Review Article | Published:

The genetics of vertebrate myogenesis

Nature Reviews Genetics volume 9, pages 632646 (2008) | Download Citation

Abstract

The molecular, genetic and cellular bases for skeletal muscle growth and regeneration have been recently documented in a number of vertebrate species. These studies highlight the role of transient subcompartments of the early somite as a source of distinct waves of myogenic precursors. Individual myogenic progenitor populations undergo a complex series of cell rearrangements and specification events in different regions of the body, all of which are controlled by distinct gene regulatory networks. Collectively, these studies have opened a window into the morphogenetic and molecular bases of the different phases of vertebrate myogenesis, from embryo to adult.

Key points

  • Vertebrate myogenesis is a complex process that has been studied in a range of model systems.

  • Myogenic regulatory factors and paired box (Pax) genes are involved in the cell-autonomous regulation of myogenesis. The context of myogenesis is determined by the nature of signals secreted from surrounding tissues, which have an important role in myogenic induction. Myogenesis can be separated into three phases — primary myotome formation, muscle growth and adult myogenesis.

  • Cell movements and cell adhesion have important roles in the early myotome.

  • Satellite cells seem to be responsible for regulating the majority of the processes involved in adult myogenesis.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    , & Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 18, 747–783 (2002).

  2. 2.

    Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr. Opin. Genet. Dev. 16, 525–532 (2006).

  3. 3.

    , , , & Extrinsic versus intrinsic cues in avian paraxial mesoderm patterning and differentiation. Dev. Dyn. 236, 2397–2409 (2007).

  4. 4.

    , , & A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435, 948–953 (2005). References 4–10 describe the identification of progenitor cells that contribute to the second phase of myogenesis in the mouse, chick and zebrafish.

  5. 5.

    , , & A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435, 954–958 (2005).

  6. 6.

    & Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates. Development 132, 689–701 (2005).

  7. 7.

    et al. Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 19, 1426–1431 (2005).

  8. 8.

    et al. Whole-somite rotation generates muscle progenitor cell compartments in the developing zebrafish embryo. Dev. Cell 12, 207–219 (2007).

  9. 9.

    , , , & Dynamic somite cell rearrangements lead to distinct waves of myotome growth. Development 134, 1253–1257 (2007).

  10. 10.

    et al. Somitic origin of limb muscle satellite and side population cells. Proc. Natl Acad. Sci. USA 103, 945–950 (2006).

  11. 11.

    et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122, 289–301 (2005). Using serial transplantation of genetically marked single muscle fibres these authors provide the strongest evidence to date that satellite cells undergo self-renewal in vivo .

  12. 12.

    et al. Direct isolation of satellite cells for skeletal muscle regeneration. Science 309, 2064–2067 (2005).

  13. 13.

    , , & Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nature Cell Biol. 8, 677–687 (2006). References 13 and 14 illustrate the capacity for asymmetric self-renewal of satellite cells and describe the potential relationship of committed progenitors and satellite stem cells.

  14. 14.

    , , & Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129, 999–1010 (2007).

  15. 15.

    & The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu. Rev. Cell Dev. Biol. 23, 645–673 (2007).

  16. 16.

    , , & Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71, 369–382 (1992).

  17. 17.

    , , & Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383–390 (1992).

  18. 18.

    et al. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351–1359 (1993).

  19. 19.

    et al. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501–506 (1993).

  20. 20.

    et al. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532–535 (1993).

  21. 21.

    et al. Disruption of the mouse MRF4 gene identifies multiple waves of myogenesis in the myotome. Development 121, 3347–3358 (1995).

  22. 22.

    , & Inactivation of the myogenic bHLH gene MRF4 results in up-regulation of myogenin and rib anomalies. Genes Dev. 9, 1388–1399 (1995).

  23. 23.

    et al. Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 431, 466–471 (2004).

  24. 24.

    , , & Two cell lineages, myf5 and myf5-independent, participate in mouse skeletal myogenesis. Dev. Cell 14, 437–445 (2008). References 24 and 25 provide the first in vivo description of two distinct lineages within the early myotome of the mouse that differentially express Myf5 .

  25. 25.

    , , , & Different autonomous myogenic cell populations revealed by ablation of Myf5-expressing cells during mouse embryogenesis. Development 135, 1597–1604 (2008).

  26. 26.

    & Myf-5 and myoD genes are activated in distinct mesenchymal stem cells and determine different skeletal muscle cell lineages. Embo J. 15, 310–318 (1996).

