Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-26T04:15:26.110Z Has data issue: false hasContentIssue false
  • English
  • Français

The influence of maternal nutrition on expression of genes responsible for adipogenesis and myogenesis in the bovine fetus

Published online by Cambridge University Press:  28 April 2016

T. D. Jennings ,
M. G. Gonda ,
K. R. Underwood ,
A. E. Wertz-Lutz  and
A. D. Blair
T. D. Jennings
Affiliation:
Department of Animal Science, South Dakota State University, Brookings, SD 57007, USA
M. G. Gonda
Affiliation:
Department of Animal Science, South Dakota State University, Brookings, SD 57007, USA
K. R. Underwood
Affiliation:
Department of Animal Science, South Dakota State University, Brookings, SD 57007, USA
A. E. Wertz-Lutz
Affiliation:
Department of Animal Science, South Dakota State University, Brookings, SD 57007, USA
A. D. Blair*
Affiliation:
Department of Animal Science, South Dakota State University, Brookings, SD 57007, USA
*
†E-mail: amanda.blair@sdstate.edu
Get access

Abstract

The objective of this study was to determine whether altered maternal energy supply during mid-gestation results in differences in muscle histology or genes regulating fetal adipose and muscle development. In total, 22 Angus cross-bred heifers (BW=527.73±8.3 kg) were assigned randomly to the three dietary treatments providing 146% (HIGH; n=7), 87% (INT; n=7) or 72% (LOW; n=8) of the energy requirements for heifers from day 85 to day 180 of gestation. Fetuses were removed via cesarean section at day 180 of gestation and longissimus muscle (LM) and subcutaneous fat were collected and prepared for analysis of gene expression. Samples from the LM and semitendinosus (ST) were evaluated for muscle fiber diameter, area and number. The right hind limb was dissected and analyzed to determine compositional analysis. Fetal growth and muscle histology characteristics of the LM and ST were similar among treatments. Preadipocyte factor-1 expression was up-regulated in fetal LM (P<0.05) of HIGH fetuses as compared with INT, whereas LOW fetuses showed increased CCAAT/enhancer-binding protein-β (C/EBP-β) expression in LM as compared with INT (P<0.05). Peroxisome proliferator-activated receptor γand C/EBP-α did not differ as a result of dietary treatment in LM or subcutaneous fat samples. There was a tendency for increased expression of fatty acid synthase in LM of LOW fetuses as compared with INT (P<0.10). Myogenin was more highly expressed (P<0.05) in LM of the LOW fetuses, whereas μ-calpain expression was increased in the HIGH treatment compared with INT. A tendency for increased expression of IGF-II was observed for both LOW and HIGH fetuses compared with INT (P<0.10). Expression of stearoyl-CoA desaturase, myoblast determination protein 1, myogenic factor 5, myogenic regulatory factor-4, m-calpain, calpastatin, IGF-I and myostatin was similar between treatments. Collectively, these results suggest that fetal growth characteristics are not affected by the level of maternal nutritional manipulation imposed in this study during mid-gestation. However, differences in expression of fetal genes regulating adipose and muscle tissue growth and development could lead to differences in postnatal composition and warrants further investigation.

Keywords

fetal programmingbovinemyogenesisadipogenesis
Type
Research Article
Information
animal , Volume 10 , Issue 10 , October 2016 , pp. 1697 - 1705
Copyright
© The Animal Consortium 2016 

