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Myostatin inactivation induces a similar muscle molecular signature in double-muscled cattle as in mice

Published online by Cambridge University Press:  01 October 2010

I. Chelh ,
B. Picard ,
J-F. Hocquette  and
I. Cassar-Malek
I. Chelh
Affiliation:
INRA, UR1213, Unité de Recherches sur les Herbivores, Equipe Croissance et Métabolisme du Muscle, Centre Clermont-Ferrand/Theix, 63122 Saint-Genès-Champanelle, France
B. Picard
Affiliation:
INRA, UR1213, Unité de Recherches sur les Herbivores, Equipe Croissance et Métabolisme du Muscle, Centre Clermont-Ferrand/Theix, 63122 Saint-Genès-Champanelle, France
J-F. Hocquette
Affiliation:
INRA, UR1213, Unité de Recherches sur les Herbivores, Equipe Croissance et Métabolisme du Muscle, Centre Clermont-Ferrand/Theix, 63122 Saint-Genès-Champanelle, France
I. Cassar-Malek*
Affiliation:
INRA, UR1213, Unité de Recherches sur les Herbivores, Equipe Croissance et Métabolisme du Muscle, Centre Clermont-Ferrand/Theix, 63122 Saint-Genès-Champanelle, France
*
†isabelle.cassar-malek@clermont.inra.fr
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Abstract

Myostatin (MSTN), a member of the TGF-β superfamily, is a negative regulator of skeletal muscle mass. We have previously shown that the cell survival/apoptosis pathway is a downstream target of MSTN loss-of-function in mice through the regulation of the expression or abundance of many survival and apoptotic factors. In this study, we used western-blot and quantitative PCR (qPCR) analyses to validate these novel downstream targets of MSTN in double-muscled (DM) cattle v. their controls including 260-day-old foetuses and adult cows from the INRA95 strain. MSTN loss-of-function in DM foetuses and DM cows resulted in a glycolytic shift of the muscles (e.g. upregulation of H-MyBP, PGM1 and SNTA1 and downregulation of H-FABP), activation of cell survival pathway through regulation of some components of the PI3K/Akt pathway (e.g. upregulation of DJ-1 and Gsk-3βser9/Gsk-3βtotal ratio and downregulation of PTEN) and upregulation of cell survival factors translationally controlled tumour protein (14-3-3E, Pink1). We also found a lower abundance of pro-apoptotic transcripts and/or proteins (Caspase-3, caspase-8, caspase-9, BID, ID2 and Daxx) and a higher expression of anti-apoptotic transcripts (Traf2 and Bcl2l2) in DM muscles. All together, these results are in favour of activation of the cell survival pathway and loss of apoptosis pathway within the muscles of DM animals. Alteration of both pathways may increase myonuclear or satellite cell survival, which is crucial for protein synthesis. This could contribute to muscle hypertrophy in DM foetuses and DM cows.

Keywords

myostatincattlemuscle hypertrophyapoptosiscell survival
Type
Full Paper
Information
animal , Volume 5 , Issue 2 , February 2011 , pp. 278 - 286
Copyright
Copyright © The Animal Consortium 2010