  27. 27.

    et al. Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 89, 139–148 (1997).

  28. 28.

    et al. Pax7 is required for the specification of myogenic satellite cells. Cell 102, 777–786 (2000).

  29. 29.

    & Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development 120, 785–796 (1994).

  30. 30.

    , , & Pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse. Development 122, 1017–1027 (1996).

  31. 31.

    , , & Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89, 127–138 (1997).

  32. 32.

    et al. Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nature Med. 14, 134–143 (2008).

  33. 33.

    et al. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev. 20, 2450–2464 (2006).

  34. 34.

    et al. Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. Genes Dev. 13, 3231–3243 (1999).

  35. 35.

    et al. Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development 132, 2235–2249 (2005).

  36. 36.

    et al. Eya1 and Eya2 proteins are required for hypaxial somitic myogenesis in the mouse embryo. Dev. Biol. 302, 602–616 (2007).

  37. 37.

    et al. Expression of myogenin during embryogenesis is controlled by Six/sine oculis homeoproteins through a conserved MEF3 binding site. Proc. Natl Acad. Sci. USA 95, 14220–14225 (1998).

  38. 38.

    et al. Six proteins regulate the activation of Myf5 expression in embryonic mouse limbs. Proc. Natl Acad. Sci. USA 104, 11310–11315 (2007).

  39. 39.

    et al. Loss of myogenin in postnatal life leads to normal skeletal muscle but reduced body size. Development 133, 601–610 (2006).

  40. 40.

    , , , & Coactivation of MEF2 by the SAP domain proteins myocardin and MASTR. Mol. Cell 23, 83–96 (2006).

  41. 41.

    , , , & The myocardin-related transcription factor, MASTR, cooperates with MyoD to activate skeletal muscle gene expression. Proc. Natl Acad. Sci. USA 105, 1545–1550 (2008).

  42. 42.

    , & Cellular heterogeneity during vertebrate skeletal muscle development. Dev. Biol. 308, 281–293 (2007).

  43. 43.

    , , , & Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev. 9, 2911–2922 (1995).

  44. 44.

    et al. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407–413 (1996).

  45. 45.

    et al. Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development 126, 4053–4063 (1999).

  46. 46.

    et al. Sonic hedgehog is a survival factor for hypaxial muscles during mouse development. Development 128, 743–752 (2001).

  47. 47.

    , , & Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. Genes Dev. 11, 2163–2175 (1997).

  48. 48.

    , , & Positive and negative regulation of muscle cell identity by members of the hedgehog and TGF-beta gene families. J. Cell Biol. 139, 145–156 (1997).

  49. 49.

    , & Hedgehog acts directly on the zebrafish dermomyotome to promote myogenic differentiation. Dev. Biol. 300, 736–746 (2006).

  50. 50.

    et al. Signals and myogenic regulatory factors restrict pax3 and pax7 expression to dermomyotome-like tissue in zebrafish. Dev. Biol. 302, 504–521 (2007).

  51. 51.

    et al. Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification. Genes Dev. 16, 114–126 (2002).

  52. 52.

    , & The initial somitic phase of Myf5 expression requires neither Shh signaling nor Gli regulation. Genes Dev. 17, 2870–2874 (2003).

  53. 53.

    et al. Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation. Development 132, 345–357 (2005).

  54. 54.

    , & Hedgehog signaling regulates the amount of hypaxial muscle development during Xenopus myogenesis. Dev. Biol. 304, 722–734 (2007).

  55. 55.

    , & Fgf8 drives myogenic progression of a novel lateral fast muscle fibre population in zebrafish. Development 132, 4211–4222 (2005).

  56. 56.

    et al. Retinoic acid activates myogenesis in vivo through Fgf8 signalling. Dev. Biol. 289, 127–140 (2006).

  57. 57.

    , , , & FGFR4 signaling is a necessary step in limb muscle differentiation. Development 129, 4559–4569 (2002).

  58. 58.

    , & Misexpression of Fgf-4 in the chick limb inhibits myogenesis by down-regulating Frek expression. Dev. Biol. 233, 56–71 (2001).

  59. 59.

    & Ectopic Myf5 or MyoD prevents the neuronal differentiation program in addition to inducing skeletal muscle differentiation, in the chick neural tube. Development 131, 713–723 (2004).

  60. 60.

    et al. Differential activation of Myf5 and MyoD by different Wnts in explants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf5. Development 125, 4155–4162 (1998).

