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JOURNAL ARTICLES
Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification
B.A. Williams, C.P. Ordahl
Development 1994 120: 785-796;

Summary

Specification of the myogenic lineage begins prior to gastrulation and culminates in the emergence of determined myogenic precursor cells from the somites. The myoD family (MDF) of transcriptional activators controls late step(s) in myogenic specification that are closely followed by terminal muscle differentiation. Genes expressed in myogenic specification at stages earlier than MDFs are unknown. The Pax-3 gene is expressed in all the cells of the caudal segmental plate, the early mesoderm compartment that contains the precursors of skeletal muscle. As somites form from the segmental plate and mature, Pax-3 expression is progressively modulated. Beginning at the time of segmentation, Pax-3 becomes repressed in the ventral half of the somite, leaving Pax-3 expression only in the dermomyotome. Subsequently, differential modulation of Pax-3 expression levels delineates the medial and lateral halves of the dermomyotome, which contain precursors of axial (back) muscle and limb muscle, respectively. Pax-3 expression is then repressed as dermomyotome-derived cells activate MDFs. Quail-chick chimera and ablation experiments confirmed that the migratory precursors of limb muscle continue to express Pax-3 during migration. Since limb muscle precursors do not activate MDFs until 2 days after they leave the somite, Pax-3 represents the first molecular marker for this migratory cell population. A null mutation of the mouse Pax-3 gene, Splotch, produces major disruptions in early limb muscle development (Franz, T., Kothary, R., Surani, M. A. H., Halata, Z. and Grim, M. (1993) Anat. Embryol. 187, 153–160; Goulding, M., Lumsden, A. and Paquette, A. (1994) Development 120, 957–971). We conclude, therefore, that Pax-3 gene expression in the paraxial mesoderm marks earlier stages in myogenic specification than MDFs and plays a crucial role in the specification and/or migration of limb myogenic precursors.

REFERENCES

    1. Beddington R. S. P.,
    2. Martin P.
    (1989) An in situ transgenic enzyme marker to monitor migration of cells in the mid-gestation mouse embryo: somite contribution to the forelimb. Mol. Biol. Med 6, 263–274
    OpenUrlPubMed
    1. Beresford B.
    (1983) Brachial muscles in the chick embryo: the fate of individual somites. J. Embryol. exp. Morph 77, 99–116
    OpenUrlPubMedWeb of Science
    1. Bonner P. H.,
    2. Hauschka S. D.
    (1974) Clonal analysis of vertebrate myogenesis: Early developmental events in the chick limb. Dev. Biol 37, 317–328
    OpenUrlCrossRefPubMedWeb of Science
    1. Braun T.,
    2. Rudnicki M.,
    3. Arnold H.,
    4. Jaenisch R.
    (1992) Targeted inactivation of the muscle regulatory gene myf-5 results in abnormal rib development and perinatal death. Cell 71, 369–382
    OpenUrlCrossRefPubMedWeb of Science
    1. Charles de la Brousse F.,
    2. Emerson C. P.
    (1990) Localized expression of a myogenic regulatory gene, qmf1, in the somite dermatome of avian embryos. Genes Dev 4, 567–581
    OpenUrlAbstract/FREE Full Text
    1. Chevallier A.,
    2. Kieny M.,
    3. Mauger A.
    (1977) Limb-somite relationship: Origin of the limb musculature. J. Embryol. exp. Morph 41, 245–258
    OpenUrlPubMedWeb of Science
    1. Chevallier A.,
    2. Kieny M.,
    3. Mauger A.
    (1978) Limb-somite relationship: effect of removal of somitic mesoderm on the wing musculature. J. Embryol. exp. Morph 43, 263–278
    OpenUrlPubMed
    1. Chiquet-Ehrismann R.
    (1991) Anti-adhesive molecules of the extracellular matrix. Curr. Op. Cell Biol 3, 800–804
