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Cellular and molecular basis of skeletal muscle hystogenesis

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Abstract

The molecular basis of development and regeneration of skeletal muscles are reviewed. A model of parent-progeny relationships of mature animals’ skeletal muscles is proposed. Different cellular populations that contribute to myogenesis in vivo and in vitro are described. Both well-known typical cellular sources for muscle regeneration (satellite cells, muscle derived stem cells) and alternative cellular sources (CD133+ cells, pericytes, SP-cells from muscles and from bone marrow, mesangioblasts, embryonic stem cells and mesenchymal stromal cells) are presented. Moreover, some evidence for the existence of ectopic myogenic precursors in nonmuscle tissues is given.

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References

  • De Angelis, L., Berghella, L., Coletta, M., et al., Skeletal Myogenic Progenitors Originating from Embryonic Dorsal Aorta Coexpress Endothelial and Myogenic Markers and Contribute to Postnatal Muscle Growth and Regeneration, J. Cell Biol., 1999, vol. 147, pp. 869–878.

    Article  PubMed  Google Scholar 

  • Asakura, A., Komaki, M., and Rudnicki, M., Muscle Satellite Cells Are Multipotential Stem Cells that Exhibit Myogenic, Osteogenic, and Adipogenic Differentiation, Differentiation, 2001, vol. 68, pp. 245–253.

    Article  PubMed  CAS  Google Scholar 

  • Bajanca, F., Luz, M., Raymond, K., Martins, G.G., et al., Integrin alpha6 beta1-Laminin Interactions Regulate Early Myotome Formation in the Mouse Embryo, Development, 2006, vol. 133, pp. 1635–1644.

    Article  PubMed  CAS  Google Scholar 

  • Barton, P.J. and Buckingham, M.E., The Myosin Alkali Light Chain Proteins and Their Genes, Biochem. J., 1985, vol. 231, pp. 249–261.

    PubMed  CAS  Google Scholar 

  • Beauchamp, J.R., Heslop, L., Yu, D.S., et al., Expression of CD34 and Myf5 Defines the Majority of Quiescent Adult Skeletal Muscle Satellite Cells, J. Cell Biol., 2000, vol. 151, pp. 1221–1234.

    Article  PubMed  CAS  Google Scholar 

  • Birchmeier, C. and Brohmann, H., Genes that Control the Development of Migrating Muscle Precursor Cells, Curr. Opin. Cell. Biol., 2000, vol. 12, pp. 725–730.

    Article  PubMed  CAS  Google Scholar 

  • Blau, H.M. and Epstein, C.J., Manipulation of Myogenesis in vitro: Reversible Inhibition by DMSO, Cell, 1979, vol. 17, pp. 95–108.

    Article  PubMed  CAS  Google Scholar 

  • Bockman, D. Bockman, D.E., Myoid Cells in Adult Human Thymus, Nature, 1968, vol. 218, pp. 286–287.

    Article  PubMed  CAS  Google Scholar 

  • Braun, T., Winter, B., Bober, E., and Arnold, H.H., Transcriptional Activation Domain of the Muscle-Specific Gene-Regulatory Protein Myf5, Nature, 1990, vol. 346, pp. 663–665.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Buckingham, M., Bajard, L., Chang, T., et al., The Formation of Skeletal Muscle: From Somite to Limb, J. Anat., 2003, vol. 202, pp. 59–68.

    Article  PubMed  Google Scholar 

  • Buskin, J.N. and Hauschka, S.D., Identification of a Myocyte Nuclear Factor that Binds to the Muscle-Specific Enhancer of the Mouse Muscle Creatine Kinase Gene, Mol. Cell. Biol., 1989, vol. 9, pp. 2627–2640.

    PubMed  CAS  Google Scholar 

  • Cossu, G., Tajbakhsh, S., and Buckingham, M., How Is Myogenesis Initiated in the Embryo?, Trends Genet., 1996, vol. 12, pp. 218–223.