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

Association of Official Analytical Chemists 1990. Official methods of analysis, 15th edition. AOAC, Arlington, VA, USA.Google Scholar
Barnoy, S, Glaser, T and Kosower, NS 1997. Calpain and calpastatin in myoblast differentiation and fusion effects of inhibitors. Biochimica et Biophysica Acta 1358, 181–188.CrossRefGoogle ScholarPubMed
Beef Cattle NRC 2000. Nutrient requirements of beef cattle, 7th revised edition. National Academies Press, Washington, DC, USA.Google Scholar
Biressi, S, Molinaro, M and Cossu, G 2007. Cellular heterogeneity during vertebrate skeletal muscle development. Developmental Biology 308, 281–293.CrossRefGoogle ScholarPubMed
Bispham, J, Gopalakrishnan, GS, Dandrea, J, Wilson, V, Budge, H, Keisler, DH, Broughton, PF, Stephenson, T and Symonds, ME 2003. Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology 144, 3575–3585.CrossRefGoogle ScholarPubMed
Bonnet, M, Cassar-Malek, I, Chilliard, Y and Picard, B 2010. Ontogenesis of muscle and adipose tissues and their interactions in ruminants and other species. Animal 4, 1093–1109.CrossRefGoogle ScholarPubMed
Brameld, JM, Mostyn, A, Dandrea, J, Stephenson, TJ, Dawson, JM, Buttery, PJ and Symonds, ME 2000. Maternal nutrition alters the expression of insulin-like growth factors in fetal sheep liver and skeletal muscle. Journal of Endocrinology 167, 429–437.CrossRefGoogle ScholarPubMed
Braun, T, Buschhausen-Denker, G, Bober, E, Tannich, E and Arnold, HH 1989. A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblast. EMBO Journal 8, 701–709.CrossRefGoogle Scholar
Brethour, JR 2000. Using serial ultrasound measures to generate models of marbling and backfat thickness changes in feedlot cattle. Journal of Animal Science 78, 2055–2061.CrossRefGoogle ScholarPubMed
Chawla, A and Lazar, MA 1994. Peroxisome proliferator and retinoid signaling pathways o-regulate preadipocyte phenotype and survival. Proceedings of the National Academy of Sciences of the United States of America 91, 1786–1790.CrossRefGoogle ScholarPubMed
Daniel, ZCTR, Brameld, JM, Craigon, J, Scollan, ND and Buttery, PJ 2007. Effect of maternal dietary restriction during pregnancy on lamb carcass characteristics and muscle fiber composition. Journal of Animal Science 85, 1565–1576.CrossRefGoogle ScholarPubMed
Darlington, GJ, Ross, SE and MacDougald, OA 1998. The role of C/EBP genes in adipocyte differentiation. Journal of Biological Chemistry 273, 300057–300060.CrossRefGoogle ScholarPubMed
Du, M, Tong, J, Zhao, J, Underwood, KR, Zhu, M, Ford, SP and Nathanielsz, PW 2010. Fetal programming of skeletal muscle development in ruminant animals. Journal of Animal Science 88, E51–E60.CrossRefGoogle ScholarPubMed
Du, M, Wang, B, Fu, X, Yang, Q and Zhu, M 2015. Fetal programming in meat production. Meat Science 109, 40–47.CrossRefGoogle ScholarPubMed
Du, M, Zhu, MJ, Means, WJ, Hess, BW and Ford, SP 2004. Effect of nutrient restriction on calpain and calpastatin content of skeletal muscle from cows and fetuses. Journal of Animal Science 82, 2541–2547.CrossRefGoogle ScholarPubMed
Faust, IM, Johnson, PR, Stern, JS and Hirsch, J 1978. Diet induced adipocyte number increase in adult rats: a new model of obesity. American Journal of Physiology 235, E279–E286.Google ScholarPubMed
Ford, SP, Hess, BW, Schwope, MM, Nijland, MJ, Gilbert, JS, Vonnahme, KA, Means, WJ, Han, H and 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.CrossRefGoogle ScholarPubMed
Ghinis-Hozumi, Y, Gonzalez-Gallardo, A, Gonzalez-Davalos, L, Antaramian, A, Villarroya, F, Shimada, A, Varela-Echavarria, A and Mora, O 2011. Bovine sirtuins: initial characterization and expression of sirtuins 1 and 3 in live, muscle, and adipose tissue. Journal of Animal Science 89, 2529–2536.CrossRefGoogle Scholar
Glass, DJ 2003. Signaling pathways that mediate skeletal muscle hypertrophy and atrophy. Nature Cell Biology 5, 87–90.CrossRefGoogle ScholarPubMed