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References

Alway, SE, Martyn, JK, Ouyang, J, Chaudhrai, A, Murlasits, ZS 2003. Id2 expression during apoptosis and satellite cell activation in unloaded and loaded quail skeletal muscles. American Journal of Physiology – Regulatory Integrative and Comparative Physiology 284, R540–R549.Google Scholar
Arch, RH, Gedrich, RW, Thompson, CB 1998. Tumor necrosis factor receptor-associated factors (TRAFs)-a family of adapter proteins that regulates life and death. Genes & Development 12, 2821–2830.CrossRefGoogle ScholarPubMed
Ashmore, C, Parker, W, Stokes, H, Doerr, L 1974. Comparative aspects of muscle fibre types in fetuses of the normal and double muscled cattle. Growth 38, 501–506.Google ScholarPubMed
Bennett, P, Craig, R, Starr, R, Offer, G 1986. The ultrastructural location of C-protein, X-protein and H-protein in rabbit muscle. Journal of Muscle Research and Cell Motility 7, 550–567.CrossRefGoogle ScholarPubMed
Bommer, UA, Thiele, BJ 2004. The translationally controlled tumour protein (TCTP). The International Journal of Biochemistry & Cell Biology 36, 379–385.Google Scholar
Bouley, J, Meunier, B, Chambon, C, De Smet, S, Hocquette, JF, Picard, B 2005. Proteomic analysis of bovine skeletal muscle hypertrophy. Proteomics 5, 490–500.CrossRefGoogle ScholarPubMed
Cassar-Malek, I, Passelaigue, F, Bernard, C, Leger, J, Hocquette, J-F 2007. Target genes of myostatin loss-of-function in muscles of late bovine fetuses. BMC Genomics 8, 63.CrossRefGoogle ScholarPubMed
Chang, F, Lee, JT, Navolanic, PM, Steelman, LS, Shelton, JG, Blalock, WL, Franklin, RA, McCubrey, JA 2003. Involvement of PI3K//Akt pathway in cell cycle progression, apoptosis, and neoplastic transformation: a target for cancer chemotherapy. Leukemia 17, 590–603.Google Scholar
Chang, HY, Nishitoh, H, Yang, X, Ichijo, H, Baltimore, D 1998. Activation of apoptosis signal-regulating kinase 1 (ASK1) by the adapter protein Daxx. Science 281, 1860–1863.CrossRefGoogle ScholarPubMed
Chelh, I, Meunier, B, Picard, B, Reecy, JM, Hocquette, J-F, Cassar-Malek, I 2009a. Apoptosis is a target of myostatin loss-of-function in mice. American Journal of Physiology – Cell Physiology (submitted).Google Scholar
Chelh, I, Meunier, B, Picard, B, Reecy, JM, Chevalier, C, Hocquette, J-F, Cassar-Malek, I 2009b. Molecular profiles of quadriceps muscle in myostatin-null mice reveal PI3K and apoptotic pathways as myostatin targets. BMC Genomics 10, 196.CrossRefGoogle ScholarPubMed
Denisov, AY, Madiraju, MSR, Chen, G, Khadir, A, Beauparlant, P, Attardo, G, Shore, GC, Gehring, K 2003. Solution structure of human BCL-w: modulation of ligand binding by the C-terminal helix. Journal of Biological Chemistry 278, 21124–21128.CrossRefGoogle ScholarPubMed
Deveaux, V, Cassar-Malek, I, Picard, P 2001. Comparison of contractile characteristics of muscle from Holstein and double-muscled Belgian Blue foetuses. Comparative Biochemistry and Physiology 131, 21–29.CrossRefGoogle ScholarPubMed
Deveaux, V, Picard, B, Bouley, J, Cassar-Malek, I 2003. Location of myostatin expression during bovine myogenesis in vivo and in vitro. Reproduction Nutrition Development 43, 527–542.CrossRefGoogle ScholarPubMed
Gagnière, H, Picard, B, Jurie, C, Geay, Y 1997. Comparative study of metabolic differentiation of foetal muscle in normal and double-muscled cattle. Meat Science 45, 145–152.CrossRefGoogle ScholarPubMed
Gagnière, H, Ménissier, F, Geay, Y, Picard, B 2000. Influence of genotype on contractile protein differentiation in different bovine muscles during foetal life. Annales de Zootechnie 49, 405–423.Google Scholar
Gao, Y, Ordas, R, Klein, JD, Price, SR 2008. Regulation of caspase-3 activity by insulin in skeletal muscle cells involves both PI3-kinase and MEK-1/2. Journal of Applied Physiology 105, 1772–1778.CrossRefGoogle ScholarPubMed
