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Evolutional principles of homology in regulatory genes of myogenesis

  • Developmental Biology
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Abstract

Analysis of early steps in muscular system development of invertebrates and vertebrates shows that early steps of myogenesis are regulated by genes-orthologs mainly belonging to two families, Pax and bHLH. In the majority of the following organisms, muscles formation (steps of determination and the earliest steps of myogenesis) is regulated by genes orthologs Pax3 which belong to the family Pax: nematodes (Caenorhabditis elegans, Pristionchus pacificus), insects (Drosophila melanogaster), echinoderms (Strongylocentrotus purpuratus), sea squirts (Ciona intestinalis, Holocynthia roretzi), fishes (Danio rerio), amphibians (Xenopus laevis), birds, and mammals (mouse, rat). The nematode C. elegans is an exception since formation of its muscles in this period is regulated by homeobox gene Pal-1 belonging to the family Caudal. The sea squirt C. intestinalis is also an exception because the earliest steps of development involved in further muscle formation are accompanied by activation of the gene CiSna (snail) (gene family basic Zinc finger). The next steps of myogenesis in all analyzed species are regulated by genes orthologs belonging to the family of transcriptional factors bHLH. They along with genes Pax3 are characterized by a high extent of homology in all studied groups of animals.

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References

  • Baylies, M.K. and Bate, M., A Myogenic Switch in Drosophila, Science, 1996, vol. 272, pp. 1481–1484.

    Article  PubMed  CAS  Google Scholar 

  • Baylies, M., Bate, M., and Ruiz-Gomez, M., Myogenesis: A View from Drosophila, Cell, 1998, vol. 93, pp. 921–927.

    Article  PubMed  CAS  Google Scholar 

  • Baylies, M.K. and Michelson, A.M., Invertebrate Myogenesis: Looking Back to the Future of Muscle Development, Curr. Opin. Genet. Dev., 2001, vol. 11, pp. 431–439.

    Article  PubMed  CAS  Google Scholar 

  • Beach, D.L., Salmon, E.D., and Bloom, K., Localization and Anchoring of mRNA in Budding Yeast, Curr. Biol., 1999, vol. 9, pp. 569–578.

    Article  PubMed  CAS  Google Scholar 

  • Braun, T., Buschhausen, D.C., Bober, E., et al., A Novel Human Muscle Factor Related to but Distinct from MyoD1 Induces Myogenic Conversion in 10T1/2 Fibroblasts, EMBO J., 1989, vol. 8, pp. 701–709.

    PubMed  CAS  Google Scholar 

  • Braun, T., Bober, E., Winter, B., et al., Myf-6, a New Member of the Human Gene Family of Myogenic Determination Factors: Evidence for a Gene Cluster on Chromosome 12, EMBO J., 1990, vol. 9, pp. 821–831.

    PubMed  CAS  Google Scholar 

  • Bryson-Richardson, R.J., and Currie, P.D., The Genetics of Vertebrate Myogenesis, Nat. Rev. Gen, 2008, vol. 9, pp. 632–646.

    Article  CAS  Google Scholar 

  • Castanon, I., Von Stetina, S., and Kass, J., Dimerization Partners Determine the Activity of the Twist bHLH Protein during Drosophila Mesoderm Development, Development, 2001, vol. 128, pp. 3145–3159.

    PubMed  CAS  Google Scholar 

  • Chen, L., Krause, M., and Sepanski, M., The Caenorhabditis elegans MYOD Homologue HLH-1 Is Essential for Proper Muscle Function and Complete Morphogenesis, Development, 1994, vol. 120, pp. 1631–1641.

    PubMed  CAS  Google Scholar 

  • Daston, G., Lamar, E., Oliver, M., and Goulding, M., Pax-3 Necessary for Migration but not Differentiation of Limb Muscle Precursors in the Mouse, Development, 1996, vol. 122, pp. 1017–1027.

    PubMed  CAS  Google Scholar 

  • Davis, R.L., Weintraub, H., and Lassar, A.B., Expression of a Single Transfected cDNA Converts Fibroblasts to Myoblasts, Cell, 1987, vol. 51, pp. 987–1000.

    Article  PubMed  CAS  Google Scholar 

  • Devoto, S.H., Melanson, E., Eisen, J.S., et al., Identification of Separate Slow and Fast Muscle Precursor Cells in vivo, Prior to Somite Formation, Development, 1996, vol. 122, pp. 3371–3380.

    PubMed  CAS  Google Scholar 

  • Duan, H., Zhang, C., Chen, J., et al., A Key Role of Pox Meso in Somatic Myogenesis of Drosophila, Development, 2007, vol. 134, pp. 3985–3997.

    Article  PubMed  CAS  Google Scholar 

  • Dunin-Borkowski, O.M., Brown, N.H., and Bate, M., Anterior-Posterior Subdivision and the Diversification of the Mesoderm in Drosophila, Development, 1995, vol. 121, pp. 4183–4193.