    Article  PubMed  CAS  Google Scholar 

  • Costa, M.L., Escaleira, R., Cataldo, A., et al., Desmin: Molecular Interactions and Putative Functions of the Muscle Intermediate Filament Protein, Braz. J. Med. Biol. Res., 2004, vol. 37, pp. 1819–1830.

    Article  PubMed  CAS  Google Scholar 

  • Cusella De Angelis, M.G., Balconi, G., Bernasconi, S., et al., Skeletal Myogenic Progenitors in the Endothelium of Lung and Yolk Sac, Exp. Cell Res., 2003, vol. 290, pp. 207–216.

    Article  PubMed  Google Scholar 

  • Danisovic, L., Varga, I., Polak, S., et al., Morphology of in vitro Expanded Human Muscle-Derived Stem Cells, Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech. Repub., 2008, vol. 152, pp. 235–238.

    Article  PubMed  Google Scholar 

  • Dellavalle, A., Sampaolesi, M., Tonlorenzi, R., et al., Pericytes of Human Skeletal Muscle Are Myogenic Precursors Distinct from Satellite Cells, Nat. Cell Biol., 2007, vol. 9, pp. 255–267.

    Article  PubMed  CAS  Google Scholar 

  • Di Rocco, G., Tritarelli, A., Toietta, G., et al., Spontaneous Myogenic Differentiation of Flk-1-Positive Cells from Adult Pancreas and Other Nonmuscle Tissues, Am. J. Physiol. Cell. Physiol., 2008, vol. 294, pp. 604–612.

    Article  Google Scholar 

  • Duprez, D. Duprez, D., Signals Regulating Muscle Formation in the Limb during Embryonic Development, Int. J. Dev. Biol., 2002, vol. 46, pp. 915–925.

    PubMed  CAS  Google Scholar 

  • Gang, E.J., Jeong, J.A., Hong, S.H., et al., Skeletal Myogenic Differentiation of Mesenchymal Stem Cells Isolated from Human Umbilical Cord Blood, Stem Cells, 2004, vol. 22, pp. 617–624.

    Article  PubMed  Google Scholar 

  • Gerhart, J., Bast, B., Neely, C., et al., MyoD-Positive Myoblasts Are Present in Mature Fetal Organs Lacking Skeletal Muscle, J. Cell Biol., 2001, vol. 155, pp. 381–392.

    Article  PubMed  CAS  Google Scholar 

  • Gnocchi, V.F., White, R.B., Ono, Y., et al., Further Characterisation of the Molecular Signature of Quiescent and Activated Mouse Muscle Satellite Cells, PLoS One, 2009, vol. 4, p. e5205.

    Article  PubMed  Google Scholar 

  • Goodell, M.A., Brose, K., Paradis, G., et al., Isolation and Functional Properties of Murine Hematopoietic Stem Cells that Are Replicating in vivo, J. Exp. Med., 1996, vol. 183, pp. 1797–1806.

    Article  PubMed  CAS  Google Scholar 

  • Gornostaeva, S.N., Rzhaninova, A.A., and Gol’dstein, D.V., Myogenesis in Hemopoietic Tissue Mesenchymal Stem Cell Culture, Bull. Exp. Biol. Med., 2006, vol. 141, pp. 493–499.

    Article  PubMed  CAS  Google Scholar 

  • Gros, J., Manceau, M., Thom, V., and Marcelle, C., A Common Somitic Origin for Embryonic Muscle Progenitors and Satellite Cells, Nature, 2005, vol. 435, pp. 954–958.

    Article  PubMed  CAS  Google Scholar 

  • Grounds, M.D., White, J.D., Rosenthal, N., and Bogoyevitch, M.A., The Role of Stem Cells in Skeletal and Cardiac Muscle Repair, J. Histochem. Cytochem., 2002, vol. 50, pp. 589–610.

    Article  PubMed  CAS  Google Scholar 

  • Hewitt, J., Lu, X., Gilbert, L., and Nanes, M.S., The Muscle Transcription Factor MyoD Promotes Osteoblast Differentiation by Stimulation of the Osterix Promoter, Endocrinology, 2008, vol. 149, pp. 3698–3707.

