Skip to main content

Part of the book series: Topics in Neuroscience ((TOPNEURO))

  • 78 Accesses

Abstract

The differentiation of skeletal muscle is an early and crucial step in the development of vertebrates since it provides the embryo with motility in the early stages.Skeletal myogenesis begins shortly after gastrulation but persists, at least in mammals, until the end of postnatal growth, and the potential for myogenesis continues for the entire life span of the animal [1]. Local signalling commits mesodermal cells to a myogenic fate, and shortly afterwards they begin to synthesise contractile proteins that accumulate in the cytoplasm and self-assemble into sarcomeres. Motility is dependent upon shortening of the sarcomeres, paracrystalline structures that are specialised for transforming chemical energy into movement. The advantage of accumulating millions of sarcomeres within a single cytoplasm has led to multinucleation, a different strategy from the coupling of single cells adopted by the heart. Within the highly structured cytoplasm of the multinucleated muscle fibre mitosis is no longer possible, and when experimentally induced by oncogenes it leads to disruption of the spindle and death (mitotic catastrophe). As a consequence, growth of the muscle fibre during fetal and postnatal development depends upon the addition of single cells, which must be instructed on when to divide and when to differentiate, by fusing either with pre-existing fibres or among themselves to generate a new fibre. It is therefore obvious that diversification of myogenic cell fate is as crucial as their commitment.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 54.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Hauschka SD (1994) The embryonic origin of skeletal muscle. In: The scientific basis of myology. Academic Press, pp 3–72

    Google Scholar 

  2. Christ B, Ordhal CP (1994) Early stages of chick somite development. Anat Embryol 191:381–396

    Article  Google Scholar 

  3. Cossu G, Tajbakhsh S, Buckingham M (1996) Myogenic specification in mammals. Trends Genet 12:218–223

    Article  PubMed  CAS  Google Scholar 

  4. Cossu G, Kelly R, Tajbakhsh S et al (1996) Activation of different myogenic pathways: Myf5 is induced by the neural tube and MyoD by the dorsal ectoderm in mouse paraxial mesoderm. Development 122:429–437

    PubMed  CAS  Google Scholar 

  5. Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M (1997) Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf5 act upstream of MyoD. Cell 89:127–138

    Article  PubMed  CAS  Google Scholar 

  6. Braun T, Rudnicki MA, Arnold HH, Jaenisch R (1992) Targeted inactivation of the muscle regulatory gene Myf5 results in abnormal rib development and perinatal death. Cell 71:369–382

    Article  PubMed  CAS  Google Scholar 

  7. Kablar B, Krastel K, Ying C et al (1997) MyoD and Myf5 differentially regulate the development of limb versus trunk skeletal muscle. Development 124:4729–4738

    PubMed  CAS  Google Scholar 

  8. Tajbakhsh S, Buckingham ME (1994) Mouse limb muscle is determined in the absence of the earhest myogenic factor Myf5. Proc Natl Acad Sei USA 91:747–751

    Article  CAS  Google Scholar 

  9. Bober E, Franz T, Arnold HH et al (1994) Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120:603–612

    PubMed  CAS  Google Scholar 

  10. Bladt F, Riethmacher D, Isenmann S et al (1995) Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376:768–771

    Article  PubMed  CAS  Google Scholar 

  11. Pourquié O, Fan CM, Coltey M et al (1996) Lateral and axial signals involved in avian somite patterning: a role for BMP4. Cell 84:461–471

    Article  PubMed  Google Scholar 

  12. Fan C, Tessier-Lavigne M (1994) Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell 79:1175–1186

    Article  PubMed  CAS  Google Scholar 

  13. Borycki AG, Brunk B, Tajbakhsh S et al (1999) Sonic hedgehog control epaxial muscle deteminao Myf5 activation. Development 126:4053–4063

    PubMed  CAS  Google Scholar 

  14. Münsterberg AE, Kitajewski J, Bumcroft DA et al (1995) Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev 9:2911–2922

    Article  PubMed  Google Scholar 

  15. Tajbakhsh S, Borello U, Vivarelli E et al (1998) Differential activation of Myf5 and MyoD by different Wnts in expiants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf5. Development 125:4155–4162

