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JOURNAL ARTICLES
Combinatorial signals from the neural tube, floor plate and notochord induce myogenic bHLH gene expression in the somite
A.E. Munsterberg, A.B. Lassar
Development 1995 121: 651-660;

Summary

The neural tube, floor plate and notochord are axial tissues in the vertebrate embryo which have been demonstrated to play a role in somite morphogenesis. Using in vitro coculture of tissue explants, we have monitored inductive interactions of these axial tissues with the adjacent somitic mesoderm in chick embryos. We have found that signals from the neural tube and floor plate/notochord are necessary for expression of the myogenic bHLH regulators MyoD, Myf5 and myogenin in the somite. Eventually somitic expression of the myogenic bHLH genes is maintained in the absence of the axial tissues. In organ culture, at early developmental stages (HH 11-), induction of myogenesis in the three most recently formed somites can be mediated by the neural tube together with the floor plate/notochord, while in more rostral somites (stages IV-IX) the neural tube without the floor plate/notochord is sufficient. By recombining somites and neural tubes from different axial levels of the embryo, we have found that a second signal is necessary to promote competence of the somite to respond to inducing signals from the neural tube. Thus, we propose that at least two signals from axial tissues work in combination to induce myogenic bHLH gene expression; one signal derives from the floor plate/notochord and the other signal derives from regions of the neural tube other than the floor plate.

Reference

    1. Aoyama H.,
    2. Asamoto K.
    (1988) Determination of somite cells: independence of cell differentiation and morphogenesis. Development 104, 15–28
    OpenUrlAbstract
    1. Artinger K. B.,
    2. Bonner-Fraser M.
    (1993) Delayed formation of the floor plate after ablation of the avian notochord. Neuron 11, 1147–1161
    OpenUrlCrossRefPubMedWeb of Science
    1. Avery G.,
    2. Chow M.,
    3. Holtzer H.
    (1956) An experimental analysis of the development of the spinal column. J. Exp. Zool 132, 409–425
    OpenUrlCrossRef
    1. Barth J.,
    2. Ivarie R.
    (1994) Polyvinyl alcohol enhances detection of low abundance transcripts in early stage quail embryos in a nonradioactive whole mount in situ hybridization technique. Biotechniques 17, 324–327
    OpenUrlPubMedWeb of Science
    1. Bober E.,
    2. Lyons G. E.,
    3. Braun T.,
    4. Cusso G.,
    5. Buckingham M.
    (1991) The muscle regulatory gene, Myf-6, has a biphasic pattern of expression during early mouse development. J. Cell Biol 113, 1255–1265
    OpenUrlAbstract/FREE Full Text
    1. Bober E.,
    2. Brand-Saberi B.,
    3. Ebensperger C.,
    4. Wilting J.,
    5. Balling R.,
    6. Paterson B.M.,
    7. Arnold H.-H.,
    8. Christ B.
    (1994) Initial steps of myogenesis in somites are independent of influence from axial structures. Development 120, 3073–3082
    OpenUrlAbstract
    1. Borman W. H.,
    2. Urlakis K. J., Jr.,
    3. Yorde D. E.
    (1994) Analysis of the in vivo myogenic status of chick somites by desmin expression in vitro. Developmental Dynamics 199, 268–279
    OpenUrlPubMed
    1. Brand-Saberi B.,
    2. Ebensperger C.,
    3. Wilting J.,
    4. Balling R.,
    5. Christ B.
    (1993) The ventralizing effect of the notochord on somite differentiation in chick embryos. Anat. Embryol 188, 239–245
    OpenUrlPubMed
    1. Braun T.,
    2. Bober E.,
    3. Buschhausen-Denker G.,
    4. Kohtz S.,
    5. Grzeschik K.-H.,
    6. Arnold H. H.
    (1989) Differentential expression of myogenic determination genes in muscle cells: possible autoactivation by the Myf gene products. EMBO J 8, 3617–3625