    CAS  Google Scholar 

  • Edmonton, D.G. and Olson, E.N., A Gene with Homology to the Myc Similarity Region of MyoD1 Is Expressed during Myogenesis and Its Sufficient to Activate the Muscle Differentiation Program, Gen. Dev., 1989, vol. 3, pp. 628–640.

    Article  Google Scholar 

  • Erives, A., Corbo, J.C., and Levine, M., Lineage-Specific Regulation of the Ciona snail Gene in the Embryonic Mesoderm and Neuroectoderm, Dev. Biol., 1998, vol. 194, pp. 213–225.

    Article  PubMed  CAS  Google Scholar 

  • Feng, X., Adiarte, E.G., and Devoto, S.H., Hedgehog Acts Directly on the Zebrafish Dermomyotome to Promote Myogenic Differentiation, Dev. Biol., 2006, vol. 300, pp. 736–746.

    Article  PubMed  CAS  Google Scholar 

  • Fisher, M.E., Isaacs, H.V., and Pownall, M.E., eFGF Is Required for Activation of XMyoD Expression in the Myogenic Cell Lineage of Xenopus laevis, Development, 2002, vol. 129, pp. 1307–1315.

    PubMed  CAS  Google Scholar 

  • Frank, D. and Harland, R.M., Transient Expression of XMyoD in Non-Somitic Mesoderm of Xenopus gastrulae, Development, 1991, vol. 113, pp. 1387–1393.

    PubMed  CAS  Google Scholar 

  • Furlong, E.E.M., Anderson, E.C., Null, B., et al., Pattern of Gene Expression during Drosophila Mesoderm Development, Science, 2001, vol. 293, pp. 1629–1633.

    Article  PubMed  CAS  Google Scholar 

  • Gilbert, S.F., Biologiya razvitiya (Developmental Biology), St. Petersburg: Inform-Planeta, 2010.

    Google Scholar 

  • Hammond, C.L., Hinits, Y., Osborn, D.P., et al., Signals and Myogenic Regulatory Factors Restrict Pax3 and Pax7 Expression to Dermomyotome-Like Tissue in Zebrafish, Dev. Biol., 2007, vol. 302, pp. 504–521.

    Article  PubMed  CAS  Google Scholar 

  • Harvey, R.P., MyoD Protein Expression in Xenopus Embryos Closely Follows a Mesoderm Induction-Dependent Amplification of MyoD Transcription and Its Synchronous across the Future Somite Exit, Mech. Dev., 1992, vol. 37, pp. 141–147.

    Article  PubMed  CAS  Google Scholar 

  • Hollenberg, S.M., Cheng, P.F., and Weintraub, H., Use of a Conditional MyoD Transcription Factor in Studies of MyoD Trans-Activation and Muscle Determination, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, pp. 8028–8032.

    Article  PubMed  CAS  Google Scholar 

  • Korochkin, L.I., Biologiya individual’nogo razvitiya (Biology of Individual Development), Moscow: Izd-vo MGU, 2002.

    Google Scholar 

  • Krause, M., Fire, A., White-Harrison, S., et al., CeMyoD Accumulation Defines the Body Wall Muscle Cell Fate during C. elegans Embryogenesis, Cell, 1990, vol. 63, pp. 907–919.

    Article  PubMed  CAS  Google Scholar 

  • Lei, H., Lin, J., Fukushige, T., et al., Caudal PAL-1 Directly Activated the Body Wall Module Regulator hlh-1 in C. elegans to Initiate the Embryonic Muscle Gene Regulatory Network, Development, 2009, vol. 136, pp. 1241–1249.

    Article  PubMed  CAS  Google Scholar 

  • Maroto, M., Reshef, R., Munsterberg, A.E., et al., Ectopic Pax-3 Activates MyoD and Myf-5 Expression in Embryonic Mesoderm and Neural Tissue, Cell, 1997, vol. 89, pp. 139–148.

    Article  PubMed  CAS  Google Scholar 

  • Meedel, T.H., Lee, J.J., and Whittaker, J.R., Muscle Development and Lineage-Specific Expression of CiMDF, the MyoD-Family Gene of Ciona intestinalis, Dev. Biol., 2002, vol. 241, pp. 238–246.

    Article  PubMed  CAS  Google Scholar 

  • Mönsterberg, A.E. and Lassar, A.B., Combinatorial Signals from the Neural Tube, Floor Plate and Notochord Induce Myogenic bHLH Gene Expression in the Somite, Development, 1995, vol. 121, pp. 651–660.

    Google Scholar 

  • Mönsterberg, A.E., Kitajewski, J., Bumcrot, D.A., et al., Combinatorial Signaling by Sonic Hedgehog and Wnt Family Members Induces Myogenic bHLH Gene Expression in the Somite, Gen. Dev., 1995, vol. 9, pp. 2911–2922.

