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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
S. Tajbakhsh, U. Borello, E. Vivarelli, R. Kelly, J. Papkoff, D. Duprez, M. Buckingham, G. Cossu
Development 1998 125: 4155-4162;

Summary

Activation of myogenesis in newly formed somites is dependent upon signals derived from neighboring tissues, namely axial structures (neural tube and notochord) and dorsal ectoderm. In explants of paraxial mesoderm from mouse embryos, axial structures preferentially activate myogenesis through a Myf5-dependent pathway and dorsal ectoderm preferentially through a MyoD-dependent pathway. Here we report that cells expressing Wnt1 will preferentially activate Myf5 while cells expressing Wnt7a will preferentially activate MyoD. Wnt1 is expressed in the dorsal neural tube and Wnt7a in dorsal ectoderm in the early embryo, therefore both can potentially act in vivo to activate Myf5 and MyoD, respectively. Wnt4, Wnt5a and Wnt6 exert an intermediate effect activating both Myf5 and MyoD equivalently in paraxial mesoderm. Sonic Hedgehog synergises with both Wnt1 and Wnt7a in explants from E8.5 paraxial mesoderm but not in explants from E9.5 embryos. Signaling through different myogenic pathways may explain the rescue of muscle formation in Myf5 null embryos, which do not form an early myotome but later develop both epaxial and hypaxial musculature. Explants of unsegmented paraxial mesoderm contain myogenic precursors capable of expressing MyoD in response to signaling from a neural tube isolated from E10.5 embryos, the developmental stage when MyoD is present throughout the embryo. Myogenic cells cannot activate MyoD in response to signaling from a less mature neural tube. Together these data suggest that different Wnt molecules can activate myogenesis through different pathways such that commitment of myogenic precursors is precisely regulated in space and time to achieve the correct pattern of skeletal muscle development.

REFERENCES

    1. Banhot P.,
    2. Brink M.,
    3. Samos C. H.,
    4. Hsieh J. C.,
    5. Wang Y.,
    6. Macke J. P.,
    7. Andrew D.,
    8. Nathans J.,
    9. Nusse R.
    (1996) A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382, 225–230
    OpenUrlCrossRefPubMedWeb of Science
    1. Bader D.,
    2. Masaki T.,
    3. Fischman D. A.
    (1982) Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol 95, 763–770
    OpenUrlAbstract/FREE Full Text
    1. Borycki A. G.,
    2. Mendham L.,
    3. Emerson C. P.
    (1998) Control of somite patterning by sonic hedgehog and its downstream signal response genes. Development 125, 777–790
    OpenUrlAbstract
    1. Braun T.,
    2. Rudnicki M. A.,
    3. Arnold H. H.,
    4. Jaenisch R.
    (1992) Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71, 369–82
    OpenUrlCrossRefPubMedWeb of Science
    1. Buckingham M.
    (1992) Making muscle in mammals. Trends Genet 8, 144–149
    OpenUrlCrossRefPubMedWeb of Science
    1. Cadigan K. M.,
    2. Nusse R.
    (1997) Wnt signaling: a common theme in animal development. Genes Dev 11, 3286–3305
    OpenUrlFREE Full Text
    1. Christ B.,
    2. Ordahl C. P.
    (1995) Early stages of chick somite development. Anat. Embryol 11, 3286–3305
    OpenUrl
    1. Cossu G.,
    2. Kelly R.,
    3. Di Donna S.,
    4. Vivarelli E.,
    5. Buckingham M.
    (1995) Myoblast differentiation during mammalian somitogenesis is dependent upon a community effect. Proc. Natl. Acad. Sci. USA 92, 2254–2258
    OpenUrlAbstract/FREE Full Text
    1. Cossu G.,
    2. Tajbakhsh S.,
    3. Buckingham M.
    (1996) How is myogenesis initiated in the embryo?. Trends Genet 12, 218–223
    OpenUrlCrossRefPubMedWeb of Science
    1. Cossu G.,
    2. Kelly R.,
    3. Tajbakhsh S.,
    4. Di Donna S.,
    5. Vivarelli E.M.,
    6. Buckingham M.
    (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
    OpenUrlAbstract
    1. Cusella-De Angelis M. G.,
    2. Molinari S.,
    3. Ledonne A.,
    4. Coletta M.,
    5. Vivarelli E.,
    6. Bouche M.,
    7. Molinaro M.,
    8. Ferrari S.,
    9. Cossu G.
    (1994) Differential response of embryonic and fetal myoblasts to TGF: a possible regulatory mechanism of skeletal muscle histogenesis. Development 120, 925–933
    OpenUrlAbstract
    1. Denetclaw W. F.,
    2. Christ B.,
    3. Ordahl C. P.
    (1997) Location and growth of epaxial myotome precursor cells. Development 124, 1601–1610
    OpenUrlAbstract
    1. Duprez D.,
    2. Fournier-Thibault C.,
    3. Le Douarin N.
    (1998) Sonic Hedgehog induces proliferation of committed myoblasts in the chick limb. Development 125, 495–505
    OpenUrlAbstract
    1. Fan C. M.,
    2. 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
    OpenUrlCrossRefPubMedWeb of Science
    1. Fan C. M.,
    2. Tessier-Lavigne M.
    (1997) A role for Wnt proteins in induction of dermomyotome. Dev. Biol 197, 160–165
    1. Gamel A. J.,
    2. Brand-Saberi B.,
    3. Christ B.,
    4. Wilting J.
    (1996) Halves of epithelial somites and segmental plate show distinct muscle differentiation behavior in vitro compared to entire somites and segmental plate. Dev. Biol 172, 625–639
    1. George-Weinstein M.,
    2. Gerhart J.,
    3. Flynn J.,
    4. Callihan B. A.,
    5. Miehle C.,
    6. Foti G. J.,
    7. Lash J. W.
    (1996) Independence of chick embryo myogenesis from gastrulation, tissue interaction and replication. Dev. Biol 173, 729–741
    OpenUrl
    1. Hirsinger E.,
    2. Duprez D.,
    3. Jouve C.,
    4. Malapert P.,
    5. Cooke J.,
    6. Pourquie O.
    (1997) Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP4 in avian somite patterning. Development 124, 4605–4614
    OpenUrlAbstract
    1. Kablar B.,
    2. Krastel K.,
    3. Ying C.,
    4. Asakura A.,
    5. Tapscott S. J.,
    6. Rudnicki M. A.
    (1997) MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development 124, 4729–4738
    OpenUrlAbstract
    1. Kelly R.,
    2. Alonso S.,
    3. Tajbakhsh S.,
    4. Cossu G.,
    5. Buckingham M.
    (1995) Myosin light chain 3F regulatory sequences confer regionalised cardiac and skeletal muscle expression in transgenic mice. J. Cell Biol 129, 383–396
    OpenUrlAbstract/FREE Full Text
    1. Kenny-Mobbs T.,
    2. Thorogood P.
    (1987) Autonomy of differentiation in avian brachial somites and the influences of adjacent tissues. Development 100, 449–462
    OpenUrlAbstract
    1. Koishi K.,
    2. Zhang M.,
    3. McLennan I. S.,
    4. Harris A. J.
    (1995) MyoD protein accumulates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers. Dev. Dyn 202, 244–254
    OpenUrlPubMedWeb of Science
    1. Leyns L.,
    2. Bouwmeester T.,
    3. Kim S.-H.,
    4. Piccolo S.,
    5. De Robertis E. M.
    (1997) Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88, 747–756
    OpenUrlCrossRefPubMedWeb of Science
    1. Lindon C.,
    2. Montarras D.,
    3. Pinset C.
    (1998) Cell cycle-regulated expression of the muscle determination factor Myf5 in proliferating myoblasts. J. Cell. Biol 140, 111–118
    OpenUrlAbstract/FREE Full Text
    1. Marcelle C.,
    2. Wolf J.,
    3. 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
    OpenUrlCrossRefPubMed
    1. Marcelle C.,
    2. Stark M. R.,
    3. Bronner-Fraser M.
    (1997) Coordinate actions of BMPs, Wnts, Shh and Noggin mediate patterning of the dorsal somite. Development 124, 3955–3963
    OpenUrlAbstract
    1. Munsterberg A. E.,
    2. Kitajewski J.,
    3. Bumcrot D. A.,
    4. McMahon A. P.,
    5. Lassar A. B.
    (1995) Combinatorial signaling by sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev 9, 2911–2922
    OpenUrlAbstract/FREE Full Text
    1. Ordahl C. P.,
    2. Le Douarin N.
    (1992) Two myogenic lineages within the developing somite. Development 114, 339–353
    OpenUrlAbstract
    1. Ott M. O.,
    2. Bober E.,
    3. Lyons G.,
    4. Arnold H.,
    5. Buckingham M.
    (1991) Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111, 1097–1107
    OpenUrlAbstract/FREE Full Text
    1. Parr B. A.,
    2. Shea M. J.,
    3. Vassileva G.,
    4. McMahon A. P.
    (1993) Mouse Wnt genes exhibit discrete domains of expression in early embryonic CNS and limb buds. Development 119, 247–261
    OpenUrlAbstract
    1. Parr B. A.,
    2. McMahon A. P.
    (1995) Dorsalization by Wnt 7a of DV and AP axes of mouse limb. Nature 374, 350–353
    OpenUrlCrossRefPubMed
    1. Pourquie O.,
    2. Fan C. M.,
    3. Coltey M.,
    4. Hirsinger E.,
    5. Watanabe Y.,
    6. Breant C.,
    7. Francis-West P.,
    8. Brickell P.,
    9. Tessier-Lavigne M.,
    10. Le Douarin N. M.
    (1996) Lateral and axial signals involved in avian somite patterning: a role for BMP4. Cell 84, 461–471
    OpenUrlCrossRefPubMedWeb of Science
    1. Rong P. M.,
    2. Teillet M. A.,
    3. Ziller C.,
    4. Le Douarin N. M.
    (1992) The neural tube/notocord complex is necessary for vertebral but not limb and body wall striated muscle differentiation. Development 114, 339–353
    1. Rudnicki M. A.,
    2. Braun T.,
    3. Hinuma S.,
    4. 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, 383–390
    OpenUrlCrossRefPubMedWeb of Science
    1. Serbedzija G.,
    2. Fraser S. E.,
    3. Bonner-Fraser M.
    (1990) Pathways of trunk neural crest migration in the mouse embryo revealed by vital dye analysis. Development 108, 605–612
    OpenUrlAbstract/FREE Full Text
    1. Smolich B. D.,
    2. McMahon J. A.,
    3. McMahon A. P.,
    4. Papkoff J.
    (1993) Wnt family proteins are secreted and associated with the cell surface. Mol. Biol. Cell 4, 1267–1275
    OpenUrlAbstract/FREE Full Text
    1. Stern H. M.,
    2. Brown A. M. C.,
    3. Hauschka S. D.
    (1995) Myogenesis in paraxial mesoderm: preferential induction by dorsal neural tube and by cells expressing Wnt-1. Development 121, 3675–3686
    OpenUrlAbstract
    1. Tajbakhsh S.,
    2. Vivarelli G.,
    3. Cusella-De Angelis G.,
    4. Rocancourt D.,
    5. Buckingham M.,
    6. Cossu G.
    (1994) A population of myogenic cells derived from the mouse neural tube. Neuron 13, 813–821
    OpenUrlCrossRefPubMedWeb of Science
    1. Tajbakhsh S.,
    2. Rocancourt D.,
    3. Buckingham M.
    (1996) Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in Myf5 null mice. Nature 384, 266–270
    OpenUrlCrossRefPubMedWeb of Science
    1. Tajbakhsh S.,
    2. Bober E.,
    3. Babinet C.,
    4. Pournin S.,
    5. Arnold H.,
    6. Buckingham M.
    (1996) 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. Dyn 206, 291–300
    OpenUrlCrossRefPubMedWeb of Science
    1. Tajbakhsh S.,
    2. Rocancourt D.,
    3. Cossu G. M.,
    4. Buckingham M.
    (1997) Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf5 act upstream of MyoD. Cell 89, 127–138
    OpenUrlCrossRefPubMedWeb of Science
    1. Tajbakhsh S.,
    2. Cossu G.
    (1997) Establishing myogenic identity during somitogenesis. Curr. Opin. Genet. Develop 7, 634–641
    OpenUrlCrossRefPubMed
    1. Wang S.,
    2. Krinks M.,
    3. Lin K.,
    4. Luyten F. P.,
    5. Moos M., Jr
    (1997) Frzb a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88, 757–766
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
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
S. Tajbakhsh, U. Borello, E. Vivarelli, R. Kelly, J. Papkoff, D. Duprez, M. Buckingham, G. Cossu
Development 1998 125: 4155-4162;
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