    OpenUrlPubMedWeb of Science
    1. Buckingham M.
    (1992) Making muscle in mammals. Trends in Genetics 8, 144–149
    OpenUrlCrossRefPubMedWeb of Science
    1. Buffinger N.,
    2. Stockdale F.
    (1994) Myogenic specification in somites: induction by axial structures. Development 120, 1443–1452
    OpenUrlAbstract
    1. Charles de la Brousse F.,
    2. Emerson P.C., Jr.
    (1990) Localized expression of a myogenic regulatory gene, qmf1, in the somite dermatome of avian embryos. Genes and Develop 4, 567–581
    OpenUrlAbstract/FREE Full Text
    1. Christ B.,
    2. Brand-Saberi B.,
    3. Grim M.,
    4. Wilting J.
    (1992) Local signalling in dermomyotomal cell type specification. Anat. Embryol 186, 505–510
    OpenUrlPubMed
    1. Chomczynski P.,
    2. Sacchi N.
    (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem 162, 156–159
    OpenUrlCrossRefPubMedWeb of Science
    1. Dietrich S.,
    2. Schubert F. R.,
    3. Gruss P.
    (1993) Altered Pax gene expression in murine notochord mutants: the notochord is required to initiate and maintain ventral identity in the somite. Mech. o. Dev 44, 189–207
    OpenUrlCrossRefPubMedWeb of Science
    1. Dugaiczyk A.,
    2. Haron J. A.,
    3. Stone E. M.,
    4. Dennison O. E.,
    5. Rothblum K. N.,
    6. Schwartz R. J.
    (1983) Cloning and sequencing of a deoxyribonucleic acid copy of glyceraldehyde-3-phosphate dehydrogenase messenger ribonucleic acid isolated from chicken muscle. Biochemistry 22, 1605–1613
    OpenUrlCrossRefPubMed
    1. Echelard Y.,
    2. Epstein D. J.,
    3. St-Jacues B.,
    4. Shen L.,
    5. Mohler J.,
    6. McMahon J. A.,
    7. McMahon A. P.
    (1993) Sonic Hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417–1430
    OpenUrlCrossRefPubMedWeb of Science
    1. Emerson C. P., Jr.
    (1993) Embryonic signals for skeletal myogenesis: arriving at the beginning. Current Opinion in Cell Biology 5, 1057–1064
    OpenUrlCrossRefPubMed
    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, 1–20
    OpenUrlCrossRefPubMedWeb of Science
    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. Hamburger V.,
    2. Hamilton H. L.
    (1951) A series of normal stages in the development of the chick embryo. J.Morph 88, 49–92
    OpenUrlCrossRefPubMedWeb of Science
    1. Hasty P.,
    2. Bradley A.,
    3. Morris J. H.,
    4. Edmondson D. G.,
    5. Venuti J. M.,
    6. Olson E.,
    7. Klein W. H.
    (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501–506
    OpenUrlCrossRefPubMedWeb of Science
    1. Hinterberger T. J.,
    2. Sassoon D. A.,
    3. Rhodes S. J.,
    4. Konienczny S. F.
    (1991) Expression of the muscle regulatory factor MRF4 during somite and skeletal myofiber development. Dev. Biol 147, 144–156
    OpenUrlCrossRefPubMedWeb of Science
    1. Hopwood N.,
    2. Pluck D. A.,
    3. Gurdon J. B.
    (1989) MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. EMBO J 8, 3409–3417
    OpenUrlPubMedWeb of Science
    1. Hopwood N.,
    2. Pluck D. A.,
    3. Gurdon J. B.
    (1989) A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest. Cell 59, 893–903
