Hostname: page-component-7479d7b7d-t6hkb Total loading time: 0 Render date: 2024-07-12T03:00:16.777Z Has data issue: false hasContentIssue false

Transcriptome changes in muscle of Nellore cows submitted to recovery weight gain under grazing condition

Published online by Cambridge University Press:  09 July 2018

D. A. Fausto
Affiliation:
Animal Science Department, ‘Luiz de Queiroz’ College of Agricultural/University of Sao Paulo, Brazil (11 Padua Dias Avenue, 13418 900 Piracicaba, Sao Paulo), Brazil
A. L. J. Ferraz
Affiliation:
Animal Science Department, Mato Grosso do Sul State University, Brazil (University City of Aquidauna, 79200-000), Brazil
E. F. Delgado*
Affiliation:
Animal Science Department, ‘Luiz de Queiroz’ College of Agricultural/University of Sao Paulo, Brazil (11 Padua Dias Avenue, 13418 900 Piracicaba, Sao Paulo), Brazil
S. C. S. Andrade
Affiliation:
Animal Science Department, ‘Luiz de Queiroz’ College of Agricultural/University of Sao Paulo, Brazil (11 Padua Dias Avenue, 13418 900 Piracicaba, Sao Paulo), Brazil
L. L. Coutinho
Affiliation:
Animal Science Department, ‘Luiz de Queiroz’ College of Agricultural/University of Sao Paulo, Brazil (11 Padua Dias Avenue, 13418 900 Piracicaba, Sao Paulo), Brazil
G. L. D. Feijó
Affiliation:
Beef Cattle Research Center/Embrapa, Campo Grande, MS, Brazil (830 Rádio Maia, 79106-550, Campo Grande, Mato Grosso do Sul), Brazil
*
E-mail: efdelgad@usp.br
Get access

Abstract

The aim of this study was to evaluate transcriptome changes in the muscle tissue of Bos taurus indicus cull cows subjected to recovery weight gain under grazing conditions. In all, 38 Nellore cull cows were divided randomly into two different management groups: (1) Maintenance (MA) and (2) Recovery gain (RG) from weight loss by moderate growth under high forage availability. After slaughter, RNA analysis was performed on the Longissimus thoracis muscle. Semaphorin 4A, solute carrier family 11 member 1, and Ficolin-2 were expressed in the RG, which may indicate an inflammatory response during tissue regrowth. Signaling factors, such as Myostatin, related to fibroblast activation, negative control of satellite cell proliferation in adults and muscle protein synthesis were less abundant in the RG group. The only gene related to anabolic processes that were more abundant in the MA group was related to fat deposition. The genes that were differentially expressed in the experiment showed muscle repair-related changes during RG based on the greater expression of genes involved in inflammatory responses and the lower expression of negative regulators of muscle cell proliferation and hypertrophy.

Type
Research Article
Copyright
© The Animal Consortium 2018 

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.)

Footnotes

a

Present address: Genetic and Evolutionary Biology Department, University de Sao Paulo (Matao street, 14, 05508-090, Sao Paulo, Sao Paulo), Brazil.

