Target genes of myostatin loss-of-function in muscles of late bovine fetuses
Tóm tắt
Myostatin, a muscle-specific member of the Transforming Growth Factor beta family, negatively regulates muscle development. Double-muscled (DM) cattle have a loss-of-function mutation in their myostatin gene responsible for the hypermuscular phenotype. Thus, these animals are a good model for understanding the mechanisms underpinning muscular hypertrophy. In order to identify individual genes or networks that may be myostatin targets, we looked for genes that were differentially expressed between DM and normal (NM) animals (n = 3 per group) in the semitendinosus muscle (hypertrophied in DM animals) at 260 days of fetal development (when the biochemical differentiation of muscle is intensive). A heterologous microarray (human and murine oligonucleotide sequences) of around 6,000 genes expressed in muscle was used. Many genes were found to be differentially expressed according to genetic type (some with a more than 5-fold change), and according to the presence of one or two functional myostatin allele(s). They belonged to various functional categories. The genes down-regulated in DM fetuses were mainly those encoding extracellular matrix proteins, slow contractile proteins and ribosomal proteins. The genes up-regulated in DM fetuses were mainly involved in the regulation of transcription, cell cycle/apoptosis, translation or DNA metabolism. These data highlight features indicating that DM muscle is shifted towards a more glycolytic metabolism, and has an altered extracellular matrix composition (e.g. down-regulation of COL1A1 and COL1A2, and up-regulation of COL4A2) and decreased adipocyte differentiation (down-regulation of C1QTNF3). The altered gene expression in the three major muscle compartments (fibers, connective tissue and intramuscular adipose tissue) is consistent with the well-known characteristics of DM cattle. In addition, novel potential targets of the myostatin gene were identified (MB, PLN, troponins, ZFHX1B). Thus, the myostatin loss-of-function mutation affected several physiological processes involved in the development and determination of the functional characteristics of muscle tissue.
Tài liệu tham khảo
McPherron AC, Lawler AM, Lee SJ: Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 1997, 387: 83-90. 10.1038/387083a0.
Kambadur R, Sharma M, Smith TP, Bass JJ: Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res. 1997, 7: 910-916.
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: A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet. 1997, 17: 71-74. 10.1038/ng0997-71.
Grobet L, Poncelet D, Royo L, Brouwers B, Pirottin D, Michaux C, Ménissier F, Zanotti M, Dunner S, Georges M: Molecular definition of an allelic series of mutations disrupting the myostatin function and causing double-muscling in cattle. Mamm Genome. 1998, 9: 210-213. 10.1007/s003359900727.
Holmes JH, Ashmore CR: A histochemical study of development of muscle fiber type and size in normal and "double muscled" cattle. Growth. 1972, 36: 351-372.
Swatland HJ, Kieffer NM: Fetal development of the double muscled condition in cattle. J Anim Sci. 1974, 38: 752-757.
Gagnière H, Ménissier F, Geay Y, Picard B: Influence of genotype on contractile protein differentiation in different bovine muscles during foetal life. Ann Zoot. 2000, 49: 1-19. 10.1051/animres:2000104.
Deveaux V, Cassar-Malek I, Picard P: Comparison of contractile characteristics of muscle from Holstein and Double-Muscled Belgian Blue foetuses. Comp Biochem Physiol. 2001, 131: 21-29. 10.1016/S1095-6433(01)00459-7.
Deveaux V, Picard B, Bouley J, Cassar-Malek I: Location of myostatin expression during bovine myogenesis in vivo and in vitro. Reprod Nutr Dev. 2003, 43: 527-542. 10.1051/rnd:2004003.
Bailey AJ, Enser MB, Dransfield E, Restall DJ, Avery NC: Muscle and adipose tissue from normal and double muscled cattle: collagen types, muscle fiber diameter, fat cell size and fatty acid composition and organoleptic properties. Muscle hypertrophy of genetic origin and its use to improve beef production. Edited by: King JWB, Ménissier F. 1982, The Hague: Martinus Nijhoff Publishers, 178-204.
Wagner KR: Muscle regeneration through myostatin inhibition. Curr Opin Rheumatol. 2005, 17: 720-724. 10.1097/01.bor.0000184163.61558.ca.
Joulia-Ekaza D, Cabello G: Myostatin regulation of muscle development: Molecular basis, natural mutations, physiological aspects. Exp Cell Res . 2006, 312: 2401-14. Erratum in: Exp Cell Res. 2006, 15;312:345
Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R: Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem. 2000, 275: 40235-40243. 10.1074/jbc.M004356200.
Picard B, Depreux F, Geay Y: Muscle differentiation of normal and double-muscled bovine foetal myoblasts in primary culture. Basic Appl Myol. 1998, 8: 197-203.