  61. 61.

    et al. The Wnt/beta-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis. Development 133, 3723–3732 (2006).

  62. 62.

    et al. R-Spondin2 is a secreted activator of Wnt/beta-catenin signaling and is required for Xenopus myogenesis. Dev. Cell 7, 525–534 (2004).

  63. 63.

    , & Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins. Nature 433, 317–322 (2005). The intracellular pathway triggered by Wnt signals to generate myogenic induction are largely unknown. This report implicates the classical cAMP pathway and the transcription factor CREB in this process.

  64. 64.

    et al. Beta-catenin-dependent Wnt signalling controls the epithelial organisation of somites through the activation of paraxis. Development 132, 3895–3905 (2005).

  65. 65.

    , , , & Regulation of ectodermal Wnt6 expression by the neural tube is transduced by dermomyotomal Wnt11: a mechanism of dermomyotomal lip sustainment. Development 133, 2897–2904 (2006).

  66. 66.

    , , , & Beta catenin-independent activation of MyoD in presomitic mesoderm requires PKC and depends on Pax3 transcriptional activity. Dev. Biol. 304, 604–614 (2007).

  67. 67.

    , & Local extrinsic signals determine muscle and endothelial cell fate and patterning in the vertebrate limb. Dev. Cell 3, 533–545 (2002).

  68. 68.

    , & Characterization of the early development of specific hypaxial muscles from the ventrolateral myotome. Development 126, 4305–4315 (1999).

  69. 69.

    , & A two-step mechanism for myotome formation in chick. Dev. Cell 6, 875–882 (2004). This paper outlines an important contribution that clarifies the process of primary myotome formation in the chick through the use of regional fate mapping by electroporation.

  70. 70.

    , & The origin and fate of pioneer myotomal cells in the avian embryo. Mech. Dev. 74, 59–73 (1998).

  71. 71.

    , & The roles of cell migration and myofiber intercalation in patterning formation of the postmitotic myotome. Development 129, 2675–2687 (2002).

  72. 72.

    , & Location and growth of epaxial myotome precursor cells. Development 124, 1601–1610 (1997).

  73. 73.

    & The growth of the dermomyotome and formation of early myotome lineages in thoracolumbar somites of chicken embryos. Development 127, 893–905 (2000).

  74. 74.

    , , & The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium. Development 128, 1731–1744 (2001).

  75. 75.

    , & Differential effects of N-cadherin-mediated adhesion on the development of myotomal waves. Development 133, 1101–1112 (2006).

  76. 76.

    et al. Integrin alpha6beta1-laminin interactions regulate early myotome formation in the mouse embryo. Development 133, 1635–1644 (2006).

  77. 77.

    , & Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice. Nature 384, 266–270 (1996).

  78. 78.

    et al. Integrin alpha6beta1-laminin interactions regulate early myotome formation in the mouse embryo. Development 133, 1635–1644 (2006).

  79. 79.

    A community effect in animal development. Nature 336, 772–774 (1988).

  80. 80.

    , , & A community effect in muscle development. Curr. Biol. 3, 1–11 (1993).

  81. 81.

    , , , & Myoblast differentiation during mammalian somitogenesis is dependent upon a community effect. Proc. Natl Acad. Sci. USA 92, 2254–2258 (1995).

  82. 82.

    , & Cadherin-mediated cell interactions are necessary for the activation of MyoD in Xenopus mesoderm. Proc. Natl Acad. Sci USA 91, 10844–10848 (1994).

  83. 83.

    , , & Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119, 1203–1215 (1993).

  84. 84.

    , , & Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122, 3371–3380 (1996).

  85. 85.

    et al. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development 122, 271–280 (1996).

  86. 86.

    et al. Myosin heavy chain expression in zebrafish and slow muscle composition. Dev. Dyn. 233, 1018–1022 (2005).

  87. 87.

    & Molecular and cellular mechanisms involved in the generation of fiber diversity during myogenesis. Int. Rev. Cytol. 216, 175–232 (2002).

  88. 88.

    et al. Cadherin-mediated differential cell adhesion controls slow muscle cell migration in the developing zebrafish myotome. Dev. Cell 5, 865–876 (2003).

  89. 89.

    et al. Hedgehog regulation of superficial slow muscle fibres in Xenopus and the evolution of tetrapod trunk myogenesis. Development 131, 3249–3262 (2004).