References

Anders, S and Huber, W 2010. Differential expression analysis for sequences count data. Genome Biology 11, R106.1R.106.Google Scholar
Archile-Contreras, A, Mandell, IB and PURSLOW, PP 2010. Disparity of dietary effects on collagen characteristics and toughness between two beef muscles. Meat Science 86, 491497.Google Scholar
Atamas, SP and White, B 2003. Cytokine regulation of pulmonary fibrosis in scleroderma. Cytokine & Growth Factor Reviews 14, 537550.Google Scholar
Baxter, RC 2000. Insulin-like growth factor (IGF)-binding proteins: interactions with IGFs and intrinsic bioactivities. American Journal of Physiology: Endocrinology and Metabolism 278, E967E976.Google Scholar
Barton-Davis, ER, Shoturma, DI and Sweeney, HL 1999. Contribution of satellite cells to IGF-I induced hypertrophy of skeletal muscle. Acta Physiologica 167, 301305.Google Scholar
Benjamini, Y and Hochberg, Y 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B 57, 289300.Google Scholar
Bouchoux, J, Beilstein, F, Pauquai, T, Guerrera, C, Chateau, D, Ly, N, Alqub, M, Klein, C, Chambaz, J, Rousset, M, Lacorte, J, Morel, E and Demignot, S 2011. The proteome of cytosolic lipid droplets isolated from differentiated Caco-2/TC7 enterocytes reveals cell-specific characteristics. Biology of the Cell 103, 499517.Google Scholar
Brasaemle, DL and Wolins, NE 2012. Packaging of fat: an evolving model of lipid droplet assembly and expansion. Journal of Biological Chemistry 287, 22732279.Google Scholar
Byrne, KA, Wang, YH, Lehnert, SA, Harper, GS, Mcwilliam, SM, Bruce, HL and Reverter, A 2005. Gene expression profiling of muscle tissue in Brahman steers during nutritional restriction. Journal of Animal Science 83, 112.Google Scholar
Cassar-Malek, I, Hocquette, JF, Jurie, C, Listrat, A, Jailler, R, Bauchart, D, Briand, Y and Picard, B 2004. Muscle-specific metabolic, histochemical and biochemical responses to a nutritionally induced discontinuous growth path. Animal Science 79, 4959.Google Scholar
Ciciliot, S and Schiaffino, S 2010. Regeneration of mammalian skeletal muscle. Basic mechanisms and clinical implications. Current Pharmaceutical Design 16, 906914.Google Scholar
Claus, M, Weich, H, Breier, G, Knies, U, Rockl, W, Waltenberger, J and Risau, W 1996. The vascular endothelial growth factor receptor flt-1 mediates biological activities. The Journal of Biological Chemistry 271, 1762917634.Google Scholar
Clemmons, DR 1998. Role of insulin like growth factor binding proteins in controlling IGF action. Molecular and Cellular Endocrinology 140, 1924.Google Scholar
Crombrugghe, B, Vuorio, T and Karsenty, G 1990. Control of type I collagen genes in scleroderma and normal fibroblasts. Rheumatic Diseases Clinics of North America 16, 109123.Google Scholar
Cuvelier, C, Cabaraux, JF, Dufrasne, I, Clinquart, A, Hocquette, JF, Istasse, L and Hornick, JL 2006. Performance, slaughter characteristics and meat quality of young bulls from Belgian Blue, Limousin and Aberdeen Angus breeds fattened with a sugar-beet pulp or a cereal-based diet. Animal Science 82, 125132.Google Scholar
Ding, X, Zhang, X, Yang, Y, Ding, Y, Xue, W, Meng, Y, Zhu, W and Yin, Z 2014. Polymorphism, expression of natural resistance-associated macrophage protein 1 encoding gene (NRAMP1) and its association with immune traits in pigs. Asian-Australasian Journal of Animal Sciences 27, 11891195.Google Scholar
Ellenberger, MA, Johnson, DE, Carstens, GE, Hossner, KL, Holland, MD, Nett, TM and Nockels, CF 1989. Endocrine and metabolic changes during altered growth rates in beef cattle. Journal of Animal Science 67, 14461454.Google Scholar
Fielding, RA, Manfredi, TJ, Ding, W, Fiatarone, MA, Evans, WJ and Cannon, JG 1993. Acute phase response in exercise. III. Neutrophil and IL-1 beta accumulation in keletal muscle. The American Journal of Physiology 265, R166R172.Google Scholar
Fry, CS, Lee, JD, Jackson, JR, Kirby, TJ, Stasko, SA, Liu, H, Dupont-Versteegden, EE, Mccarthy, JJ and Peterson, CA 2014. Regulation of the muscle fiber microenvironment by activated satellite cells during hypertrophy. The FASEB Journal 28, 16541665.Google Scholar
Garred, P, Honoré, C, Ma, YJ, Munthe-fog, L and Hummelshoj, T 2009. MBL2, FCN1, FCN2 and FCN3: the genes behind the initiation of the lectin pathway of complement. Molecular Immunology 46, 27372744.Google Scholar
Huang, DW, Sherman, BT and Lempicki, RA 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4, 4457.Google Scholar
Ihn, H and Tamaki, K 2000. Oncostatin M stimulates the growth of dermal fibroblasts via a mitogen-activated protein kinase-dependent pathway. J Immunol 165, 21492155.Google Scholar
Jackman, RW and Kandarian, SC 2004. The molecular basis of skeletal muscle atrophy. American Journal of Physiology – Cell Physiology 287, C834C843.Google Scholar
Jensen, ML, Honore, C, Hummelshoj, T, Hansen, BE, Madsen, HO and Garred, P 2007. Ficolin-2 recognizes DNA and participates in the clearance of dying host cells. Molecular Immunology 44, 856865.Google Scholar
