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Reduced satellite cell density and myogenesis in Wagyu compared with Angus cattle as a possible explanation of its high marbling

Published online by Cambridge University Press:  09 October 2017

X. Fu ,
Q. Yang ,
B. Wang ,
J. Zhao ,
M. Zhu ,
S. M. Parish  and
M. Du
X. Fu
Affiliation:
Department of Animal Sciences and Department of Pharmaceutical Sciences, Washington Center for Muscle Biology, Washington State University, Pullman, WA 99164, USA
Q. Yang
Affiliation:
Department of Animal Sciences and Department of Pharmaceutical Sciences, Washington Center for Muscle Biology, Washington State University, Pullman, WA 99164, USA
B. Wang
Affiliation:
Department of Animal Sciences and Department of Pharmaceutical Sciences, Washington Center for Muscle Biology, Washington State University, Pullman, WA 99164, USA
J. Zhao
Affiliation:
College of Animal Science and Veterinary Medicine, Shanxi Agricultural University, Taigu, Shanxi 030801, P. R. China.
M. Zhu
Affiliation:
School of Food Sciences, Washington State University, Pullman, WA 99164, USA
S. M. Parish
Affiliation:
College of Veterinary Medicine, Washington State University, Pullman, WA 99164, USA
M. Du*
Affiliation:
Department of Animal Sciences and Department of Pharmaceutical Sciences, Washington Center for Muscle Biology, Washington State University, Pullman, WA 99164, USA
*
†E-mail: Min.Du@wsu.edu
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Abstract

Mechanisms responsible for excellent marbling in Japanese black cattle, Wagyu, remain to be established. Because both muscle cells and intramuscular adipocytes are developed from mesenchymal progenitor cells during early muscle development, we hypothesized that intramuscular progenitor cells in Wagyu cattle have attenuated myogenic capacity in favor of adipogenesis, leading to high marbling but reduced muscle growth. Biceps femoris muscle biopsy samples were obtained from both Angus (n=3) and Wagyu (n=3) cattle at 12 months of age. Compared with Angus, the density of satellite cells was much lower in Wagyu muscle (by 45.8±10%, P<0.05). Consistently, the formation of myotubes from muscle-derived progenitor cells was also lower (by 64.2±12.9%, P<0.05), but adipogenic capacity was greater in Wagyu. The average muscle fiber diameter was larger in Wagyu (by 23.9±6.8%, P=0.089) despite less muscle mass, suggesting less muscle fiber formation in Wagyu compared with Angus cattle. Because satellite cells are derived from fetal myogenic cells, the reduction in satellite cell density together with lower muscle fiber formation suggests that myogenesis was attenuated during early muscle development in Wagyu cattle. Given the shared pool of mesenchymal progenitor cells, the attenuated myogenesis likely shifts progenitor cells to adipogenesis during early development, which may contribute to high intramuscular adipocyte formation in Wagyu cattle.

Keywords

intramuscular lipidmyogenesismarblingsatellite cellskeletal muscle
Type
Research Article
Information
animal , Volume 12 , Issue 5 , May 2018 , pp. 990 - 997
Copyright
© The Animal Consortium 2017 

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Footnotes

a

Present address: School of Animal Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.