    OpenUrlCrossRefPubMedWeb of Science
    1. Kavinsky C. J.,
    2. Umeda P. K.,
    3. Sinha A. M.,
    4. Wlzinga M. W.,
    5. Tong S. W.,
    6. Zak R.,
    7. Jakovicic S.,
    8. Rabinowitz M.
    (1983) Cloned mRNA sequences for two types of embryonic myosing heavy chains from chick skeletal muscle. J. Biological Chemistry 258, 5196–5205
    OpenUrlAbstract/FREE Full Text
    1. Kenny-Mobbs T.,
    2. Thorogood P.
    (1987) Autonomy of differentiation in avian brachial somites and the influence of adjacent tissues. Development 100, 449–462
    OpenUrlAbstract
    1. Koseki H.,
    2. Wallin J.,
    3. Wilting J.,
    4. Mizutani Y.,
    5. Kispert A.,
    6. Ebensperger C.,
    7. Herrmann B.,
    8. Christ B.,
    9. Balling R.
    (1993) A role for Pax-1 as a mediator of notochordal signals during the dorsoventral specification of vertebrae. Development 119, 649–660
    OpenUrlAbstract/FREE Full Text
    1. Krauss S.,
    2. Concordet J. P.,
    3. Ingham P. W.
    (1993) A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431–1444
    OpenUrlCrossRefPubMedWeb of Science
    1. Lash J.,
    2. Holtzer S.,
    3. Holtzer H.
    (1957) An experimental analysis of the development of the spinal column. Exp. Cell Res 13, 292–303
    1. Lassar A. B.,
    2. Munsterberg A. E.
    (1994) Wiring diagrams: regularoty circuits and the control of skeletal myogenesis. Current Opinion in Cell Biology 6, 432–442
    OpenUrlCrossRefPubMedWeb of Science
    1. Lin A.-Y.,
    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. Lipton B. H.,
    2. Jacobson A. G.
    (1974) Experimental analysis of the mechanisms of somite morphogenesis. Dev. Biol 38, 91–103
    OpenUrlCrossRefPubMedWeb of Science
    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. Olson E. N.,
    2. Klein W. H.
    (1994) bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev 8, 1–8
    OpenUrlFREE 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. Packard D. S., Jr.,
    2. Jacobson A. G.
    (1976) The influence of axial structures on chick somite formation. Dev. Biol 53, 36–48
    OpenUrlCrossRefPubMedWeb of Science
    1. Placzek M.,
    2. Tessier-Lavigne M.,
    3. Yamada T.,
    4. Jessell T.,
    5. Dodd J.
    (1990) Mesodermal control of neural cell identitiy: Floor plate induction by the notochord. Science 250, 985–988
    OpenUrlAbstract/FREE Full Text
    1. Placzek M.,
    2. Jessell T. M.,
    3. Dodd J.
    (1993) Induction of floor plate differentiation by contact-dependent, homeogenetic signals. Development 117, 205–218
    OpenUrlAbstract/FREE Full Text
    1. Pownall M. E.,
    2. Emerson C. P., Jr.
    (1992) Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Dev. Biol 151, 67–79
    OpenUrlCrossRefPubMedWeb of Science
    1. Riddle R. D.,
    2. Johnson R. L.,
    3. Laufer E.,
    4. Tabin C.
    (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401–1416
    OpenUrlCrossRefPubMedWeb of Science
    1. Roelink H.,
    2. Augsburger A.,
    3. Heemskerk J.,
    4. Korzh V.,
    5. Norlin. s.,
    6. Ruiz i Altaba A.,
    7. Tanabe Y.,
    8. Placzek M.,
    9. Edlund T.,
    10. Jessell T. M.,
    11. Dodd J.
    (1994) Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761–775
    OpenUrlCrossRefPubMedWeb of Science
    1. Rong P. M.,
    2. Teillet M.-A.,
    3. Ziller C.,
    4. Le Douarin N. M.
    (1992) The neural tube/floor plate/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. A.,