  90. 90.

    Development of the lateral musculature in the teleost, Brachydanio rerio: a fine structural study. Am. J. Anat. 125, 457–493 (1969).

  91. 91.

    et al. Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish. Evol. Dev. 8, 101–110 (2006).

  92. 92.

    , & Growth in the larval zebrafish pectoral fin and trunk musculature. Dev. Dyn. 237, 307–315 (2008).

  93. 93.

    & Myf-5 is transiently expressed in nonmuscle mesoderm and exhibits dynamic regional changes within the presegmented mesoderm and somites I–IV. Dev. Biol. 232, 77–90 (2001).

  94. 94.

    & Somitogenesis in the amphibian Xenopus laevis: scanning electron microscopic analysis of intrasomitic cellular arrangements during somite rotation. J. Embryol. Exp. Morphol. 64, 23–43 (1981).

  95. 95.

    The origin and morphogenesis of amphibian somites. Curr. Top. Dev. Biol. 47, 183–246 (2000).

  96. 96.

    , , , & Cell behaviors associated with somite segmentation and rotation in Xenopus laevis. Dev. Dyn. 235, 3268–3279 (2006).

  97. 97.

    Muscle development in a biphasic animal: the frog. Dev. Dyn. 236, 2444–2453 (2007).

  98. 98.

    Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493–495 (1961).

  99. 99.

    , , , & Origin of satellite cells in avian skeletal muscles. Arch. Anat. Microsc. Morphol. Exp. 72, 163–181 (1983).

  100. 100.

    , & Control of muscle regeneration in the Xenopus tadpole tail by Pax7. Development 133, 2303–2313 (2006).

  101. 101.

    , , & Salamander limb regeneration involves the activation of a multipotent skeletal muscle satellite cell population. J. Cell Biol. 172, 433–440 (2006).

  102. 102.

    Muscle satellite cells in urodele amphibians: facilitated identification of satellite cells using ruthenium red staining. J. Exp. Zool. 198, 57–64 (1976).

  103. 103.

    et al. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 172, 91–102 (2006).

  104. 104.

    , & Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J. 23, 3430–3439 (2004).

  105. 105.

    , , , & Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors. Cell 130, 349–362 (2007).

  106. 106.

    et al. Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nature Cell Biol. 10, 77–84 (2008).

  107. 107.

    , & A homeo-paired domain-binding motif directs Myf5 expression in progenitor cells of limb muscle. Development 134, 1171–1180 (2007).

  108. 108.

    et al. Myf5 expression in satellite cells and spindles in adult muscle is controlled by separate genetic elements. Dev. Biol. 273, 454–465 (2004).

  109. 109.

    , , & The A17 enhancer directs expression of Myf5 to muscle satellite cells but Mrf4 to myonuclei. Dev. Dyn. 236, 3419–3426 (2007).

  110. 110.

    , , & Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination. J. Cell Biol. 177, 769–779 (2007).

  111. 111.

    et al. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol. Ther. 15, 867–877 (2007).

  112. 112.

    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. 147, 869 (1999).

  113. 113.

    et al. The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129, 2773–2783 (2002).

  114. 114.

    et al. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444, 574–579 (2006).

  115. 115.

    , , & Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575–1577 (2003). References 115–118 investigate the molecular basis for the decline of satellite-cell function with age and implicate Notch and Wnt signal transduction in this process.

  116. 116.

    et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807–810 (2007).

  117. 117.

    et al. Augmented Wnt signaling in a mammalian model of accelerated aging. Science 317, 803–806 (2007).

  118. 118.

    et al. Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390, 45–51 (1997).

  119. 119.

    et al. Satellite cell activation in stretched skeletal muscle and the role of nitric oxide and hepatocyte growth factor. Am. J. Physiol. Cell Physiol. 290, C1487–C1494 (2006).

  120. 120.

    , , & Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. Am. J. Physiol. Cell Physiol. 278, C174–C181 (2000).

  121. 121.

    & Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 191, 270–283 (1997).

  122. 122.

    et al. Evolutionary origins of vertebrate appendicular muscle. Nature 408, 82–86 (2000).

  123. 123.

    , , , & Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376, 768–771 (1995).

  124. 124.

    et al. The role of SF/HGF and c-Met in the development of skeletal muscle. Development 126, 1621–1629 (1999).

  125. 125.

    , , , & Pax3 modulates expression of the c-Met receptor during limb muscle development. Proc. Natl Acad. Sci. USA 93, 4213–4218 (1996).