Ríos R, Carneiro C, Arce V, Devesa J: Myostatin is an inhibitor of myogenic differentiation. Am J Physiol Cell Physiol. 2002, 282: C993-C999.
Langley B, Thomas M, Bishop A, Sharma M, Gilmour S, Kambadur R: Myostatin Inhibits Myoblast Differentiation by Down-regulating MyoD Expression. J Biol Chem. 2002, 277: 49831-49840. 10.1074/jbc.M204291200.
Zhu X, Topouzis S, Liang LF, Stotish RL: Myostatin signaling through Smad2, Smad3 and Smad4 is regulated by the inhibitory Smad7 by a negative feedback mechanism. Cytokine. 2004, 26: 262-272. 10.1016/j.cyto.2004.03.007.
Philip B, Lu Z, Gao Y: Regulation of GDF-8 signaling by the p38 MAPK. Cell Signalling. 2005, 17: 365-375. 10.1016/j.cellsig.2004.08.003.
Joulia D, Bernardi H, Garandel V, Rabenoelina F, Vernus B, Cabello G: Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin. Exp Cell Res. 2003, 286: 263-275. 10.1016/S0014-4827(03)00074-0.
Bouley J, Meunier B, Chambon C, De Smet S, Hocquette JF, Picard B: Proteomic analysis of bovine skeletal muscle hypertrophy. Proteomics. 2005, 5: 490-500. 10.1002/pmic.200400925.
Sudre K, Leroux C, Piétu G, Cassar-Malek I, Petit E, Listrat A, Auffray C, Picard B, Martin P, Hocquette J-F: Transcriptome analysis of two bovine muscles during ontogenesis. J Biochem. 2003, 133: 745-756.23. 10.1093/jb/mvg096.
Picard B, Lefaucheur L, Berri C, Duclos MJ: Muscle fibre ontogenesis in farm animal species. Reprod Nutr Dev. 2002, 42: 415-431. 10.1051/rnd:2002035.
Everts-van der Wind A, Larkin DM, Green CA, Elliott JS, Olmstead CA, Chiu R, Schein JE, Marra MA, Womack JE, Lewin HA: A high-resolution whole-genome cattle-human comparative map reveals details of mammalian chromosome evolution. Proc Natl Acad Sci U S A. 2005, 102: 18526-18531. 10.1073/pnas.0509285102.
Casas E, Keele JW, Shackelford SD, Koohmaraie M, Sonstegard TS, Smith TP, Kappes SM, Stone RT: Association of the muscle hypertrophy locus with carcass traits in beef cattle. J Anim Sci. 1998, 76: 468-473.
Steelman CA, Recknor JC, Nettleton D, Reecy JM: Transcriptional profiling of myostatin-knockout mice implicates Wnt signaling in postnatal skeletal muscle growth and hypertrophy. FASEB J. 2006, 20: 580-582.
Potts JK, Echternkamp SE, Smith TP, Reecy JM: Characterization of gene expression in double-muscled and normal-muscled bovine embryos. Anim Genet. 2003, 34: 438-444. 10.1046/j.0268-9146.2003.01055.x.
Verrecchia F, Wagner EF, Mauviel A: Distinct involvement of the Jun-N-terminal kinase and NF-kappaB pathways in the repression of the human COL1A2 gene by TNF-alpha. EMBO Rep. 2002, 3: 1069-1074. 10.1093/embo-reports/kvf219.
Karasseva N, Tsika G, Ji J, Zhang A, Mao X, Tsika R: 1 binds multiple muscle MEF2 and A/T-rich elements during fast-to-slow skeletal muscle fiber type transitions. Mol Cell Biol. 2003, 23: factor5143-5164. 10.1128/MCB.23.15.5143-5164.2003.
Halestrap AP, Meredith D: The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflueg Arch Eur J Physiol. 2004, 447: 619-628. 10.1007/s00424-003-1067-2.
Girgenrath S, Song K, Whittemore L-A: Loss of myostatin expression alters fiber-type distribution and expression of myosine heavy chain isoforms in slow- and fast-type skeletal muscle. Muscle Nerve. 2005, 31: 34-40. 10.1002/mus.20175.
Ashmore C, Parker W, Stokes H, Doerr L: Comparative aspects of muscle fibre types in fetuses of the normal and double muscled cattle. Growth. 1974, 38: 501-506.
Goetsch SC, Hawke TJ, Gallardo TD, Richardson JA, Garry DJ: Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol Genomics. 2003, 14: 261-271.
Sanes JR: The basement membrane/basal lamina of skeletal muscle. J Biol Chem. 2003, 278: 12601-12604. 10.1074/jbc.R200027200.
Hanset R: The major gene of muscular hypertrophy in the Belgian Blue cattle breed. Breeding for disease resistance in farm animals. Edited by: JB Owen RFE. 1991, Axford eds. CAB International, 467-478.