Georges, M, Grobet, L, Poncelet, D, Royo, LJ, Pirottin, D, Brouwers, B 1998. Positional candidate cloning of the bovine mh locus identifies an allelic series of mutations disrupting the myostatin function and causing double muscling in cattle. In: Quantitative genetic theory; selection theory and experiments; internationalisation of breeding programs; detection of quantitative trait loci; exploitation of quantitative trait loci; quantitative trait loci maps; transgenics; developmental genetics. Proceedings of the 6th World Congress on Genetics Applied to Livestock Production, Armidale, Australia 26, 195–202pp.Google Scholar
Gerrard, DE, Judge, MD 1993. Induction of myoblast proliferation in L6 myoblast cultures by fetal serum of double-muscled and normal cattle. Journal of Animal Science 71, 1464–1470.CrossRefGoogle ScholarPubMed
Glass, DJ 2003. Molecular mechanisms modulating muscle mass. Trends in Molecular Medicine 9, 344–350.CrossRefGoogle ScholarPubMed
Grimes, CA, Jope, RS 2001. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Progress in Neurobiology 65, 391–426.Google Scholar
Grobet, L, Martin, LJ, Poncelet, D, Pirottin, D, Brouwers, B, Riquet, J, Schoeberlein, A, Dunner, S, Menissier, F, Massabanda, J, Fries, R, Hanset, R, Georges, M 1997. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nature Genetics 17, 71–74.Google Scholar
Hocquette, JF, Ortigues-Marty, I, Pethick, D, Herpin, P, Fernandez, X 1998. Nutritional and hormonal regulation of energy metabolism in skeletal muscles of meat-producing animals. Livestock Production Science 56, 115–143.CrossRefGoogle Scholar
Izumiya, Y, Hopkins, T, Morris, C, Sato, K, Zeng, L, Viereck, J, Hamilton, JA, Ouchi, N, LeBrasseur, NK, Walsh, K 2008. Fast/glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metabolism 7, 159–172.Google Scholar
Joulia-Ekaza, D, Cabello, G 2006. Myostatin regulation of muscle development: molecular basis, natural mutations, physiopathological aspects. Experimental Cell Research 312, 2401–2414.Google Scholar
Kambadur, R, Sharma, M, Smith, TPL, Bass, JJ 1997. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and piedmontese cattle. Genome Research 7, 910–915.CrossRefGoogle ScholarPubMed
Kaul, SC, Deocaris, CC, Wadhwa, R 2007. Three faces of mortalin: a housekeeper, guardian and killer. Experimental Gerontology 42, 263–274.CrossRefGoogle ScholarPubMed
Kim, RH, Peters, M, Jang, Y, Shi, W, Pintilie, M, Fletcher, GC, DeLuca, C, Liepa, J, Zhou, L, Snow, B, Binari, RC, Manoukian, AS, Bray, MR, Liu, FF, Tsao, M-S, Mak, TW 2005. DJ-1, a novel regulator of the tumor suppressor PTEN. Cancer Cell 7, 263–273.CrossRefGoogle ScholarPubMed
Lee, SJ 2004. Regulation of muscle mass by myostatin. Annual Review of Cell and Developmental Biology 20, 61–86.CrossRefGoogle ScholarPubMed
Laemmli, UK 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.CrossRefGoogle ScholarPubMed
Lenth, RV 2007. Statistical power calculations. Journal of Animal Science 85, E24–E29.CrossRefGoogle ScholarPubMed
Lev, N, Roncevich, D, Ickowicz, D, Melamed, E, Offen, D 2006. Role of DJ-1 in Parkinson’s disease. Journal of Molecular Neuroscience 29, 215–225.CrossRefGoogle ScholarPubMed
Li, H, Zhu, H, Xu, CJ, Yuan, J 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the fas pathway of apoptosis. Cell 94, 491–501.Google Scholar
Lin, J, Adam, RM, Santiestevan, E, Freeman, MR 1999. The phosphatidylinositol 3’-kinase pathway is a dominant growth factor-activated cell survival pathway in LNCaP human prostate carcinoma cells. Cancer Research 59, 2891–2897.Google ScholarPubMed
Martyn, JK, Bass, JJ, Oldham, JM 2004. Skeletal muscle development in normal and double-muscled cattle. The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology 281A, 1363–1371.CrossRefGoogle Scholar
McPherron, AC, Lee, SJ 1997. Double muscling in cattle due to mutations in the myostatin gene. Proceedings of the National Academy of Sciences 94, 12457–12461.CrossRefGoogle ScholarPubMed
McPherron, AC, Lawler, AM, Lee, SJ 1997a. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387, 83–90.CrossRefGoogle ScholarPubMed