References

Aberle, ED 1984. Myofiber differentiation in skeletal muscles of newborn runt and normal weight pigs. Journal of Animal Science 59, 1651–1656.CrossRefGoogle ScholarPubMed
Afolayan, RA, Pitchford, WS, Deland, MP and McKiernan, WA 2007. Breed variation and genetic parameters for growth and body development in diverse beef cattle genotypes. Animal 1, 13–20.Google Scholar
Albrecht, E, Gotoh, T, Ebara, F, Xu, JX, Viergutz, T, Nurnberg, G, Maak, S and Wegner, J 2011. Cellular conditions for intramuscular fat deposition in Japanese Black and Holstein steers. Meat Science 89, 13–20.Google Scholar
Archile-Contreras, AC, Mandell, IB and Purslow, PP 2010. Disparity of dietary effects on collagen characteristics and toughness between two beef muscles. Meat Science 86, 491–497.Google Scholar
Bailey, P, Holowacz, T and Lassar, AB 2001. The origin of skeletal muscle stem cells in the embryo and the adult. Current Opinion in Cell Biology 13, 679–689.Google Scholar
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.Google Scholar
Boykin, C, Eastwood, L, Harris, M, Hale, D, Kerth, C, Griffin, D, Arnold, A, Hasty, J, Belk, K and Woerner, D 2017. National Beef Quality Audit–2016: In-plant survey of carcass characteristics related to quality, quantity, and value of fed steers and heifers. Journal of Animal Science 95, 2993–3002.Google 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
Bushman, AL 2007. Correlated response in litter traits to selection for intramuscular fat in Duroc swine. Master of science thesis, Iowa state university, Ames, Iowa, United States.Google Scholar
Davis, TA and Fiorotto, ML 2009. Regulation of muscle growth in neonates. Current Opinion in Clinical Nutrition and Metabolic Care 12, 78–85.CrossRefGoogle ScholarPubMed
Dryden, F and Maechello, J 1970. Influence of total lipid and fatty acid composition upon the palatability of three bovine muscles. Journal of Animal Science 31, 36–41.Google Scholar
Du, M, Huang, Y, Das, AK, Yang, Q, Duarte, MS, Dodson, MV and Zhu, MJ 2013. Meat Science and Muscle Biology Symposium: manipulating mesenchymal progenitor cell differentiation to optimize performance and carcass value of beef cattle. Journal of Animal Science 91, 1419–1427.Google Scholar
Du, M, Wang, B, Fu, X, Yang, Q and Zhu, MJ 2015. Fetal programming in meat production. Meat Science 109, 40–47.Google Scholar
Duarte, MS, Paulino, PV, Das, AK, Wei, S, Serao, NV, Fu, X, Harris, SM, Dodson, MV and Du, M 2013. Enhancement of adipogenesis and fibrogenesis in skeletal muscle of Wagyu compared with Angus cattle. Journal of Animal Science 91, 2938–2946.Google Scholar
Fu, X, Zhao, JX, Zhu, MJ, Foretz, M, Viollet, B, Dodson, MV and Du, M 2013. AMP-activated protein kinase alpha1 but not alpha2 catalytic subunit potentiates myogenin expression and myogenesis. Molecular and Cellular Biology 33, 4517–4525.Google Scholar
Garcia, LG, Nicholson, KL, Hoffman, TW, Lawrence, TE, Hale, DS, Griffin, DB, Savell, JW, Vanoverbeke, DL, Morgan, JB, Belk, KE, Field, TG, Scanga, JA, Tatum, JD and Smith, GC 2008. National Beef Quality Audit-2005: survey of targeted cattle and carcass characteristics related to quality, quantity, and value of fed steers and heifers. Journal of Animal Science 86, 3533–3543.Google Scholar
Gesta, S, Tseng, Y-H and Kahn, CR 2007. Developmental origin of fat: tracking obesity to its source. Cell 131, 242–256.Google Scholar
Lunt, D, Riley, R and Smith, S 1993. Growth and carcass characteristics of Angus and American Wagyu steers. Meat Science 34, 327–334.CrossRefGoogle ScholarPubMed
Moore, MC, Gray, GD, Hale, DS, Kerth, CR, Griffin, DB, Savell, JW, Raines, CR, Belk, KE, Woerner, DR, Tatum, JD, Igo, JL, VanOverbeke, DL, Mafi, GG, Lawrence, TE, Delmore, RJ Jr., Christensen, LM, Shackelford, SD, King, DA, Wheeler, TL, Meadows, LR and O’Connor, ME 2012. National Beef Quality Audit-2011: in-plant survey of targeted carcass characteristics related to quality, quantity, value, and marketing of fed steers and heifers. Journal of Animal Science 90, 5143–5151.CrossRefGoogle ScholarPubMed
Tong, JF, Yan, X, Zhu, MJ, Ford, SP, Nathanielsz, PW and Du, M 2009. Maternal obesity downregulates myogenesis and beta-catenin signaling in fetal skeletal muscle. American Journal of Physiology-Endocrinology and Metabolism 296, E917–E924.CrossRefGoogle ScholarPubMed
Wei, S, Fu, X, Liang, X, Zhu, M, Jiang, Z, Parish, S, Dodson, M, Zan, L and Du, M 2015. Enhanced mitogenesis in stromal vascular cells derived from subcutaneous adipose tissue of Wagyu compared with those of Angus cattle. Journal of Animal Science 93, 1015–1024.Google Scholar
Whitley, E and Ball, J 2002. Statistics review 4: sample size calculations. Critical Care 6, 335–341.Google Scholar
Yan, X, Zhu, MJ, Xu, W, Tong, JF, Ford, SP, Nathanielsz, PW and Du, M 2010. Up-regulation of toll-like receptor 4/nuclear factor-κB signaling is associated with enhanced adipogenesis and insulin resistance in fetal skeletal muscle of obese sheep at late gestation. Endocrinology 151, 380–387.Google Scholar
Zembayashi, M and Lunt, D 1995. Distribution of intramuscular lipid throughout M. longissimus thoracis et lumborum in Japanese Black, Japanese Shorthorn, Holstein and Japanese Black crossbreds. Meat Science 40, 211–216.Google Scholar
Zhu, MJ, Ford, SP, Nathanielsz, 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.Google Scholar
Zhu, MJ, Han, B, Tong, J, Ma, C, Kimzey, JM, Underwood, KR, Xiao, Y, Hess, BW, Ford, SP, Nathanielsz, PW and Du, M 2008. AMP-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. Journal of Physiology 586, 2651–2664.Google Scholar
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