Goll, DE, Thompson, VF, Taylor, RG and Ouali, A 1998. The calpain system and skeletal muscle growth. Canadian Journal of Animal Science 78, 503–512.CrossRefGoogle Scholar
Hannon, K, Smith, CK, Bales, KR and Santerre, RF 1992. Temporal quantitative analysis of myogenic regulatory and growth factor gene expression in the developing mouse embryo. Developmental Biology 151, 137–144.CrossRefGoogle ScholarPubMed
Lazar, MA 1999. PPARγ in adipocyte differentiation. Journal of Animal Science 77, 16–22.CrossRefGoogle Scholar
McPherron, AC, Lawler, AM and Lee, SJ 1997. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387, 83–90.CrossRefGoogle ScholarPubMed
Meyer, AM, Reed, JJ, Vonnahme, KA, Soto-Navarro, SA, Reynolds, LP, Ford, SP, Hess, BW and Canton, JS 2010. Effects of stage of gestation and nutrient restriction during early to mid-gestation on maternal and fetal visceral organ mass and indices of jejunal growth and vascularity in beef cows. Journal of Animal Science 88, 2410–2424.CrossRefGoogle ScholarPubMed
Perry, RL and Rudnicki, MA 2000. Molecular mechanisms regulating myogenic determination and differentiation. Frontiers in Bioscience 5, D750–D767.CrossRefGoogle ScholarPubMed
Pfaffl, MW, Tichopad, A, Prgomet, C and Neuvians, TP 2004. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: bestKeeper – excel-based tool using pair-wise correlations. Biotechnology Letters 26, 509–515.CrossRefGoogle ScholarPubMed
Rasby, RJ, Wetterman, RP, Geisert, RD, Rice, LE and Wallace, CR 1990. Nutrition, body composition and reproduction in beef cows: fetal and placental development, and estrogens and progesterone in plasma. Journal of Animal Science 68, 4267–4276.CrossRefGoogle Scholar
Rehfeldt, C, Lefaucheur, L, Block, J, Stabenow, B, Pfuhl, R, Otten, W, Metges, C 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, 151–165.CrossRefGoogle ScholarPubMed
Russell, RG and Oteruelo, FT 1981. An ultrastructural study of the differentiation of skeletal muscle in the bovine fetus. Anatomy and Embryology 162, 403–417.CrossRefGoogle ScholarPubMed
Sul, HS, Latasa, MJ, Moon, Y and Kim, KH 2000a. Regulation of the fatty acid synthase promoter by insulin. Journal of Nutrition 130, 315S–320S.CrossRefGoogle ScholarPubMed
Sul, HS, Smas, C, Mei, B and Zhou, L 2000b. Function of pref-1 as an inhibitor of adipocyte differentiation. International Journal of Obesity 24 (suppl. 4), S15–S19.CrossRefGoogle ScholarPubMed
Tong, J, Zhu, MJ, Underwood, KR, Hess, BW, Ford, SP and Du, M 2008. Amp-activated protein kinase and adipogenesis in sheep fetal skeletal muscle and 3T3-L1 cells. Journal of Animal Science 86, 1296–1305.CrossRefGoogle Scholar
Underwood, KR, Tong, JF, Price, PL, Roberts, AJ, Grings, EE, Hess, BW, Means, WJ and Du, M 2010. Nutrition during mid to late gestation affects growth, adipose tissue deposition, and tenderness in cross-bred beef steers. Meat Science 86, 588–593.CrossRefGoogle ScholarPubMed
Valet, P, Tavernier, G, Castan-Laurell, I, Saulnier-Blache, JS and Langin, D 2002. Understanding adipose tissue development from transgenic animal models. Journal of Lipid Research 43, 835–860.CrossRefGoogle ScholarPubMed
Wertz, AE, Berger, LL, Walker, PM, Faulkner, DB, McKeith, FK and Rodriguez-Zas, SL 2002. Early-weaning and postweaning nutritional management affect feedlot performance, carcass merit, and the relationship of 12th-rib fat, marbling score, and feed efficiency among Angus and Wagyu heifers. Journal of Animal Science 80, 28–37.CrossRefGoogle ScholarPubMed
Zhu, MJ, Ford, SP, Natanielsz, PW and Du, M 2004. Effect of maternal nutrient restriction in sheep on the development of fetal skeletal muscle. Biology of Reproduction 71, 1968–1973.CrossRefGoogle ScholarPubMed
Zhu, MJ, Ford, SP, Means, WJ, Hess, BW, Nathanielsz, PW and Du, M 2006. Maternal nutrient restriction affects properties of skeletal muscle in offspring. Journal of Physiology 575, 241–250.CrossRefGoogle ScholarPubMed