oksbjerg, N 2011. Advances in research on the prenatal development of skeletal muscle in animals in relation to the quality of muscle-based food. I. Regulation of myogenesis and environmental impact. Animal 5, 718730.CrossRefGoogle Scholar
Santalucia, T, Camps, M, Castelló, A, Muñoz, P, Nuel, A, Testar, X, Palacin, M and Zorzano, A 1992. Developmental regulation of GLUT-1 (erythroid/Hep G2) and GLUT-4 (muscle/fat) glucose transporter expression in rat heart, skeletal muscle, and brown adipose tissue. Endocrinology 130, 837846.Google Scholar
White, JD, Vuocolo, T, McDonagh, M, Grounds, MD, Harper, GS, Cockett, NE and Tellam, R 2008. Analysis of the callipyge phenotype through skeletal muscle development; association of Dlk1 with muscle precursor cells. Differentiation 76, 283298.Google Scholar
Wigmore, PM and Stickland, NC 1983. Muscle development in large and small pig fetuses. Journal of Anatomy 137, 235245.Google Scholar
Wilschut, KJ, Jaksani, S, Van Den Dolder, J, Haagsman, HP and Roelen, BA 2008. Isolation and characterization of porcine adult muscle-derived progenitor cells. Journal of Cellular Biochemistry. 105, 12281239.Google Scholar