Krishnan, K, Steptoe, AL, Martin, HC, Wani, S, Nones, K, Waddell, N, Mariasegaram, M, Simpson, PT, Lakhani, SR, Gabrielli, B, Vlassov, A, Cloonan, N and Grimmond, SM 2013. MicroRNA-182-5p targets a network of genes involved in DNA repair. RNA 19, 230242.Google Scholar
Kumanogoh, A, Shikina, T, Suzuki, K, Uematsu, S, Yukawa, K, Kashiwamura, S, Tsutsui, H, Yamamoto, M, Takamatsu, H, Komitamura, EP, Takegahara, N, Marukawa, S, Ishida, I, Morishita, H, Prasad, DV, Tamura, M, Mizui, M, Toyofuku, T, Akira, S, Takeda, K, Okabe, M and Kikutani, H 2005. Non redundant roles of Sema4A in the immune system: defective T cell priming and Th1/Th2 regulation in Sema4A-deficient mice. Immunity 22, 305316.Google Scholar
Langmead, B, Trapnell, C, Pop, M and Salzberg, Sl 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10, 125.Google Scholar
Lee, SH, Engle, TE and Hossner, KL 2002. Effects of dietary copper on the expression of lipogenic genes and metabolic hormones in steers. Journal of Animal Science 80, 19992005.Google Scholar
Lee, HG, Hidari, H, Kang, SK, Hong, ZS, Xu, CX, Kim, SH, Seo, KS, Yoon, DH and Choi, YJ 2005. The relationships between plasma insulin-like growth factor (IGF)-1 and IGF-binding proteins (IGFBPs) to growth pattern, and characteristics of plasma IGFBPs in steers. Asian Australasian Journal of Animal Sciences, Gwanak-gu 18, 15751581.Google Scholar
Li, ZB, Kollias, HD and Wagner, KR 2008. Myostatin directly regulates skeletal muscle fibrosis. Journal of Biological Chemistry 283, 1937119378.Google Scholar
Love, MI, Huber, W and Anders, S 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15, 550571.Google Scholar
Mann, CJ, Perdiguero, E, Kharraz, Y, Aguilar, S, Pessina, P, Serrano, AL and Muñoz-Cánoves, P 2011. Aberrant repair and fibrosis development in skeletal muscle. Skeletal Muscle 1, 21.Google Scholar
Meda, C, Molla, F, Pizzol, M, Regano, D, Maione, F, Capano, S, Locati, M, Mantovani, A, Latini, R, Bussolino, F and Giraudo, E 2012. Semaphorin 4A exerts a proangiogenic effect by enhancing vascular endothelial growth factor – a expression in macrophages. The Journal of Immunology 188, 40814092.Google Scholar
Murphy, MM, Lawson, JA, Mathew, SJ, Hutcheson, DA and Kardon, G 2011. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138, 36253637.Google Scholar
Rios, R, Carneiro, I, Arce, VM and Devesa, J 2002. Myostatin is an inhibitor of myogenic differentiation. American Journal of Physiology – Cell Physiology 282, C993C999.Google Scholar
Rodgers, BD and Garikipati, DK 2008. Clinical, agricultural, and evolutionary biology of myostatin: a comparative review. Endocrine Reviews 29, 513534.Google Scholar
Roth, L, Koncina, E, Satkauskas, S, Crémel, G, Aunis, D and Bagnard, D 2009. The many faces of semaphorins: from development to pathology. Cellular and Molecular Life Sciences 66, 649666.Google Scholar
Sachdeva, M, Jeffrey, KM, Lee, CL, Zhang, M, Li, Z, Dodd, RD, Cason, D, Luo, L, Ma, Y, Mater, DY, Gladdy, R, Lev, DC, Cardona, DM and Kirsch, DG 2014. MicroRNA-182 drives metastasis of primary sarcomas by targeting multiple genes. The Journal of Clinical Investigation 124, 43054319.Google Scholar
Song, E, Ouyang, N, Horbelt, M, Antus, B, Wang, M and Exton, MS 2000. Influence of alternatively and classically activated macrophages on fibrogenic activities of human fibroblasts. Cellular Immunology 204, 1928.Google Scholar
Trapnell, C, Pachter, L and Salzberg, SL 2009. TopHat: discovering splice junctions with RNA-seq. Bioinformatics 25, 11051111.Google Scholar
Tripathi, G, Salih, DAM, Drozd, AC, Cosgrove, RA, Cobb, LJ and Pell, JM 2009. IGF-independent effects of insulin-like growth factor binding protein-5 (Igfbp5) in vivo. The FASEB Journal 23, 26162626.Google Scholar
Tu, HJ, Lin, TH, Chiu, YC, Tang, CH, Yang, RS and Fu, WM 2013. Enhancement of placenta growth factor expression by Oncostatin m in human rheumatoid arthritis synovial fibroblasts. Journal of Cellular Physiology 228, 983990.Google Scholar
Viita, H, Markkanen, J, Eriksson, E, Nurminen, M, Kinnunen, K, Babu, M, Heikura, T, Turpeinen, S, Laidinen, S, Takalo, T and Ylä-Herttuala, S 2008. 5-lipoxygenase-1 prevents vascular endothelial growth factor A- and placental growth factor-induced angiogenic effects in rabbit skeletal muscles via reduction in growth factor mRNA levels, NO bioactivity, and downregulation of VEGF receptor 2 expression. Circulation Research 102, 177184.Google Scholar
Xi, G, Kamanga-Sollo, E, Hathaway, MR, Dayton, WR and White, ME 2006. Effect of constitutive expression of porcine IGFBP-3 on proliferation and differentiation of L6 myogenic cells. Domestic Animal Endocrinology 31, 3551.Google Scholar
Zhu, J, Li, Y, Shen, W, Qiao, C, Ambrosio, F, Lavasani, M, Nozaki, M, Branca, MF and Huard, J 2007. Relationships between Transforming Growth Factor-β 1, Myostatin, and Decorin: implications for skeletal muscle fibrosis. The Journal of Biological Chemistry 282, 2585225863.Google Scholar