  126. 126.

    et al. The transcriptional activator PAX3–FKHR rescues the defects of Pax3 mutant mice but induces a myogenic gain-of-function phenotype with ligand-independent activation of Met signaling in vivo. Genes Dev. 17, 2950–2965 (2003).

  127. 127.

    et al. N-cadherin is involved in myoblast migration and muscle differentiation in the avian limb bud. Dev. Biol. 178, 160–173 (1996).

  128. 128.

    , , , & Regulation and function of SF/HGF during migration of limb muscle precursor cells in chicken. Dev. Biol. 180, 566–578 (1996).

  129. 129.

    & Early specification of limb muscle precursor cells by the homeobox gene Lbx1h. Nature Genet. 23, 213–216 (1999).

  130. 130.

    , & The role of Lbx1 in migration of muscle precursor cells. Development 127, 437–445 (2000).

  131. 131.

    et al. Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development 127, 413–424 (2000).

  132. 132.

    et al. CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev. 19, 2187–2198 (2005).

  133. 133.

    et al. Inhibitors of CXCR4 affect the migration and fate of CXCR4+ progenitors in the developing limb of chick embryos. Dev. Dyn. 235, 3007–3015 (2006).

  134. 134.

    et al. Intrinsic, Hox-dependent cues determine the fate of skeletal muscle precursors. Dev. Cell 5, 379–390 (2003).

  135. 135.

    et al. Met and Hgf signaling controls hypaxial muscle and lateral line development in the zebrafish. Development 131, 4857–4869 (2004).

  136. 136.

    & A distinct developmental programme for the cranial paraxial mesoderm in the chick embryo. Development 125, 3461–3472 (1998).

  137. 137.

    & Distinct regulatory cascades for head and trunk myogenesis. Development 129, 573–583 (2002).

  138. 138.

    et al. Antagonists of Wnt and BMP signaling promote the formation of vertebrate head muscle. Genes Dev. 17, 3087–3099 (2003).

  139. 139.

    & The molecular setup of the avian head mesoderm and its implication for craniofacial myogenesis. Dev. Dyn. 235, 2845–2860 (2006).

  140. 140.

    & Heartening news for head muscle development. Trends Genet. 8, 365–369 (2007).

  141. 141.

    , & Muscle development: forming the head and trunk muscles. Acta Histochem. 110, 97–108 (2008).

  142. 142.

    & Neural crest and the origin of vertebrates: a new head. Science 220, 268–273 (1983).

  143. 143.

    , , & Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract. Development 133, 1943–1953 (2006).

  144. 144.

    et al. The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development. Development 135, 647–657 (2008).

  145. 145.

    , , & Neural tube derived signals and Fgf8 act antagonistically to specify eye versus mandibular arch muscles. Development 133, 2731–2745 (2006).

  146. 146.

    et al. Cranial neural crest cells regulate head muscle patterning and differentiation during vertebrate embryogenesis. Development 134, 3065–3075 (2007).

  147. 147.

    , , & MyoR: a muscle-restricted basic helix-loop-helix transcription factor that antagonizes the actions of MyoD. Proc. Natl Acad. Sci. USA 96, 552–557 (1999).

  148. 148.

    et al. Control of facial muscle development by MyoR and capsulin. Science 298, 2378–2381 (2002).

  149. 149.

    , & The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum. Mol. Genet. 13, 2829–2840 (2004).

  150. 150.

    et al. Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development 133, 977–87 (2006).

  151. 151.

    et al. Tbx1 regulation of myogenic differentiation in the limb and cranial mesoderm. Dev. Dyn. 236, 353–363 (2007).

  152. 152.

    et al. Pitx2 promotes development of splanchnic mesoderm-derived branchiomeric muscle. Development 133, 4891–4899 (2006).

  153. 153.

    , & Global transcriptional regulation of the locus encoding the skeletal muscle determination genes Mrf4 and Myf5. Genes Dev. 22, 265–276 (2008).

  154. 154.

    et al. Modular long-range regulation of Myf5 reveals unexpected heterogeneity between skeletal muscles in the mouse embryo. Development 127, 4455–4467 (2000).

  155. 155.

    et al. Analysis of a key regulatory region upstream of the Myf5 gene reveals multiple phases of myogenesis, orchestrated at each site by a combination of elements dispersed throughout the locus. Development 130, 3415–3426 (2003).

  156. 156.

    et al. The early epaxial enhancer is essential for the initial expression of the skeletal muscle determination gene Myf5 but not for subsequent, multiple phases of somitic myogenesis. Development 129, 4571–4580 (2002).

  157. 157.

    , & Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15–20 (2005).

  158. 158.

    et al. Essential role for Dicer during skeletal muscle development. Dev. Biol. 311, 359–368 (2007).

  159. 159.

    et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nature Genet. 38, 228–233 (2006). The authors demonstrate a specific role for miRNAs in muscle formation by targeting transcriptional activators and repressors that coordinate muscle formation in X. laevis .

  160. 160.

    , , , & MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. J. Cell Biol. 175, 77–85 (2006).

  161. 161.

    , , , & Muscle-specific microRNA miR-206 promotes muscle differentiation. J. Cell Biol. 174, 677–687 (2006).

  162. 162.

    et al. An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proc. Natl Acad. Sci. USA 104, 20844–20849 (2007).

  163. 163.

    , , , & Myogenic factors that regulate expression of muscle-specific microRNAs. Proc. Natl Acad. Sci. USA 103, 8721–8726 (2006).

  164. 164.

    , , , & Zebrafish miR-214 modulates Hedgehog signaling to specify muscle cell fate. Nature Genet. 39, 259–263 (2007).

  165. 165.

    et al. The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation. Nature Cell Biol. 8, 278–284 (2006).

  166. 166.

    et al. MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2, 219–229 (2008).

  167. 167.

    et al. Myostatin promotes the terminal differentiation of embryonic muscle progenitors. Genes Dev. 22, 668–681 (2008).

  168. 168.

    et al. Pax3 regulation of FGF signaling affects the progression of embryonic progenitor cells into the myogenic program. Genes Dev. 22, 1828–1837 (2008).

Download references

Acknowledgements

We are most grateful to S. Dietrich for her extensive comments on the manuscript and the communication of unpublished data. We would also like to thank R. P. Currie for comments on the manuscript.

Author information

Affiliations

  1. Victor Chang Cardiac Research Institute, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.

    • Robert J. Bryson-Richardson
    •  & Peter D. Currie
  2. School of Medical Sciences, Faculty of Medicine, Wallace Wurth Building, University of New South Wales, Sydney, New South Wales 2052, Australia.  r.bryson-richardson@victorchang.edu.au

    • Robert J. Bryson-Richardson
  3. St Vincent's Clinical School, Faculty of Medicine, University of New South Wales, Level 5, de Lacy Building, Victoria Street, St Vincent's Hospital, Darlinghurst New South Wales 2010, Australia.  p.currie@victorchang.edu.au

    • Peter D. Currie

Authors

  1. Search for Robert J. Bryson-Richardson in:

  2. Search for Peter D. Currie in:

Glossary

Primary myotome

The first differentiated muscle to derive from the dermomyotome.

Satellite cell

Resident stem cell of adult skeletal muscle.

Somite

A metameric division of the vertebrate mesoderm, which gives rise to a number of lineage-restricted cellular compartments, including the dermomyotome.

Paraxial mesoderm

Mesodermal tissue that lies lateral to the notochord and that segments to form the somites.

Dermomyotome

Epithelial layer derived from dorsal division of the amniote somite. It generates a number of different cell types, including the muscles and dermis of the back.

Epaxial

Epaxial muscles generate the muscles of the back in amniotes and are defined by their innervation by the dorsal branch of the spinal nerve.

Hypaxial

Hypaxial muscles derive from the ventro–lateral portion of the dermomyotome. They are innervated by ventral spinal nerves and give rise to body-wall muscles and, at limb level, the appendicular muscle as well as a number of migratory muscle populations such as the diaphragm and hypoglossal chord or tongue.

Lateral plate mesoderm

Mesoderm that is found at the periphery of the embryo, lateral to the paraxial mesoderm.

Fast- and slow-twitch muscle

Fast- and slow-twitch muscles are distinguished by their rate of contraction, which is imparted by the expression of specific myosin isoforms.

Sclerotome

Ventrally located somitic subcompartment that contributes the progenitors of the axial skeleton.

Hyperplasia

The division and proliferation of progenitor cells to increases cell number.

Hypertrophy

Growth produced by an increase in the size of individual cells without an increase in cell number.

About this article

Publication history

Published

DOI

https://doi.org/10.1038/nrg2369

Further reading