McPherron, AC, Lawler, AM, Lee, SJ 1997b. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387, 83–90.Google Scholar
Ouali, A, Herrera-Mendez, CH, Coulis, G, Becila, S, Boudjellal, A, Aubry, L, Sentandreu, MA 2006. Revisiting the conversion of muscle into meat and the underlying mechanisms. Meat Science 74, 44–58.CrossRefGoogle ScholarPubMed
Pallafacchina, G, Calabria, E, Serrano, AL, Kalhovde, JM, Schiaffino, S 2002. A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proceedings of the National Academy of Sciences of the United States of America 99, 9213–9218.Google Scholar
Picard, B, Depreux, F, Geay, Y 1998. Muscle differentiation of normal and double-muscled bovine foetal myoblasts in primary culture. Basic and Applied Myology 8, 197–198.Google Scholar
Picard, B, Gagnière, H, Robelin, J, Geay, Y 1995. Comparison of the foetal development of muscle in normal and double-muscled cattle. Journal of Muscle Research and Cell Motility 16, 629–639.Google Scholar
Porter, GW, Khuri, FR, Fu, H 2006. Dynamic 14-3-3/client protein interactions integrate survival and apoptotic pathways. Seminars in Cancer Biology 16, 193–202.Google Scholar
Ross, AJ, Waymire, KG, Moss, JE, Parlow, AF, Skinner, MK, Russell, LD, MacGregor, GR 1998. Testicular degeneration in Bclw-deficient mice. Nature Genetics 18, 251–256.Google Scholar
Stambolic, V, Woodgett, JR 1994. Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochemical Journal 303, 701–704.CrossRefGoogle ScholarPubMed
Swatland, HJ, Kieffer, NM 1974. Fetal development of the double muscled condition in cattle. Journal of Animal Science 38, 752–757.CrossRefGoogle ScholarPubMed
Tang, B, Xiong, H, Sun, P, Zhang, Y, Wang, D, Hu, Z, Zhu, Z, Ma, H, Pan, Q, Xia, J-h, Xia, K, Zhang, Z 2006. Association of PINK1 and DJ-1 confers digenic inheritance of early-onset Parkinson’s disease. Human Molecular Genetics 15, 1816–1825.Google Scholar
Thomas, M, Langley, B, Berry, C, Sharma, M, Kirk, S, Bass, J, Kambadur, R 2000. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. Journal of Biological Chemistry 275, 40235–40243.CrossRefGoogle ScholarPubMed
Timothy, KM, Antonio, G 1998. TRAF2 expression in differentiated muscle. Journal of Cellular Biochemistry 71, 461–466.Google Scholar
Uytterhaegen, L, Claeys, E, Demeyer, D 1994. Effects of exogenous protease effectors on beef tenderness development and myofibrillar degradation and solubility. Journal of Animal Science 72, 1209–1223.CrossRefGoogle ScholarPubMed
Vandebrouck, A, Sabourin, J, Rivet, J, Balghi, H, Sebille, S, Kitzis, A, Raymond, G, Cognard, C, Bourmeyster, N, Constantin, B 2007. Regulation of capacitative calcium entries by {alpha}1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of {alpha}1-syntrophin. FASEB Journal 21, 608–617.Google Scholar
Wegner, J, Albrecht, E, Fiedler, I, Teuscher, F, Papstein, HJ, Ender, K 2000. Growth- and breed-related changes of muscle fiber characteristics in cattle. Journal of Animal Science 78, 1485–1496.CrossRefGoogle ScholarPubMed
Wong, ML, Medrano, JF 2005. Real-time PCR for mRNA quantitation. BioTechniques 39, 75–85.CrossRefGoogle ScholarPubMed
Yang, X, Khosravi-Far, R, Chang, HY, Baltimore, D 1997. Daxx, a Novel fas-binding protein that activates JNK and apoptosis. Cell 89, 1067–1076.CrossRefGoogle ScholarPubMed
Yeh, W-C, Shahinian, A, Speiser, D, Kraunus, J, Billia, F, Wakeham, A, de la Pompa, JL, Ferrick, D, Hum, B, Iscove, N, Ohashi, P, Rothe, M, Goeddel, DV, Mak, TW 1997. Early lethality, functional NF-[kappa]B activation, and increased sensitivity to TNF-induced cell death in TRAF2-deficient mice. Immunity 7, 715–725.CrossRefGoogle Scholar
Zhang, L, Blackwell, K, Thomas, GS, Sun, S, Yeh, W-C, Habelhah, H 2009. TRAF2 suppresses basal IKK activity in resting cells and TNF[alpha] can activate IKK in TRAF2 and TRAF5 double knockout cells. Journal of Molecular Biology 389, 495–510.Google Scholar