    OpenUrlCrossRefPubMed
    1. Choi J.,
    2. Costa M. L.,
    3. Mermelstein C. S.,
    4. Chagas C.,
    5. Holtzer S.,
    6. Holtzer H.
    (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, 7988–7992
    OpenUrlAbstract/FREE Full Text
    1. Christ B.,
    2. Jacob H.,
    3. Jacob M.
    (1974) Uber den ursprung der flugelmuskulature. Experientia 30, 1446–1448
    OpenUrlCrossRefPubMedWeb of Science
    1. Christ B.,
    2. Jacob H.,
    3. Jacob M.
    (1977) Experimental analysis of the origin of the wing musculature in avian embryos. Anat. Embryol 150, 171–186
    OpenUrlCrossRefPubMed
    1. Corbin V.,
    2. Michelson A. M.,
    3. Abmayr S. M.,
    4. Neel V.,
    5. Alcamo E.,
    6. Maniatis T.,
    7. Young M. W.
    (1991) A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell 67, 311–323
    OpenUrlCrossRefPubMedWeb of Science
    1. Cserjesi P.,
    2. Lilly B.,
    3. Bryson L.,
    4. Wang Y.,
    5. Sassoon D. A.,
    6. Olson E. N.
    (1992) MHox: a mesodermally restricted homeodomain protein that binds an essential site in the muscle creatine kinase enhancer. Development 115, 1087–1101
    OpenUrlAbstract
    1. Dienstman S. R.,
    2. Biehl J.,
    3. Holtzer S.,
    4. Holtzer H.
    (1974) Myogenic and chondrogenic lineages in developing limb buds grown in vitro. Dev. Biol 39, 83–95
    OpenUrlPubMedWeb of Science
    1. Emerson C. P.
    (1993) Skeletal myogenesis: genetics and embryology to the fore. Curr. Op. Gen. Dev 3, 265–274
    OpenUrlCrossRefPubMed
    1. Epstein D.,
    2. Vekemans M.,
    3. Gros P.
    (1991) Splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3. Cell 67, 767–774
    OpenUrlCrossRefPubMedWeb of Science
    1. Franz T.
    (1993) The Splotch (Sp1H) and Splotch-delayed (Spd) alleles: differential phenotypic effects on neural crest and limb musculature. Anat. Embryol 187, 371–377
    OpenUrlPubMed
    1. Franz T.,
    2. Kothary R.,
    3. Surani M. A. H.,
    4. Halata Z.,
    5. Grim M.
    (1993) The Splotch mutation interferes with muscle development in the limbs. Anat. Embryol 187, 153–160
    OpenUrlPubMed
    1. Frohman M. A.,
    2. Boyle M.,
    3. Martin G. R.
    (1990). Isolation of the mouse Hox-2.9 gene; analysis of embryonic expression suggests that positional information along the anterior-posterior axis is specified by mesoderm. Development 110, 589–607
    OpenUrlAbstract/FREE Full Text
    1. Goulding M.,
    2. Sterrer S.,
    3. Fleming J.,
    4. Balling R.,
    5. Nadeau J.,
    6. Moore K.,
    7. Brown S.,
    8. Steel K.,
    9. Gruss P.
    (1993) Analysis of the Pax-3 gene in the mouse mutant Splotch. Genomics 17, 355–363
    OpenUrlCrossRefPubMedWeb of Science
    1. Goulding M. D.,
    2. Chalepakis G.,
    3. Deutsch U.,
    4. Erselius J. R.,
    5. Gruss P.
    (1991) Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J 10, 1135–1147
    OpenUrlPubMedWeb of Science
    1. Goulding M. D.,
    2. Lumsden A.,
    3. Gruss P.
    (1993) Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord. Development 117, 1001–1016
    OpenUrlAbstract
    1. Goulding M.,
    2. Lumsden A.,
    3. Paquette A. J.
    (1994) Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120, 957–971
    OpenUrlAbstract
    1. Gruss P.,
    2. Walther C.
    (1992) Pax in development. Cell 69, 719–722
    OpenUrlCrossRefPubMedWeb of Science
    1. Halpern M. E.,
    2. Ho R. K.,
    3. Walker C.,
    4. Kimmel C. B.
    (1993) Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell 75, 99–111
    OpenUrlCrossRefPubMedWeb of Science
    1. Hamburger V.,
    2. Hamilton H. L.
    (1951) A series of normal stages in the development of the chick embryo. J. Morphol 88, 49–92
    OpenUrlCrossRefPubMedWeb of Science
    1. Hamburger V.,
    2. Hamilton H. L.
    (1992) A series of normal stages in the development of the chick embryo. Dev. Dynam 195, 231–272
    OpenUrlCrossRefPubMedWeb of Science
    1. Hartenstein A. Y.,
    2. Rugendorff A.,
    3. Tepass U.,
    4. Hartenstein V.
    (1992) The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development 116, 1203–1220
    OpenUrlAbstract/FREE Full Text
    1. Hasty P.,
    2. Bradley A.,
    3. Morris J.,
    4. Edmondson D.,
    5. Venuti J.,
    6. Olson E.,
    7. Klein W.
    (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501–506
    OpenUrlCrossRefPubMedWeb of Science
    1. Heitzler P.,
    2. Simpson P.
    (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64, 1083–1092
    OpenUrlCrossRefPubMedWeb of Science
    1. Jones F. S.,
    2. Prediger E. A.,
    3. Bittner D. A.,
    4. DeRobertis E. M.,
    5. Edelman G. M.
    (1992). Cell adhesion molecules as targets for Hox genes: Neural cell adhesion molecule promoter activity is modulated by cotransfection with Hox-2.5 and -2.4. Proc. Natl. Acad. Sci. USA 89, 2086–2090
    OpenUrlAbstract/FREE Full Text
    1. Kaehn K.,
    2. Jacob H. J.,
    3. Christ B.,
    4. Hinrichsen K.,
    5. Poelmann R.
    (1988) The onset of myotome formation in the chick. Anat. Embryol 177, 191–201
    OpenUrlCrossRefPubMed
    1. Keynes R.,
    2. Stern C.
    (1988) Mechanisms of vertebrate segmentation. Development 103, 413–429
    OpenUrlPubMedWeb of Science
    1. Krenn V.,
    2. Gorka P.,
    3. Wachtler F.,
    4. Christ B.,
    5. Jacob H. J.
    (1988) On the origin of cells determined to form skeletal muscle in avian embryos. Anat. Embryol 179, 49–54
    OpenUrlCrossRefPubMed
    1. Le Douarin N. M.
    (1973) A Feulgen-positive nucleus. Exp. Cell Res 77, 459–468
    OpenUrlCrossRefPubMedWeb of Science
    1. Lin Z.,
    2. Dechesne C. A.,
    3. Eldridge J.,
    4. Paterson B. M.
    (1989) An avian muscle factor related to MyoD1 activates muscle-specific promoters in nonmuscle cells of different germ-layer origin and in BrdU-treated myoblasts. Genes Dev 3, 986–996
    OpenUrlAbstract/FREE Full Text
    1. Moase C. E.,
    2. Trasler D. G.
    (1990) Delayed neural crest cell emigration from Sp and Spdmouse neural tube explants. Teratology 42, 171–182
    OpenUrlCrossRefPubMedWeb of Science
    1. Moase C. E.,
    2. Trasler D. G.
    (1991) N-CAM alteration in splotch neural tube defect mouse embryos. Development 113, 1049–1058
    OpenUrlAbstract
    1. Nabeshima Y.,
    2. Hanaoka K.,
    3. Hayasaka M.,
    4. Esumi E.,
    5. Li S.,
    6. Nonaka I.,
    7. Nabeshima Y.
    (1993) Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532–535
    OpenUrlCrossRefPubMedWeb of Science
    1. Newman S. A.,
    2. Pautou M.-P.,
    3. Kieny M.
    (1981) The distal boundary of myogenic primordia in chimeric avian limb buds and its relation to an accessible population of cartilage progenitor cells. Dev. Biol 84, 440–448
    OpenUrlCrossRefPubMedWeb of Science
    1. Olson E. N.
    (1992) Interplay between proliferation and differentiation within the myogenic lineage. Dev. Biol 154, 261–272
    OpenUrlCrossRefPubMedWeb of Science
    1. Ordahl C. P.,
    2. Le Douarin N. M.
    (1992) Two myogenic lineages within the developing somite. Development 114, 339–353
    OpenUrlAbstract
    1. Ott M.,
    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. Pourquie O.,
    2. Coultey M.,
    3. Teillet M.-A.,
    4. Ordahl C. P.,
    5. Le Douarin N. M.
    (1993) Control of dorsoventral patterning of the somitic derivatives by notochord and floor plate. Proc. Natl. Acad. Sci. USA 90, 5242–5246
    OpenUrlAbstract/FREE Full Text
    1. Pownall M. E.,
    2. Emerson C. P.
    (1992) Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Dev. Biol 151, 67–79
    OpenUrlCrossRefPubMedWeb of Science
    1. Reaume A. G.,
    2. Conlon R. A.,
    3. Zirngibl R.,
    4. Yamaguchi T. P.,
    5. Rossant J.
    (1992) Expression analysis of a Notch homologue in the mouse embryo. Dev. Biol 154, 377–387
    OpenUrlCrossRefPubMedWeb of Science
    1. Rong P. M.,
    2. Teillet M.-A.,
    3. Ziller C.,
    4. Le Douarin N. M.
    (1992) The neural tube/notochord complex is necessary for vertebral but not limb and body wall striated muscle differentiation. Development 115, 657–672
    OpenUrlAbstract/FREE Full Text
    1. Rudnicki M.,
    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. Rutz R.,
    2. Haney C.,
    3. Hauschka S.
    (1982) Spatial analysis of limb bud myogenesis: A proximodistal gradient of muscle colony-forming cells in chick embryo leg buds. Dev. Biol 90, 399–411
    OpenUrlCrossRefPubMedWeb of Science
    1. Searls R.,
    2. Janners M.
    (1969) The stabilization of cartilage properties in the cartilage-forming mesenchyme of the embryonic chick limb. J. Exp. Zool 170, 365–376
    OpenUrlCrossRefPubMedWeb of Science
    1. Seed J.,
    2. Hauschka S. D.
    (1984) Temporal separation of the migration of distinct myogenic precursor populations into the developing chick wing bud. Dev. Biol 106, 389–393
    OpenUrlCrossRefPubMed
    1. Selleck M.,
    2. Stern C.
    (1991) Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. Development 112, 615–626
    OpenUrlAbstract
    1. Stark R.,
    2. Searls R.
    (1974) The establishment of the cartilage pattern in the embryonic chick wing, and evidence for a role of the dorsal and ventral ectoderm in normal wing development. Dev. Biol 38, 51–63
    OpenUrlCrossRefPubMedWeb of Science
    1. Tan S.-S.,
    2. Prieto A. L.,
    3. Newgreen D. F.,
    4. Crossin K. L.,
    5. Edelman G. M.
    (1991) Cytotactin expression in somites after dorsal neural tube and neural crest ablation in chicken embryos. Proc. Natl. Acad. Sci. USA 88, 6398–6402
    OpenUrlAbstract/FREE Full Text
    1. Weintraub H.,
    2. Davis R.,
    3. Tapscott S.,
    4. Thayer M.,
    5. Krause M.,
    6. Benezra R.,
    7. Blackwell T. K.,
    8. Turner D.,
    9. Rupp R.,
    10. Hollenberg S.,
    11. Zhuang Y.,
    12. Lassar A.
    (1991) The myoD gene family: Nodal point during specification of the muscle cell lineage. Science 251, 761–766
    OpenUrlAbstract/FREE Full Text
    1. Weintraub H.,
    2. Tapscott S. J.,
    3. Davis R. L.,
    4. Thayer M. J.,
    5. Adam M. A.,
    6. Lassar A. B.,
    7. Miller A. D.
    (1989) Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc. Natl. Acad. Sci. USA 86, 5434–5438
    OpenUrlAbstract/FREE Full Text
    1. White N. K.,
    2. Bonner P. H.,
    3. Nelson D. R.,
    4. Hauschka S. D.
    (1975) Clonal analyis of vertebrate myogenesis: Medium-dependent classification of colony-forming cells. Dev. Biol 44, 346–361
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification
B.A. Williams, C.P. Ordahl
Development 1994 120: 785-796;
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