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A sensitised mutagenesis screen in the mouse to explore the bovine genome: study of muscle characteristics

Published online by Cambridge University Press:  10 December 2010

L. Magnol ,
O. Monestier ,
K. Vuillier-Devillers ,
S. Wagner ,
O. Cocquempot ,
M. C. Chevallier  and
V. Blanquet
L. Magnol
Affiliation:
UMR1061-INRA, Unité de Génétique Moléculaire Animale, Université de Limoges, 87060 Limoges, France
O. Monestier
Affiliation:
UMR1061-INRA, Unité de Génétique Moléculaire Animale, Université de Limoges, 87060 Limoges, France
K. Vuillier-Devillers
Affiliation:
UMR1061-INRA, Unité de Génétique Moléculaire Animale, Université de Limoges, 87060 Limoges, France
S. Wagner
Affiliation:
Helmholtz Zentrum München, German Research Center for Environmental Health, Institute of Experimental Genetics, 85764 Neuherberg/Munich, Germany
O. Cocquempot
Affiliation:
UMR1061-INRA, Unité de Génétique Moléculaire Animale, Université de Limoges, 87060 Limoges, France
M. C. Chevallier
Affiliation:
UMR1061-INRA, Unité de Génétique Moléculaire Animale, Université de Limoges, 87060 Limoges, France
V. Blanquet*
Affiliation:
UMR1061-INRA, Unité de Génétique Moléculaire Animale, Université de Limoges, 87060 Limoges, France
*
†E-mail: veronique.blanquet@unilim.fr
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Abstract

Meat yield and quality are closely related to muscle development. The muscle characteristics mainly take place during embryonic and postnatal phases. Thus, genetic control of muscle development in early stages represents a significant stake to improve product quality and production efficiency. In bovine, several programmes have been developed to detect quantitative trait loci (QTL) affecting growth, carcass composition or meat quality traits. Such strategy is incontestably very powerful yet extremely cumbersome and costly when dealing with large animals such as ruminants. Furthermore, the fine mapping of the QTL remains a real challenge. Here, we proposed an alternative approach based on chemical mutagenesis in the mouse combined with comparative genomics to identify regions or genes controlling muscle development in cattle. At present, we isolated seven independent mouse lines of high interest. Two lines exhibit a hypermuscular phenotype, and the other five show various skeletomuscular phenotypes. Detailed characterisation of these mouse mutants will give crucial input for the identification and the mapping of genes that control muscular development. Our strategy will provide the opportunity to understand the function and control of genes involved in improvement of animal physiology.

Keywords

animal modelsmutagenesismyostatinmuscle developmentcattle
Type
Full Paper
Information
animal , Volume 5 , Issue 5 , 04 April 2011 , pp. 663 - 671
Copyright
Copyright © The Animal Consortium 2010