    Article  Google Scholar 

  • Olson, E.N., Interplay between Proliferation and Differentiation within the Myogenic Lineage, Dev. Biol., 1992, vol. 154, pp. 261–272.

    Article  PubMed  CAS  Google Scholar 

  • Olson, E.N. and Klein, W.H., bHLH Factors in Muscle Development: Dead Lines and Commitments, What to Leave in and What to Leave Out, Gen. Dev., 1994, vol. 8, pp. 1–8.

    Article  CAS  Google Scholar 

  • Ozernyuk, N.D., Regulation of Myogenesis, Biol. Bull., 1998, vol. 25, no. 3, pp. 265–276.

    Google Scholar 

  • Ozernyuk, N.D., Comparative Properties of Myogenesis in Invertebrates and in Lower and Higher Vertebrates, Russ. J. Dev. Biol., 2004, vol. 35, no. 6, pp. 360–369.

    Article  CAS  Google Scholar 

  • Pownall, M.E. and Emerson, C.P., Sequential Activation of Three Myogenic Regulatory Genes during Somite Morphogenesis in Quail Embryos, Dev. Biol., 1992, vol. 151, pp. 67–79.

    Article  PubMed  CAS  Google Scholar 

  • Rawls, A. and Olson, E.N., MyoD Meets Its Maker, Cell, 1997, vol. 89, pp. 5–8.

    Article  PubMed  CAS  Google Scholar 

  • Rhodes, S.J. and Konieczny, S.F., Identification of MRF4: A New Member of the Muscle Regulatory Factor Gene Family, Gen. Dev., 1989, vol. 3, pp. 2050–2061.

    Article  CAS  Google Scholar 

  • Sato, D., Sugimura, K., Satoh, D., et al., Crossveinless-C, the Drosophila Homolog of Tumor Suppressor DLC1, Regulates Directional Elongation of Dendritic Branches via Down-Regulating Rho1 Activity, Gen. Cells, 2010, vol. 15, pp. 485–500.

    CAS  Google Scholar 

  • Sulston, J.E. and Horvitz, H.R., Post-Embryonic Cell Lineages of the Nematode Caenorhabditis elegans, Dev. Biol., 1977, vol. 56, pp. 110–156.

    Article  PubMed  CAS  Google Scholar 

  • Sulston, J.E., Schierenberg, E., White, J.G., et al., The Embryonic Cell Lineage of the Nematode Caenorhabditis elegans, Dev. Biol., 1983, vol. 100, pp. 64–119.

    Article  PubMed  CAS  Google Scholar 

  • Thisse, C., Thisse, B., Schillling, T.F., et al., Structure of the Zebrafish snail Gene and Its Expression in Wild-Type, spadetail and no tail Mutant Embryos, Development, 1996, vol. 119, pp. 1203–1215.

    Google Scholar 

  • Wang, W., Yu, H., and Long, M., Duplication-Degeneration as a Mechanism of Gene Fission and the Origin of New Genes in Drosophila Species, Nat. Genet., 2004, vol. 36, pp. 523–527.

    Article  PubMed  CAS  Google Scholar 

  • Weinberg, E.S., Allende, M.L., Kelly, C.S., et al., Developmental Regulation of Zebrafish MyoD in wild-type, no tail and spadetail embryos, Development, 1996, vol. 122, pp. 271–280.

    PubMed  CAS  Google Scholar 

  • Williams, B.A. and Ordahl, C.P., Pax-3 Expression in Segmental Mesoderm Marks Early Stages in Myogenic Cell Specification, Development, 1994, vol. 120, pp. 785–786.

    PubMed  CAS  Google Scholar 

  • Yamada, L., Kobayashi, K., Degan, B., et al., A Genomic Wide Survey of Developmentally Relevant Genes in Ciona intestinalis, Dev. Gen. Evol., 2003, vol. 213, pp. 245–253.

    Article  CAS  Google Scholar 

  • Yi, B., Bumbarger, D., and Sommer, R.J., Genetic Evidence for Pax-3 Function in Myogenesis in the Nematode Pristionchus pacificus, Evol. Dev., 2009, vol. 11, pp. 669–679.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Koltsov Institute of Developmental Biology, Russian Academy of Sciences, ul. Vavilova 26, Moscow, 119334, Russia

    N. D. Ozernyuk & N. S. Myuge

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  1. N. D. Ozernyuk
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  2. N. S. Myuge
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Correspondence to N. D. Ozernyuk.

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Original Russian Text © N.D. Ozernyuk, N.S. Myuge, 2012, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2012, No. 4, pp. 383–390.

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Ozernyuk, N.D., Myuge, N.S. Evolutional principles of homology in regulatory genes of myogenesis. Biol Bull Russ Acad Sci 39, 316–322 (2012). https://doi.org/10.1134/S1062359012040085

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