    PubMed  CAS  Google Scholar 

  16. Murtaugh LC, Chyung JH, Lassar AB (1999) Sonic hedgehog promotes somitic chon-drogenesis by altering the cellular response to BMP signaling. Genes Dev 15:225–237

    Article  Google Scholar 

  17. Hirsinger E, Duprez D, Jouve C et al (1997) Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP4 in avian somite patterning. Development 124:4605–4614

    PubMed  CAS  Google Scholar 

  18. Marcelle C, Stark MR, Bronner-Fraser M (1997) Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124:3955–3963

    PubMed  CAS  Google Scholar 

  19. Banhot P, Brink M, Samos CH et al (1996) A new member of the frizzled family from Drosophila functions as a wingless receptor. Nature 382:225–230

    Article  Google Scholar 

  20. Wodarz A, Nusse R (1998) Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 14:59–88

    Article  PubMed  CAS  Google Scholar 

  21. Dierick H, Bejsovec A (1999) Cellular mechanisms of wingless/Wnt signal transduction. Curr Top Dev Biol 43:153–190

    Article  PubMed  CAS  Google Scholar 

  22. Kengaku M, Capdevila J, Rodriguez-Esteban C et al (1998) WNT3a regulates AER formation and utilizes an intracellular signaling pathway distinct from the dorso-ventral signal WNT7a during chick limb morphogenesis. Science 280:1274–1277

    Article  PubMed  CAS  Google Scholar 

  23. Leyns L, Bouwmeester T, Kim S-H et al (1997) Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88:747–756

    Article  PubMed  CAS  Google Scholar 

  24. Wang S, Krinks M, Lin K et al (1997) Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88:757–766

    Article  PubMed  CAS  Google Scholar 

  25. Borello U, Coletta M, Tajbakhsh S et al (1999) Trans-placental delivery of the Wnt antagonist Frzbl inhibits development of caudal paraxial mesoderm and skeletal myogenesis in mouse embryos. Development 126:4247–4255

    PubMed  CAS  Google Scholar 

  26. Ikeya M, Takada S (1998) Wnt signaling from the dorsal neural tube is required for the formation of the medial dermomyotome. Development 125:4969–4976

    PubMed  CAS  Google Scholar 

  27. Teillet M-A, Watanabe Y, Jeffs P et al (1998) Sonic hedgehog is required for survival of both myogenic and chondrogenic somitic lineages. Development 125:2019–2030

    PubMed  CAS  Google Scholar 

  28. Duprez D, Four nier-Thibault C, Douarin N. le (1998) Sonic hedgehog induces proliferation of committed skeletal muscle cells in the chick limb. Development 125:495–505

    PubMed  CAS  Google Scholar 

  29. Tajbakhsh S, Cossu G (1997) Establishing myogenic identity during somitogenesis. Curr Opin Genet Dev 7:634–641

    Article  PubMed  CAS  Google Scholar 

  30. Kelly AM, Zachs S (1969) The histogenesis of rat intercostal muscle. J Cell Biol 42:154–169

    Article  PubMed  CAS  Google Scholar 

  31. Baylies MK, Bate M, Ruiz Gomez M (1998) Myogenesis: a view from Drosophila. Cell 93:921–927

    Article  PubMed  CAS  Google Scholar 

  32. McGrew M J, Pourquié O (1998) Somitogenesis: segmenting a vertebrate. Curr Opin Genet Dev 8:487–493

    Article  PubMed  CAS  Google Scholar 

  33. Wilson-Rawls J, Molkentin JD, Black BL, Olson EN (1999) Activated Notch inhibits myogenic activity of the MADS-Box transcription factor myocyte enhancer factor 2C. Mol Cell Biol 4:2853–2862

    Google Scholar 

  34. Nofziger D, Miyamoto A, Lyons KM, Weinmaster G (1999) Notch signaling imposes two distinct blocks in the differentiation of C2C12 myoblasts. Development 126:1689–1702

    PubMed  CAS  Google Scholar 

  35. Buffmger N, Stockdale PB (1994) Myogenic specification in somites: induction by axial structures. Development 120:1443–1452

    Google Scholar 

  36. Kalcheim C, Neufeld G (1990) Expression of basic fibroblast growth factor in the nervous system of early avian embryos. Development 109:203–215