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References

Abe, T, Saburi, J, Hasebe, H, Nakagawa, T, Kawamura, T, Saito, K, Nade, T, Misumi, S, Okumura, T, Kuchida, K, Hayashi, T, Nakane, S, Mitsuhasi, T, Nirasawa, K, Sugimoto, Y, Kobayashi, E 2008. Bovine quantitative trait loci analysis for growth, carcass, and meat quality traits in an F2 population from a cross between Japanese Black and Limousin. Journal of Animal Sciences 86, 2821–2832.CrossRefGoogle Scholar
Artaza, JN, Bhasin, S, Magee, TR, Reisz-Porszasz, S, Shen, R, Groome, NP, Meerasahib, MF, Gonzalez-Cadavid, NF 2005. Myostatin inhibits myogenesis and promotes adipogenesis in C3H10T(1/2) mesenchymal multipotent cells. Endocrinology 146, 3547–3557.CrossRefGoogle Scholar
Arthur, PF 1995. Double muscling in cattle: a review. Australian Journal of Comment: agricultural research 46, 1493–1515.Google Scholar
Bach, EA, Vincent, S, Zeidler, MP, Perrimon, N 2003. A sensitized genetic screen to identify novel regulators and components of the Drosophila Janus Kinase/signal transducer and activator of transcription pathway. Genetics 165, 1149–1166.CrossRefGoogle ScholarPubMed
Bellinge, RH, Liberles, DA, Iaschi, SP, O'brien, PA, Tay, GK 2005. Myostatin and its implications on animal breeding: a review. Animal Genetics 36, 1–6.CrossRefGoogle ScholarPubMed
Besson, V, Nalesso, V, Herpin, A, Bizot, JC, Messaddeq, N, Romand, R, Puech, A, Blanquet, V, Herault, Y 2005. Training and aging modulate the loss-of-balance phenotype observed in a new ENU-induced allele of Otopetrin1. Biology of Cell 97, 787–798.CrossRefGoogle Scholar
Boichard, D, Grohs, C, Bourgeois, F, Cerqueira, F, Faugeras, R, Neau, A, Rupp, R, Amigues, Y, Boscher, MY, Leveziel, H 2003. Detection of genes influencing economic traits in three French dairy cattle breeds. Genetics Selection Evolution 35, 77–101.CrossRefGoogle ScholarPubMed
Brown, SD, Chambon, P, de Angelis, MH 2005. EMPReSS: standardized phenotype screens for functional annotation of the mouse genome. Nature Genetics 37, 1155.Google ScholarPubMed
Buac, K, Watkins-Chow, DE, Loftus, SK, Larson, DM, Incao, A, Gibney, G, Pavan, WJ 2008. A Sox10 expression screen identifies an amino acid essential for Erbb3 function. PLoS Genetics 4, e1000177.CrossRefGoogle ScholarPubMed
Carpinelli, MR, Hilton, DJ, Metcalf, D, Antonchuk, JL, Hyland, CD, Mifsud, SL, Di Rago, L, Hilton, AA, Willson, TA, Roberts, AW, Ramsay, RG, Nicola, NA, Alexander, WS 2004. Suppressor screen in Mpl-/- mice: c-Myb mutation causes supraphysiological production of platelets in the absence of thrombopoietin signalling. Proceedings of the National Academy of Sciences USA 101, 6553–6558.CrossRefGoogle Scholar
Clark, AT, Goldowitz, D, Takahashi, JS, Vitaterna, MH, Siepka, SM, Peters, LL, Frankel, WN, Carlson, GA, Rossant, J, Nadeau, JH, Justice, MJ 2004. Implementing large-scale ENU mutagenesis screens in North America. Genetica 122, 51–64.CrossRefGoogle ScholarPubMed
Cordes, SP 2005. N-ethyl-N-nitrosourea mutagenesis: boarding the mouse mutant express. Microbiology and Molecular Biology Reviews 69, 426–439.CrossRefGoogle ScholarPubMed
Drögemüller, C, Distl, O, Leeb, T 2001. Partial deletion of the bovine ED1 gene causes anhidrotic ectodermal dysplasia in cattle. Genome Research 11, 1699–1705.CrossRefGoogle ScholarPubMed
Duchesne, A, Gautier, M, Chadi, S, Grohs, C, Floriot, S, Gallard, Y, Caste, G, Ducos, A, Eggen, A 2006. Identification of a doublet missense substitution in the bovine LRP4 gene as a candidate causal mutation for syndactyly in Holstein cattle. Genomics 88, 610–621.CrossRefGoogle ScholarPubMed
Elkasrawy, MN, Hamrick, MW 2010. Myostatin (GDF-8) as a key factor linking muscle mass and bone structure. Journal of Musculoskeletal and Neuronal Interactions 10, 56–63.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Grobet, L, Poncelet, D, Royo, LJ, Brouwers, B, Pirottin, D, Michaux, C, Menissier, F, Zanotti, M, Dunner, S, Georges, M 1998. Molecular definition of an allelic series of mutations disrupting the myostatin function and causing double-muscling in cattle. Mammalian Genome 9, 210–213.CrossRefGoogle ScholarPubMed
Grobet, L, Pirottin, D, Farnir, F, Poncelet, D, Royo, LJ, Brouwers, B, Christians, E, Desmecht, D, Coignoul, F, Kahn, R, Georges, M 2003. Modulating skeletal muscle mass by postnatal, muscle-specific inactivation of the myostatin gene. Genesis 35, 227–238.CrossRefGoogle ScholarPubMed