    Article  PubMed  CAS  Google Scholar 

  • Hinterberger, T.J., Sassoon, D.A., Rhodes, S.J., and Konieczny, S.F., Expression of the Muscle Regulatory Factor MRF4 during Somite and Skeletal Myofiber Development, Dev. Biol., 1991, vol. 147, pp. 144–156.

    Article  PubMed  CAS  Google Scholar 

  • Kaufman, S.J. and Foster, R.F., Replicating Myoblasts Express a Muscle-Specific Phenotype, Proc. Natl. Acad. Sci. USA, 1988, vol. 85, pp. 9606–9610.

    Article  PubMed  CAS  Google Scholar 

  • Krupnick, A.S., Balsara, K.R., Kreisel, D., et al., Fetal Liver as a Source of Autologous Progenitor Cells for Perinatal Tissue Engineering, Tissue Eng., 2004, vol. 10, pp. 723–735.

    Article  PubMed  Google Scholar 

  • Kuang, S., Chargé, S.B., Seale, P., et al., Distinct Roles for Pax7 and Pax3 in Adult Regenerative Myogenesis, J. Cell Biol., 2006, vol. 172, pp. 103–113.

    Article  PubMed  CAS  Google Scholar 

  • Kuçi, S., Kuçi, Z., Schmid, S., et al., Efficient in vitro Generation of Adult Multipotent Cells from Mobilized Peripheral Blood CD133+ Cells, Cell Prolif., 2008, vol. 41, pp. 12–27.

    Article  PubMed  Google Scholar 

  • Li, H. and Capetanaki, Y., Regulation of the Mouse Desmin Gene: Transactivated by MyoD, Myogenin, MRF4 and Myf5, Nucleic Acid Res., 1993, vol. 21, pp. 335–343.

    Article  PubMed  CAS  Google Scholar 

  • Li, Z., Mericskay, M., Agbulut, O., et al., Desmin Is Essential for the Tensile Strength and Integrity of Myofibrils but not for Myogenic Commitment, Differentiation, and Fusion of Skeletal Muscle, J. Cell Biol., 1997, vol. 139, pp. 129–144.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Y., Song, J., Liu, W., et al., Growth and Differentiation of Rat Bone Marrow Stromal Cells: Does 5-Azacytidine Trigger Their Cardiomyogenic Differentiation?, Cardiovasc. Res., 2003, vol. 58, pp. 460–468.

    Article  PubMed  CAS  Google Scholar 

  • Luth, E.S., Jun, S.J., Wessen, M.K., et al., Bone Marrow Side Population Cells Are Enriched for Progenitors Capable of Myogenic Differentiation, J. Cell Sci., 2008, vol. 121, pp. 1426–1434.

    Article  PubMed  CAS  Google Scholar 

  • Mauro, A. and Adams, W.R., The Structure of the Sarcolemma of the Frog Skeletal Muscle Fiber, J. Biophys. Biochem. Cytol., 1961, vol. 10, pp. 177–185.

    Article  PubMed  Google Scholar 

  • McKinnell, I.W., Ishibashi, J., Le Grand, F., et al., Pax7 Activates Myogenic Genes by Recruitment of a Histone Methyltransferase Complex, Nat. Cell Biol., 2008, vol. 10, pp. 77–84.

    Article  PubMed  CAS  Google Scholar 

  • Miller, J.B., Myogenic Programs of Mouse Muscle Cell Lines: Expression of Myosin Heavy Chain Isoforms, MyoD1, and Myogenin, J. Cell Biol., 1990, vol. 111, pp. 1149–1159.

    Article  PubMed  CAS  Google Scholar 

  • Minasi, M.G., Riminucci, M., De Angelis, L., et al., The Meso-Angioblast: A Multipotent, Self-Renewing Cell that Originates from the Dorsal Aorta and Differentiates into Most Mesodermal Tissues, Development, 2002, vol. 129, pp. 2773–2783.