Ménissier F: General survey of the effect of double muscling on cattle performance. Muscle hypertrophy of genetic origin and its use to improve beef production. Edited by: King JBW, Ménissier F. 1982, The Hague Martinus Nijhoff, 21-53.
Listrat A, Picard B, Geay Y: Age-related changes and location of type I, III, IV, V and VI collagens during development of four foetal skeletal muscles of double-muscled and normal bovine animals. Tissue Cell. 1999, 31: 17-27. 10.1054/tice.1998.0015.
Rautavuoma K, Takaluoma K, Sormunen R, Myllyharju J, Kivirikko KI, Soininen R: Premature aggregation of type IV collagen and early lethality in lysylhydroxylase 3 null mice. Proc Natl Acad Sci USA. 2004, 101: 14120-14125. 10.1073/pnas.0404966101.
Schaffler A, Ehling A, Neumann E, Herfarth H, Tarner I, Gay S, Scholmerich J, Muller-Ladner U: Genomic organization, chromosomal localization and adipocytic expression of the murine gene for CORS-26 (collagenous repeat-containing sequence of 26 kDa protein). Biochim Biophys Acta. 2003, 1628: 64-70.
Lin J, Arnold HB, Della-Fera MA, Azain MJ, Hartzell DL, Baile CA: Myostatin knockout in mice increases myogenesis and decreases adipogenesis. Biochem Biophys Res Commun. 2002, 291: 701-716. 10.1006/bbrc.2002.6500.
Artaza JN, Bhasin S, Magee TR, Reisz-Porszasz S, Shen R, Groome NP, Fareez MM, Gonzalez-Cadavid NF: Myostatin inhibits myogenesis and promotes adipogenesis in C3H 10T(1/2) mesenchymal multipotent cells. Endocrinology. 2005, 146: 3547-3557. 10.1210/en.2005-0362.
Barnola I, Hocquette J-F, Cassar-Malek I, Jurie C, Gentès G, Cabaraux JF, Cuvelier C, Istasse L, Dufrasne I: Adipocyte fatty acid-binding protein expression and mitochondrial activity as indicators of Intramuscular fat content in young bulls. Indicators of milk and beef quality. Edited by: Hocquette J-F, Gigli S. 2005, EAAP Publication 112. Wageningen, The Netherlands: Wageningen Academic Publishers, 419-424.
Cianzo DS, Topel DG, Whitehurst GB, Beitz DC, Self HL: Adipose tissue growth and cellularity: changes in bovine adipocyte and number. J Anim Sci. 1985, 60: 970-976.
Gagnière H, Picard B, Geay Y: Contractile differentiation of foetal cattle muscles: intermuscular variability. Reprod Nutr Dev. 1999, 39: 637-655.
Cardioserve, IFR 26 de Nantes. [http://cardioserve.nantes.inserm.fr/ptf-puce/myochips_en.php]
Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC, Gaasterland T, Glenisson P, Holstege FCP, Kim IF, Markowitz V, Matese JC, Parkinson H, Robinson A, Sarkans U, Schulze-Kremer S, Stewart J, Taylor R, Vilo J, Vingron M: Minimum information about a microarray experiment (MIAME) – toward standards for microarray data. Nature Genet. 2001, 29: 365-371. 10.1038/ng1201-365.
Entrez GEO profiles. [http://www.ncbi.nlm.nih.gov/geo/]
Le Meur N, Lamirault G, Bihouée A, Steenman M, Bédrine-Ferran H, Teusan R, Ramstein G, Léger JJ: A dynamic, web-accessible resource to process raw microarray scan data into consolidated gene expression values: importance of replication. Nucleic Acids Res. 2004, 32: 5349-5358. 10.1093/nar/gkh870.
Tusher VG, Tibshirani R, Chu G: Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci. 2001, 98: 5116-5120. 10.1073/pnas.091062498.
Didier G, Brezellec P, Remy E, Henaut A: GeneANOVA – gene expression analysis of variance. Bioinformatics. 2002, 18: 490-491. 10.1093/bioinformatics/18.3.490.
Sturn A, Quackenbush J, Trajanoski Z: Genesis: cluster analysis of microarray data. Bioinformatics. 2002, 18: 207-208. 10.1093/bioinformatics/18.1.207.
Babelomics. [http://babelomics.bioinfo.cipf.es/index.html]
Al-Shahrour F, Minguez P, Vaquerizas JM, Conde L, Dopazo J: Babelomics: a suite of web-tools for functional annotation and analysis of group of genes in high-throughput experiments. Nucleic Acids Res. 2005, 33 (Web Server issue): W460-W464. 10.1093/nar/gki456.
Genomatix Portal. [http://www.genomatix.de]