Guenet, JL 2004. Chemical mutagenesis of the mouse genome: an overview. Genetica 122, 9–24.CrossRefGoogle ScholarPubMed
Guo, W, Flanagan, J, Jasuja, R, Kirkland, J, Jiang, L, Bhasin, S 2008. The effects of myostatin on adipogenic differentiation of human bone marrow-derived mesenchymal stem cells are mediated through cross-communication between Smad3 and Wnt/beta-catenin signalling pathways. Journal of Biological Chemistry 283, 9136–9145.CrossRefGoogle Scholar
Hamrick, MW, Shi, X, Zhang, W, Pennington, C, Thakore, H, Haque, M, Kang, B, Isales, CM, Fulzele, S, Wenger, KH 2007. Loss of myostatin (GDF8) function increases osteogenic differentiation of bone marrow-derived mesenchymal stem cells but the osteogenic effect is ablated with unloading. Bone 40, 1544–1553.CrossRefGoogle ScholarPubMed
Karim, FD, Chang, HC, Therrien, M, Wassarman, DA, Laverty, T, Rubin, GM 1996. A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetics 143, 315–329.CrossRefGoogle ScholarPubMed
Kellum, E, Starr, H, Arounleut, P, Immel, D, Fulzele, S, Wenger, K, Hamrick, MW 2009. Myostatin (GDF-8) deficiency increases fracture callus size, Sox-5 expression, and callus bone volume. Bone 44, 17–23.CrossRefGoogle ScholarPubMed
Kunieda, T, Ide, H, Nakagiri, M, Yoneda, K, Konfortov, B, Ogawa, H 2000. Localization of the locus responsible for Chediak–Higashi syndrome in cattle to bovine chromosome. Animal Genetics 31, 87–90.CrossRefGoogle ScholarPubMed
Loo, S, Laurenson, P, Foss, M, Dillin, A, Rine, J 1995. Roles of ABF1, NPL3, and YCL54 in silencing in Saccharomyces cerevisiae. Genetics 141, 889–902.CrossRefGoogle ScholarPubMed
McPherron, AC, Lee, SJ 1997. Double muscling in cattle due to mutations in the myostatin gene. Proceedings of the National Academy of Sciences USA 94, 12457–12461.CrossRefGoogle ScholarPubMed
McPherron, AC, Lawler, AM, Lee, SJ 1997. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387, 83–90.CrossRefGoogle ScholarPubMed
Raftery, LA, Twombly, V, Wharton, K, Gelbart, WM 1995. Genetic screens to identify elements of the decapentaplegic signalling pathway in Drosophila. Genetics 139, 241–254.CrossRefGoogle ScholarPubMed
Rebbapragada, A, Benchabane, H, Wrana, JL, Celeste, AJ, Attisano, L 2003. Myostatin signals through a transforming growth factor beta-like signalling pathway to block adipogenesis. Molecular and Cellular Biology 23, 7230–7242.CrossRefGoogle ScholarPubMed
Rogers, DC, Fisher, EM, Brown, SD, Peters, J, Hunter, AJ, Martin, JE 1997. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mammalian Genome 8, 711–713.CrossRefGoogle ScholarPubMed
Rubio-Aliaga, I, Soewarto, D, Wagner, S, Klaften, M, Fuchs, H, Kalaydjiev, S, Busch, DH, Klempt, M, Rathkolb, B, Wolf, E, Abe, K, Zeiser, S, Przemeck, GK, Beckers, J, de Angelis, MH 2007. A genetic screen for modifiers of the delta1-dependent notch signalling function in the mouse. Genetics 175, 1451–1463.CrossRefGoogle ScholarPubMed
Satterthwaite, AB, Willis, F, Kanchanastit, P, Fruman, D, Cantley, LC, Helgason, CD, Humphries, RK, Lowell, CA, Simon, M, Leitges, M, Tarakhovsky, A, Tedder, TF, Lesche, R, Wu, H, Witte, ON 2000. A sensitized genetic system for the analysis of murine B lymphocyte signal transduction pathways dependent on Bruton's tyrosine kinase. Proceedings of the National Academy of Sciences USA 97, 6687–6692.CrossRefGoogle ScholarPubMed
Simon, MA, Bowtell, DD, Dodson, GS, Laverty, TR, Rubin, GM 1991. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signalling by the sevenless protein tyrosine kinase. Cell 67, 701–716.CrossRefGoogle Scholar
Soewarto, D, Blanquet, V, de Angelis Hrabe, M 2003. Random ENU mutagenesis. Methods of Molecular Biology 209, 249–266.Google ScholarPubMed
Soewarto, D, Klaften, M, Rubio-Aliaga, I 2009. Features and strategies of ENU mouse mutagenesis. Current Pharmalogical Biotechnology 10, 198–213.CrossRefGoogle ScholarPubMed
Takeda, H, Takami, M, Oguni, T, Tsuji, T, Yoneda, K, Sato, H, Ihara, N, Itoh, T, Kata, SR, Mishina, Y, Womack, JE, Moritomo, Y, Sugimoto, Y, Kunieda, T 2002. Positional cloning of the gene LIMBIN responsible for bovine chondro-dysplastic dwarfism. Proceedings of the National Academy of Sciences USA 99, 10549–10554.CrossRefGoogle ScholarPubMed