    PubMed  CAS  Google Scholar 

  • Olson, E. Olson, E.N., MyoD Family: A Paradigm for Development?, Genes Dev., 1990, vol. 4, pp. 1454–1461.

    Article  PubMed  CAS  Google Scholar 

  • Packard, D.S., Jr. and Meier, S., An Experimental Study of the Somitomeric Organization of the Avian Segmental Plate, Dev. Biol., 1983, vol. 97, pp. 191–202.

    Article  PubMed  Google Scholar 

  • Péault, B., Rudnicki, M., Torrente, Y., et al., Stem and Progenitor Cells in Skeletal Muscle Development, Maintenance, and Therapy, Mol. Ther., 2007, vol. 15, pp. 867–877.

    Article  PubMed  Google Scholar 

  • Payushina, O.V., Khnykova, O.N., Butorina, N.N., et al., Spontaneous Myogenesis in the Primary Culture of Fetal Rat Liver, Dokl. Biol. Sci., 2009, vol. 425, pp. 187–189.

    Article  Google Scholar 

  • Qu-Petersen, Z., Deasy, B., Jankowski, R., et al., Identification of a Novel Population of Muscle Stem Cells in Mice: Potential for Muscle Regeneration, J. Cell Biol., 2002, vol. 157, pp. 851–864.

    Article  PubMed  CAS  Google Scholar 

  • Relaix, F., Montarras, D., Zaffran, S., et al., Pax3 and Pax7 Have Distinct and Overlapping Functions in Adult Muscle Progenitor Cells, J. Cell Biol., 2006, vol. 172, pp. 91–102.

    Article  PubMed  CAS  Google Scholar 

  • Rose, O., Rohwedel, J., Reinhardt, S., et al., Expression of M-Cadherin Protein in Myogenic Cells during Prenatal Mouse Development and Differentiation of Embryonic Stem Cells in Culture, Dev. Dyn., 1994, vol. 201, pp. 245–259.

    Article  PubMed  CAS  Google Scholar 

  • Rudnicki, M.A., Le Grand, F., McKinnell, I., and Kuang, S., The Molecular Regulation of Muscle Stem Cell Function, Cold Spring Harb. Symp. Quant. Biol., 2008, vol. 73, pp. 323–331.

    Article  PubMed  CAS  Google Scholar 

  • Tam, P. Tam, P.P., The Control of Somitogenesis in Mouse Embryos, J. Embryol. Exp. Morphol., 1981, vol. 65, pp. 103–128.

    PubMed  Google Scholar 

  • Tamaki, T., Okada, Y., Uchiyama, Y., et al., Clonal Multipotency of Skeletal Muscle-Derived Stem Cells between Mesodermal and Ectodermal Lineage, Stem Cells, 2007, vol. 25, pp. 2283–2290.

    Article  PubMed  CAS  Google Scholar 

  • Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., et al., Embryonic Stem Cell Lines Derived from Human Blastocysts, Science, 1998, vol. 282, pp. 1145–1147.

    Article  PubMed  CAS  Google Scholar 

  • Weintraub, H., The MyoD Family and Myogenesis: Redundancy, Networks, and Thresholds, Cell, 1993, vol. 75, pp. 1241–1244.

    Article  PubMed  CAS  Google Scholar 

  • Zheng, J.K., Wang, Y., Karandikar, A., et al., Skeletal Myogenesis by Human Embryonic Stem Cells, Cell Res., 2006, vol. 16, pp. 713–722.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

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

    O. N. Sheveleva, O. V. Payushina & V. I. Starostin

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  1. O. N. Sheveleva
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  2. O. V. Payushina
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  3. V. I. Starostin
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Correspondence to O. V. Payushina.

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Original Russian Text © O.N. Sheveleva, O.V. Payushina, V.I. Starostin, 2012, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2012, No. 6, pp. 579–588.

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Sheveleva, O.N., Payushina, O.V. & Starostin, V.I. Cellular and molecular basis of skeletal muscle hystogenesis. Biol Bull Russ Acad Sci 39, 495–503 (2012). https://doi.org/10.1134/S1062359012060118

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