    PubMed  CAS  Google Scholar 

  37. Marcelle C, Wolf J, Bonner-Fraser M (1995) The in vivo expression of the FGF receptor FREK mRNA in avian myoblasts suggests a role in muscle growth and differentiation. Dev Biol 172:100–114

    Article  PubMed  CAS  Google Scholar 

  38. Cusella de Angelis MG, Molinari S, Ledonne A et al (1994) Differential response of embryonic and fetal myoblasts to TGFß: a possible regulatory mechanism of skeletal muscle histogenesis. Development 120:925–933

    PubMed  CAS  Google Scholar 

  39. Zappelli F, Willems D, Osada S et al (1996) The inhibition of differentiation caused by TGFß in fetal myoblasts is dependant upon selective expression of PKCO: A possible molecular basis for myoblast diversification during limb histogenesis. Dev Biol 180:156–164

    Article  PubMed  CAS  Google Scholar 

  40. Bischoff R (1994) The satellite cell and muscle regeneration, In: Engel AG, Franzini-Armstrong C (eds) Myology, 2nd edn. McGraw-Hill, New York, pp 97–133

    Google Scholar 

  41. Miller JB, Schaefer L, Dominov JA (1999) Seeking muscle stem cells. Curr Top Dev Biol 43:191–219

    Article  PubMed  CAS  Google Scholar 

  42. Seale P, Rudnicki MA (2000) A new look at the origin, function, and “stem-cell” status of muscle satellite cells. Dev Biol 218:115–124

    Article  PubMed  CAS  Google Scholar 

  43. Cossu G, Molinaro M (1987) Cell heterogeneity in the myogenic lineage. Curr Top Dev Biol 23:185–208

    Article  PubMed  CAS  Google Scholar 

  44. Armand O, Boutineau AM, Mauger A et al (1983) Origin of satellite cells in avian skeletal muscles. Arch Anat Microsc 72:163–181

    CAS  Google Scholar 

  45. Grounds MD, Garrett KL, Lai MC et al (1992) Identification of skeletal muscle precursor cells in vivo by use of MyoDl and myogenin probes. Cell Tissue Res 267:99–104

    Article  PubMed  CAS  Google Scholar 

  46. Tajbakhsh S, Vivarelli G, Cusella de AngeHs G et al (1994) A population of myogenic cells derived from the mouse neural tube. Neuron 13:813–821

    Article  PubMed  CAS  Google Scholar 

  47. Cossu G (1997) Unorthodox myogenesis: possible developmental significance and implications for tissue histogenesis and regeneration. Histol Histopathol 12:755–760

    PubMed  CAS  Google Scholar 

  48. Ferrari G, Cusella de Angelis MG, Coletta M et al (1998) Skeletal muscle regeneration by bone marrow derived myogenic progenitors. Science 279:1528–1530

    Article  PubMed  CAS  Google Scholar 

  49. De Angelis L, Berghella L, Coletta M et al (1999) Skeletal myogenic progenitors originating from embryonic dorsal aorta co-express endothelial and myogenic markersand contribute to post-natal muscle growth and regeneration. J Cell Biol 147:869–878

    Article  PubMed  Google Scholar 

  50. Katagiri T, Yamaguchi A, Komaki M et al (1994) Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol 127:1755–1766

    Article  PubMed  CAS  Google Scholar 

  51. Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74

    Article  PubMed  CAS  Google Scholar 

  52. Kaul A, Köster M, Neahus H, Braun T (2000) Myf-5 revisited: loss of early myotome formation does not lead to a rib phenotype in homozygous Myf-5 mutant mice. Cell 102:17–19

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer-Verlag Italia

About this chapter

Cite this chapter

Cossu, G. (2002). Ontogeny of Skeletal Muscle Cells. In: Vincent, A., Martino, G. (eds) Autoantibodies in Neurological Diseases. Topics in Neuroscience. Springer, Milano. https://doi.org/10.1007/978-88-470-2097-9_6

Download citation

  • DOI: https://doi.org/10.1007/978-88-470-2097-9_6

  • Publisher Name: Springer, Milano

  • Print ISBN: 978-88-470-2163-1

  • Online ISBN: 978-88-470-2097-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics