The Origin and Genetic Regulation of Myogenic Cells: From the Embryo to the Adult

  • Margaret Buckingham
  • Didier Montarras
Part of the Advances in Muscle Research book series (ADMR, volume 3)


Satellite Cell Myogenic Cell Muscle Satellite Cell Myogenic Regulatory Factor Muscle Progenitor Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Armand O, Boutineau AM, Mauger A, Pautou MP, Kieny M (1983) Origin of satellite cells in avian skeletal muscles. Arch Anat Microsc Morphol Exp 72:163–181PubMedGoogle Scholar
  2. Asakura A, Lyons GE, Tapscott, SJ (1995) The regulation of MyoD gene expression: conserved elements mediate expression in embryonic axial muscle. Dev Biol 171:386–398PubMedGoogle Scholar
  3. Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA (2002) Myogenic specification of side population cells in skeletal muscle. J Cell Biol 159:123–134PubMedGoogle Scholar
  4. Bajanca F, Luz M, Raymond K, Martins GG, Sonnenberg A, Tajbakhsh S, Buckingham M, Thorsteinsdottir S (2006) Integrin alpha6beta1-laminin interactions regulate early myotome formation in the mouse embryo. Development 133:1635–1644PubMedGoogle Scholar
  5. Bajard L, Relaix F, Lagha M, Rocancourt D, Daubas P, Buckingham ME (2006) A distinct genetic hierarchy controls hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes & Dev 20:2450–2464Google Scholar
  6. Barr FG (2001) Gene fusions involving PAX and FOX family members in alveolar rhabdomyosarcoma. Oncogene 20:5736–5746PubMedGoogle Scholar
  7. Beauchamp JR, Heslop L, Yu DSW, Kelly RG, Tajbakhsh T, Buckingham ME, Partridge TA, Zammit PS (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221–1233PubMedGoogle Scholar
  8. Ben-Yair R, Kalcheim C (2005) Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates. Development 132:689–701PubMedGoogle Scholar
  9. Bergstrom DA, Tapscott SJ (2001) Molecular distinction between specification and differentiation in the myogenic basic helix-loop-helix transcription factor family. Mol Cell Biol 21:2404–2412PubMedGoogle Scholar
  10. Birchmeier C, Brohmann H (2000) Genes that control the development of migrating muscle precursor cells. Curr Opin Cell Biol 12:725–730PubMedGoogle Scholar
  11. Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C (1995) Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376:768–771PubMedGoogle Scholar
  12. Blau H, Chiu C-P, Webster C (1983) Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell 32:1171–1180PubMedGoogle Scholar
  13. Borello U, Berarducci B, Murphy P, Bajard L, Buffa V, Piccolo S, Buckingham M, Cossu G (2006) The Wnt/β-catenin pathway regulates the Shh-mediated Myf5 activation during somitogenesis. Development 133:3723–3732PubMedGoogle Scholar
  14. Borue X, Noden DM (2004) Normal and aberrant craniofacial myogenesis by grafted trunk somitic and segmental plate mesoderm. Development 131:3967–3980PubMedGoogle Scholar
  15. Borycki AG, Li J, Jin F, Emerson CP, Epstein JA (1999) Pax3 functions in cell survival and in Pax7 regulation. Development 126:1665–1674PubMedGoogle Scholar
  16. Braun T, Rudnicki MA, Arnold HH, Jaenisch R (1992) Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71:369–382PubMedGoogle Scholar
  17. Brent AE, Schweitzer R, Tabin CJ (2003) A somitic compartment of tendon progenitors. Cell 113: 235–248PubMedGoogle Scholar
  18. Brown CB, Engleka KA, Wenning J, Lu MM, Epstein JA (2005) Identification of a hypaxial somite enhancer element regulating Pax3 expression in migrating myoblasts and characterization of hypaxial muscle Cre transgenic mice. Genesis 41:202–209PubMedGoogle Scholar
  19. Brunelli S, Relaix F, Baesso S, Buckingham M, Cossu G (2007) Beta catenin-independent activation of MyoD by Wnt7a requires PKC and depends on Pax3 transcriptional activity. Dev Biol. 304:604–614Google Scholar
  20. Buchberger A, Nomokonova N, Arnold HH (2003) Myf5 expression in somites and limb buds of mouse embryos is controlled by two distinct distal enhancer activities. Development 130, 3297–3307Google Scholar
  21. Buckingham M (1994) Which myogenic factors make muscle? Curr Biol 4(1):61–63PubMedGoogle Scholar
  22. Buckingham M, Tajbakhsh S (1999) Myogenic cell specification during somitogenesis. In: Moody SA (ed) Cell lineage and fate determination. Academic Press, Chapter 41, pp 617–633Google Scholar
  23. Buckingham M (2006) Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr Opin Genet Dev 16:525–532PubMedGoogle Scholar
  24. Buckingham M, Relaix F (2007) The role of Pax genes in the deveopment of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Ann. Rev. Cell Dev. Biol. 23:645–673.Google Scholar
  25. Busslinger M (2004) Transcriptional control of early B cell development. Annu Rev Immunol 22:55–79PubMedGoogle Scholar
  26. Carvajal JJ, Cox D, Summerbell D, Rigby PW (2001) A BAC transgenic analysis of the Mrf4/Myf5 locus reveals interdigitated elements that control activation and maintenance of gene expression during muscle development. Development 128:1857–1868PubMedGoogle Scholar
  27. Chang TH-T, Primig M, Hadchouel J, Tajbakhsh, S, Rocancourt D, Fernandez A, Kappler R, Scherthan H, Buckingham M. (2004) An enhancer directs differential expression of the linked Mrf4 and Myf5 myogenic regulatory genes in the mouse. Dev Biol 269:595–608PubMedGoogle Scholar
  28. Chang TH-T, Vincent SD, Buckingham ME, Zammit PS. (2007) The A17 enhancer directs expression of Myf5 to satellite cells but Myf4 to myonudei. Dev. Dynamics 236, in pressGoogle Scholar
  29. Cheng TC, Wallace MC, Merlie JP, Olson EN (1993) Separable regulatory elements governing myogenin transcription in mouse embryogenesis. Science 261:215–218PubMedGoogle Scholar
  30. Chen Y, Lin G, Slack JMW (2006) Control of muscle regeneration in the Xenopus tadpole tail by Pax7. Development 133:2303–2313PubMedGoogle Scholar
  31. Choi J, Costa ML, Mermelstein CS, Chagas C, Holtzer S (1990) MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. Proc Natl Acad Sci USA 87:7988–7992PubMedGoogle Scholar
  32. Cinnamon Y, Ben-Yair R, Kalcheim C (2006) Differential effects of N-cadherin-mediated adhesion on the development of myotomal waves. Development 133:1101–1112PubMedGoogle Scholar
  33. Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, Morgan JE (2005) Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122:289–301PubMedGoogle Scholar
  34. Conboy IM, Rando TA (2002) The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 3:397–409PubMedGoogle Scholar
  35. Conboy IM, Conboy MJ, Smythe GM, Rando TA (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science 302:1575–1577PubMedGoogle Scholar
  36. Cornelison DD, Olwin BB, Rudnicki MA, Wold BJ (2000) MyoD(-/-) satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev Biol 224:122–137PubMedGoogle Scholar
  37. Cossu G, Kelly R, Di Donna S, Vivarelli E, Buckingham M (1995) Myoblast differentiation during mammalian somitogenesis is dependent upon a community effect. Proc Natl Acad Sci USA 92: 2254–2258PubMedGoogle Scholar
  38. Cossu G, Kelly R, Tajbakhsh S, Di Donna S, Vivarelli E, Buckingham M. (1996) Activation of different myogenic pathways: myf-5 is induced by the neural tube and MyoD by the dorsal ectoderm in mouse paraxial mesoderm. Development 122:429–437PubMedGoogle Scholar
  39. Cusella-De Angelis MG, Lyons G, Sonnino C, De Angelis L, Vivarelli E, Farmer K, Wright WE, Molinaro M, Bouche M, Buckingham M et al. (1992) MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites. J Cell Biol 116:1243–1255PubMedGoogle Scholar
  40. Davis RL, Weintraub H, Lassar AB (1987) Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51:987–1000PubMedGoogle Scholar
  41. Dietrich S, Abou-Rebyeh F, Brohmann H, Bladt F, Sonnenberg-Riethmacher E, Yamaai T, Lumsden A, Brand-Saberi B, Birchmeier C (1999) The role of SF/HGF and c-Met in the development of skeletal muscle. Development 126:1621–1629PubMedGoogle Scholar
  42. Epstein JA, Shapiro DN, Cheng J, Lam PY, Maas RL (1996) Pax3 modulates expression of the c-Met receptor during limb muscle development. Proc Natl Acad Sci USA 93:4213–4218PubMedGoogle Scholar
  43. Esner M, Meilhac SM, Relaix F, Nicolas J-F, Cossu G, Buckingham ME (2006) Smooth muscle of the dorsal aorta shares a common clonal origin with skeletal muscle of the myotome: a model for precursor cell migration from the somite. Development 133:737–749PubMedGoogle Scholar
  44. Fan CM, Lee CS, Tessier-Lavigne M (1997) A role for WNT proteins in induction of dermomyotome. Dev Biol 191:160–165PubMedGoogle Scholar
  45. Fomin M, Nomokonova N, Arnold HH (2004) Identification of a critical control element directing expression of the muscle-specific transcription factor MRF4 in the mouse embryo. Dev Biol 272:498–509PubMedGoogle Scholar
  46. Geetha-Loganathan P, Nimmagadda S, Prols F, Patel K, Scaal M, Huan R, Christ B (2005) Ectodermal Wnt-6 promotes Myf5-dependent avian limb myogenesis. Dev Biol 288:221–233PubMedGoogle Scholar
  47. Gerber AN, Klesert TR, Bergstrom DA, Tapscott SJ (1997) Two domains of MyoD mediate transcriptional activation of genes in repressive chromatin: a mechanism for lineage determination in myogenesis. Genes Dev 11:436–450PubMedGoogle Scholar
  48. Giordani J, Bajard L, Demignon J, Buckingham M, Maire P (2007) Six proteins regulate the activation of Myf5 expression in embryonic mouse limbs. PNAS 104:11310–11315PubMedGoogle Scholar
  49. Goldhamer DJ, Brunk BP, Faerman A, King A, Shani M, Emerson CP Jr (1995) Embryonic activation of the myoD gene is regulated by a highly conserved distal control element. Development 121:637–649PubMedGoogle Scholar
  50. Grifone R, Laclef C, Spitz F, Lopez S, Demignon J, Guidotti JE, Kawakami K, Xu PX, Kelly R, Petrof BJ, Daegelen D, Concordet JP, Maire P (2004) Six1 and Eya1 expression can reprogram adult muscle from the slow-twitch phenotype into the fast-twitch phenotype. Mol Cell Biol 24:6253–6267PubMedGoogle Scholar
  51. Grifone R, Demignon J, Houbron C, Souil E, Niro C, Seller MJ, Hamard G, Maire P (2005) Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development 132:2235–2249PubMedGoogle Scholar
  52. Gros J, Scaal M, Marcelle C (2004) A two-step mechanism for myotome formation in chick. Dev Cell 6:875–882PubMedGoogle Scholar
  53. Gros J, Manceau M, Thome V, Marcelle C (2005) A common somitic origin for embyronic muscle progenitors and satellite cells. Nature 435:954–958PubMedGoogle Scholar
  54. Gustafsson MK, Pan H, Pinney DF, Liu Y, Lewandowski A, Epstein DJ, Emerson CP Jr (2002) Myf5 is a direct target of long-range shh signaling and Gli regulation for muscle specification. Genes Dev 16:114–126PubMedGoogle Scholar
  55. Gussoni E, Soneoka Y, Strickland CD, Buzney EA, Khan MK, Flint AF, Kunkel LM, Mulligan RC (1999) Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401: 390–394PubMedGoogle Scholar
  56. Hadchouel J, Tajbakhsh S, Primig M, Chang THT, Daubas P, Rocancourt D, Buckingham M (2000) Modular long-range regulation of Myf5 reveals unexpected heterogeneity between skeletal muscles in the mouse embryo. Development 127:4455–4467PubMedGoogle Scholar
  57. Hadchouel J, Carvajal JJ, Daubas P, Bajard L, Chang T, Rocancourt D, Cox D, Summerbell D, Tajbakhsh S, Rigby PWJ, Buckingham M (2003) 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 130:3415–3426PubMedGoogle Scholar
  58. Hasty P, Bradley A, Morris JH, Edmondson DG, Venuti JM, Olson EN, Klein WH (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364:501–506PubMedGoogle Scholar
  59. Horst D, Ustanina S, Sergi C, Mikuz G, Juergens H, Braun T, Vorobyov E (2006) Comparative expression analysis of Pax3 and Pax7 during mouse myogenesis. Int J Dev Biol 50:47–54PubMedGoogle Scholar
  60. Inanlou MR, Dhillon GS, Belliveau AC, Reid AM, Ying C, Rudnicki MA, Kablar B (2003) A significant reduction of the diaphragm in mdx: MyoD-/- 9th embryos suggests a role for MyoD in the diaphragm development. Dev. Biol 261:324–336PubMedGoogle Scholar
  61. Kablar B, Krastel K, Ying C, Tapscott SJ, Goldhamer DJ, Rudnicki MA (1999) Myogenic determination occurs independently in somites and limb buds. Dev. Biol 206:219–231PubMedGoogle Scholar
  62. Kalcheim C, Ben-Yair R (2005) Cell rearrangements during development of the somite and its derivatives. Curr Opin Genet Dev 15:371–380PubMedGoogle Scholar
  63. Kardon G, Campbell JK, Tabin CJ (2002) Local extrinsic signals determine muscle and endothelial cell fate and patterning in the vertebrate limb. Dev Cell 3:533–545PubMedGoogle Scholar
  64. Kassar-Duchossoy L, Gayraud-Morel B, Gomès D, Rocancourt D, Buckingham M, Shinin V, Tajbakhsh S (2004) Mrf4 directs skeletal muscle indentity in Myf5: MyoD double mutant mice. Nature 431: 466–471PubMedGoogle Scholar
  65. Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomes D, Tajbakhsh S (2005) Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev 19:1426–1431PubMedGoogle Scholar
  66. Kaul A, Köster M, Neuhaus 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 102:17–19PubMedGoogle Scholar
  67. Kelly RG, Jerome-Majewska LA, Papaioannou VE (2004) The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum Mol Genet 13:2829–2840PubMedGoogle Scholar
  68. Kitamura K, Miura H, Miyagawa-Tomita S, Yanazawa M, Katoh-Fukui Y, Suzuki R, Ohuchi H, Suehiro A, Motegi Y, Nakahara Y, Kondo S, Yokoyama M (1999) Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism. Development 126:5749–5758PubMedGoogle Scholar
  69. Knapp JR, Davie JK, Myer A, Meadows E, Olson EN, Klein WH (2006) Loss of myogenin in postnatal life leads to normal skeletal muscle but reduced body size. Development 133:601–610PubMedGoogle Scholar
  70. Konieczny SF, Emerson SP Jr (1984) 5-Azacytidine induction of stable mesodermal stem cell lineages from 10T1/2 cells: evidence for regularoty genes controlling determination. Cell 38:791–800PubMedGoogle Scholar
  71. Kuang S, Charge SB, Seale P, Huh M, Rudnicki MA (2006) Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J. Cell Biol 172:103–113PubMedGoogle Scholar
  72. Laclef C, Hamard G, Demignon J, Souil E, Houbron C, Maire P (2003) Altered myogenesis in Six1-deficient mice. Development 130:2239–2252PubMedGoogle Scholar
  73. Lassar AB, Paterson BM, Weintraub H (1986) Transfection of a DNA locus that mediates the conversion of 10T1/2 fibroblasts to myoblasts. Cell 47:649–656PubMedGoogle Scholar
  74. Lu J-R, Bassel-Duby R, Hawkins A, Chang P, Valdez R, Wu H, Gan L, Shelton JM, Richardson JA, Olson EN (2002) Control of facial muscle development by MyoR and Capsulin. Science 298:2378–2381PubMedGoogle Scholar
  75. Mankoo BS, Collins NS, Ashby P, Grigorieva E, Pevny LH, Candia A, Wright CV, Rigby PW, Pachnis V (1999) Mox2 is a component of the genetic hierarchy controlling limb muscle development. Nature 400:69–73PubMedGoogle Scholar
  76. Mansouri A, Stoykova A, Torres M, Gruss P (1996) Dysgenesis of cephalic neural crest derivatives in Pax7-/- mutant mice. Development 122:831–838PubMedGoogle Scholar
  77. McDermott A, Gustafsson M, Elsam T, Hui CC, Emerson CP Jr, Borycki AG (2005) Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation. Development 132:345–357PubMedGoogle Scholar
  78. McLoon LK, Rowe J, Wirtschafter J, McCormick KM (2004) Continuous myofiber remodeling in uninjured extraocular myofibers: myonuclear turnover and evidence for apoptosis. Muscle Nerve 29:707–715PubMedGoogle Scholar
  79. Megeney LA, Kablar B, Garrett K, Anderson JE, Rudnicki, MA (1996) MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes & Dev 10:1173–1183Google Scholar
  80. Minasi MG, Riminucci M, De Angelis L, Borello U, Berarducci B, Innocenzi A, Caprioli A, Sirabella D, Baiocchi M, De Maria R, Boratto R, Jaffredo T, Broccoli V, Bianco P, Cossu G (2002) The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129:2773–2783PubMedGoogle Scholar
  81. Montarras D, Lindon C, Pinset C, Domeyne P (2000) Cultured myf5 null and myoD null muscle precursor cells display distinct growth defects. Biol. Cell 92:565–572PubMedGoogle Scholar
  82. Montarras D, Morgan J, Collins C, Relaix F, Cumano A, Partridge T, Buckingham M (2005) Direct isolation of muscle satellite cells demonstrates their major role in skeletal muscle self renewal. Science 309:2064–2067PubMedGoogle Scholar
  83. Morrison GM, Brickman JM (2006) Conserved roles for Oct4 homologues in maintaining multipotency during early vertebrate development. Development 133:2011–2022PubMedGoogle Scholar
  84. Nabeshima Y, Hanaoka K, Hayasaka M, Esumi E, Li S, Nonaka I, Nabeshima Y (1993) Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364:532–535PubMedGoogle Scholar
  85. Noden DM, Francis-West P (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:1194–1218PubMedGoogle Scholar
  86. Olguin HC, Olwin BB (2004) Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev Biol 275:375–388PubMedGoogle Scholar
  87. Olson E, Arnold HH, Rigby PWJ, Wold BJ (1996) Know your neighbours: three phenotypes in null mutants of the myogenic bHLH gene Mrf4. Cell 85:1–4PubMedGoogle Scholar
  88. Ontell M, Kozeka K (1984) Organogenesis of the mouse extensor digitorum logus muscle: a quantitative study. Am J Anat 171:149–161PubMedGoogle Scholar
  89. Oustanina S, Hause G, Braun T (2004) Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J 23:3430–3439PubMedGoogle Scholar
  90. Pardanaud L, Luton D, Prigent M, Bourcheix LM, Catala M, Dieterlen-Lievre F (1996) Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. Development 122:1363–1371PubMedGoogle Scholar
  91. Pin CL, Ludolph DC, Cooper ST, Klocke BJ, Merlie JP, Konieczny, SF (1997) Distal regulatory elements control MRF4 gene expression in early and late myogenic cell populations. Dev Dyn 208:299–312PubMedGoogle Scholar
  92. Pin CL, Konieczny, SF (2002) A fast fiber enhancer exists in the muscle regulatory factor 4 gene promoter. Biochem Biophys Res Commun 299:7–13PubMedGoogle Scholar
  93. Porter JD, Khanna S, Kaminski HJ, Rao JS, Merriam AP, Richmonds CR, Leahy P, Li J, Andrade FH (2001) Extraocular muscle is defined by a fundamentally distinct gene expression profile. Proc Natl Acad Sci USA 98:12062–12067PubMedGoogle Scholar
  94. Porter JD, Merriam AP, Khanna S, Andrade FH, Richmonds CR, Leahy P, Cheng G, Karathanasis P, Zhou X, Kusner LL, Adams ME, Willem M, Mayer U, Kaminski HJ (2003) Constitutive properties, not molecular adaptations, mediate extraocular muscle sparing in dystrophic mdx mice. FASEB J 17:893–895PubMedGoogle Scholar
  95. Pouget C, Gautier R, Teillet MA, Jaffredo T (2006) Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk. Development 133:1013–1022PubMedGoogle Scholar
  96. Rawls A, Valdez MR, Zhang W, Richardson J, Klein WH, Olson EN (1998) Overlapping functions of the myogenic bHLH genes MRF4 and MyoD revealed in double mutant mice. Development 125:2349–2358PubMedGoogle Scholar
  97. Relaix F, Buckingham M (1999) From insect eye to vertebrate muscle: redeployment of a regulatory network. Genes & Dev 13:3171–3178Google Scholar
  98. Relaix F, Polimeni M, Rocancourt D, Ponzetto C, Schäfer BW, Buckingham M (2003) The transcriptional activator PAX3-FKHR rescues the Pax3 mutant phenotype and induces a gain of function phenotype with ligand-independent activation of Met signaling. Genes & Dev 17:2950–2965Google Scholar
  99. Relaix F, Rocancourt D, Mansouri M, Buckingham M. (2004) Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes and Dev 18:1088–1105PubMedGoogle Scholar
  100. Relaix F, Rocancourt D, Mansouri A, Buckingham MA (2005) A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435:948–953PubMedGoogle Scholar
  101. Relaix F, Montarras D, Zaffran S, Gayraud-Morel B, Rocancourt D, Tajbakhsh S, Mansouri A, Cumano A, Buckingham M (2006) Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J Cell Biol 172:91–102PubMedGoogle Scholar
  102. Rose O, Rohwedel J, Reinhardt S, Bachmann M, Cramer M, Rotter M, Wobus A, Starzinski-Powitz A. (1994) Expression of M-cadherin protein in myogenic cells during prenatal mouse development and differentiation of embryonic stem cells in culture. Dev Dyn 201:245–259PubMedGoogle Scholar
  103. Rudnicki MA, Braun T, Hinuma S, Jaenisch R (1992) Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71:383–390PubMedGoogle Scholar
  104. Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, Jaenisch R (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75:1351–1359PubMedGoogle Scholar
  105. Sabourin LA, Girgis-Gabardo A, Seale P, Asakura A, Rudnicki MA (1999) Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle. J Cell Biol 144:631–643PubMedGoogle Scholar
  106. Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D’Antona G, Pellegrino MA, Barresi R, Bresolin N, De Angelis MG, Campbell KP, Bottinelli R, Cossu G (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301:487–492PubMedGoogle Scholar
  107. Sampaolesi M, Blot S, D’Antona G, Granger N, Tonlorenzi R, Innocenzi A, Mognol P, Thibaud JL, Galvez BG, Barthelemy I, Perani L, Mantero S, Guttinger M, Pansarasa O, Rinaldi C, Cusella De Angelis MG, Torrente Y, Bordignon C, Bottinelli R, Cossu G (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444:574–579PubMedGoogle Scholar
  108. Schienda J, Engleka KA, Jun S, Hansen MS, Epstein JA, Tabin CJ, Kunkel LM, Kardon G (2006) Somitic origin of limb muscle satellite cell and side population cells. Proc Natl Acad Sci USA 103:945–950PubMedGoogle Scholar
  109. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786PubMedGoogle Scholar
  110. Shen H, McElhinny AS, Cao Y, Gao P, Liu J, Bronson R, Griffin JD, Wu L (2006) The Notch coactivator, MAML1, functions as a novel coactivator for MEF2-C-mediated transcription and is required for normal myogenesis. Genes Dev 20:675–688PubMedGoogle Scholar
  111. Shinin V, Gayraud-Morel B, Gomes D, Tabjakhsh S (2006) Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8:677–687PubMedGoogle Scholar
  112. Spitz F, Demignon J, Porteu A, Kahn A, Concordet J-P, Daegelen D, Maire P (1998) Expression of myogenin during embryogenesis is controlled by Six/sine oculis homeoproteins through a conserved MEF3 binding site. Proc Natl Acad Sci USA 95:14220–14225PubMedGoogle Scholar
  113. Summerbell D, Ashby PR, Coutelle O, Cox D, Yee S, Rigby PW (2000) The expression of Myf5 in the developing mouse embryo is controlled by discrete and dispersed enhancers specific for particular populations of skeletal muscle precursors. Development 127:3745–3757PubMedGoogle Scholar
  114. Summerbell D, Halai C, Rigby PW (2002) Expression of the myogenic regulatory factor Mrf4 precedes or is contemporaenous with that of Myf5 in the somitic bud. Mech. Dev 117:331–335PubMedGoogle Scholar
  115. Tajbakhsh S, Buckingham ME (1994) Mouse limb muscle is determined in the absence of the earliest myogenic factor myf-5. Proc Natl Acad Sci USA 91:747–751PubMedGoogle Scholar
  116. Tajbakhsh S, Rocancourt D, Buckingham M (1996a) Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice. Nature 384:266–270Google Scholar
  117. Tajbakhsh S, Bober E, Babinet C, Pournin S, Arnold H, Buckingham M (1996b) Gene targeting the myf-5 locus with nlacZ reveals expression of this myogenic factor in mature skeletal muscle fibres as well as early embryonic muscle. Dev Dynamics 206:291–300Google Scholar
  118. Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M (1997) Redefining the genetic hierarchies controling skeletal myogenesis: Pax3 and Myf-5 act upstream of MyoD. Cell 89:127–138PubMedGoogle Scholar
  119. Tajbakhsh S, Borello U, Vivarelli E, Kelly R, Papkoff J, Duprez D, Buckingham M, Cossu G (1998) 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 125:4155–4162PubMedGoogle Scholar
  120. Tajbakhsh S, Buckingham M (2000) The birth of muscle progenitor cells in the mouse: spatiotemporal considerations. In: Ordahl CP (ed) Current topics in developmental biology: Somitogenesis, vol. 47. Academic Press, pp 225–268Google Scholar
  121. Tapscott SJ (2005) The circuitry of a master switch: MyoD and the regulation of skeletal muscle gene transcription. Development 132:2685–2695PubMedGoogle Scholar
  122. Teboul L, Hadchouel J, Daubas P, Summerbell D, Buckingham M, Rigby PWJ (2002) The early epaxial enhancer of Myf5 is essential for the initial transcription of this myogenic determination gene in the somite but not for subsequent expression in the myotome. Development 129:4571–4580PubMedGoogle Scholar
  123. Teboul L, Summerbell D, Rigby PW (2003) The initial somitic phase of Myf5 expression requires neither Shh signaling nor Gli regulation. Genes Dev 17:2870–2874PubMedGoogle Scholar
  124. Thompson AL, Filatov G, Chen C, Porter I, Li Y, Rich MM, Kraner SD (2005) A selective role for MRF4 ininnervated adult skeletal muscle: Na(V) 1.4 Na+ channel expression is reduced in MRF4-null mice. Gene Expr 12:289–303PubMedGoogle Scholar
  125. Tzahor E, Kempf H, Mootoosamy RC, Poon AC, Abzhanov A, Tabin CJ, Dietrich S, Lassar AB (2003) Antagonists of Wnt and BMP signaling promote the formation of vertebrate head muscle. Genes Dev 17:3087–3099PubMedGoogle Scholar
  126. Vasyutina E, Stebler J, Brand-Saberi B, Schulz S, Raz E, Birchmeier C (2005) CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev 19:2187–2198PubMedGoogle Scholar
  127. Venuti JM, Morris JH, Vivian JL, Olson EN, Klein, WH (1995) Myogenin is required for late but not early aspects of myogenesis during mouse development. J Cell Biol 128:563–576PubMedGoogle Scholar
  128. Vivian JL, Gan L, Olson EN, Klein WH (1999) A hypomorphic myogenin allele reveals distinct myogenin expression levels required for viability, skeletal muscle development and sternum formation. Dev Biol 208:44–55PubMedGoogle Scholar
  129. Vivian JL, Olson EN, Klein WH (2000) Thoracic skeletal defects in myogenin- and MRF4-deficient mice correlate with early defects in myotome and intercostal musculature. Dev Biol 224:29–41PubMedGoogle Scholar
  130. Vorobyov E, Horst J (2004) Expression of two protein isoforms of PAX7 is controlled by competing cleavage-polyadenylation and splicing. Gene 342:107–112PubMedGoogle Scholar
  131. Wang ZZ, Washabaugh CH, Yao Y, Wang JM, Zhang L, Ontell MP, Watkins SC, Rudnicki MA, Ontell, M (2003) Aberrant development of motor axons and neuromuscular synapses in MyoD-null mice. J Neurosci 23:5161–5169PubMedGoogle Scholar
  132. Weintraub H, Davis R, Tapscott S, Thayer M, Krause M, Benezra R, Blackwell TK, Turner D, Rupp R, Hollenberg S et al (1991) The MyoD gene family: nodal point during specification of the muscle cell lineage. Science 251:761–766PubMedGoogle Scholar
  133. Wright WE (1984) Induction of muscle genes in neural cells. J Cell Biol 98:427–435PubMedGoogle Scholar
  134. Wright WE, Sassoon DA, Lin VK (1989) Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56:607–617PubMedGoogle Scholar
  135. Yablonka-Reuveni Z, Rudnicki MA, Rivera AJ, Primig M, Anderson JE, Natanson P (1999) The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD. Dev Biol 210:440–455PubMedGoogle Scholar
  136. Yee SP, Rigby PW (1993) The regulation of myogenin gene expression during the embryonic development of the mouse. Genes & Dev 7:1277–1289Google Scholar
  137. Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR (2004a) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166:347–357Google Scholar
  138. Zammit PS, Carvajal JJ, Golding JP, Morgan JE, Summerbell D, Zolnerciks J, Partridge TA, Rigby PW, Beauchamp JR (2004b) Myf5 expression in satellite cells and spindles in adult muscle is controlled by separate genetic elements. Dev Biol 273:454–465Google Scholar
  139. Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, Partridge TA, Beauchamp JR (2006) Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119:1824–1832PubMedGoogle Scholar
  140. Zhao P, Caretti G, Mitchell S, McKeehan WL, Boskey AL, Pachman LM, Sartorelli V, Hoffman EP (2006) Fgfr4 is required for effective muscle regeneration in vivo. Delineation of a MyoD-Tead2-Fgfr4 transcriptional pathway. J Biol Chem 281:429–438PubMedGoogle Scholar
  141. Zhou Z, Bornemann A (2001) MRF4 protein expression in regenerating rat muscle. J Muscle Res Cell Motil 22:311–316PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Margaret Buckingham
    • 1
  • Didier Montarras
    • 1
  1. 1.Département de Biologie du DéveloppementCNRS URA 2578, Institut Pasteur75015 ParisFrance

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