    2. Schnegelsberg P. N. J.,
    3. Stead R. H.,
    4. Braun T.,
    5. Arnold H. H.,
    6. Jaenisch R.
    (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351–1359
    OpenUrlCrossRefPubMedWeb of Science
    1. Saitoh O.,
    2. Fujisawa-Sehara A.,
    3. Nabeshima Y.,
    4. Periasamy M.
    (1993) Expression of myogenic factors in denervated chicken breast muscle: isolation of the chicken Myf-5 gene. Nucleic Acid Res 21, 2503–2509
    OpenUrlAbstract/FREE Full Text
    1. Sassoon D.
    (1993) Myogenic regulatory factors: dissecting their role and regulation during vertebrate embryogenesis. Dev. Biol 156, 11–23
    OpenUrlCrossRefPubMedWeb of Science
    1. Sassoon D.,
    2. Lyons G.,
    3. Wright W. E.,
    4. Lin V.,
    5. Lassar A. B.,
    6. Weintraub H.,
    7. Buckingham M.
    (1989) Expression of two myogenic regulatory factors, myogenin and MyoD1, during mouse embyogenesis. Nature 341, 303–307
    OpenUrlCrossRefPubMed
    1. Smith J. L.,
    2. Schoenwolf G. C.
    (1989) Notochordal induction of cell wedging in the chidk neural plate and its role in neural tube formation. J. Exp. Zoology 250, 49–62
    OpenUrlCrossRefPubMedWeb of Science
    1. Tapscott S. J.,
    2. Davis R. L.,
    3. Thayer M. J.,
    4. Cheng P.-F.,
    5. Weintraub H.,
    6. Lassar A. B.
    (1988) MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts. Science 242, 405–411
    OpenUrlAbstract/FREE Full Text
    1. Teillet M.-A.,
    2. Le Douarin N. M.
    (1983) Consequences of neural tube and notochord excision on the development of the peripheral nervous system in the chick embryos. Dev. Biol 98, 192–211
    OpenUrlCrossRefPubMed
    1. van Straaten H. W. M.,
    2. Hekking J. W. M.,
    3. Wiertz-Hoessels E. L.,
    4. Thors F.,
    5. Drukker J.
    (1988) Effect of the notochord on the differentiation of a floor plate area in the neural tube of the chick embryo. Anat. Embryol 177, 317–324
    OpenUrlCrossRefPubMed
    1. van Straaten H. W. M.,
    2. Hekking J. W. M.
    (1991) Development of floor plate, neurons and axonal autgrowth pattern in the early spinal cord of the notochord-deficient chick embryo. Anat. Embryol 184, 55–63
    OpenUrlCrossRefPubMed
    1. Vivarelli E.,
    2. Cossu G.
    (1986) Neural control of early myogenic differentiation in cultures of mouse somites. Dev. Biol 117, 319–325
    OpenUrlCrossRefPubMed
    1. Wachtler F.,
    2. Christ B.
    (1992) The basic embryology of skeletal muscle formation in vertebrates: the avian model. Dev. Biol 3, 217–227
    1. Weintraub H.
    (1993) The MyoD family and myogenesis: Redundancy, networks and thresholds. Cell 75, 1241–1244
    OpenUrlCrossRefPubMedWeb of Science
    1. Wolf C.,
    2. Thisse C.,
    3. Stoetzel C.,
    4. Thisse B.,
    5. Gerlinger P.,
    6. Perrin-Schmitt F.
    (1991) The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev. Biol 143, 363–373
    OpenUrlCrossRefPubMedWeb of Science
    1. Yamada T.,
    2. Placzek M.,
    3. Tanaka H.,
    4. Dodd J.,
    5. Jessell T. M.
    (1991) Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64, 635–647
    OpenUrlCrossRefPubMedWeb of Science
    1. Yamada T.,
    2. Pfaff S. L.,
    3. Edlund T.,
    4. Jessell T. M.
    (1993) Control of cell pattern in the neural tube: Motor neuron induction by diffusible factors from notochord and floor plate. Cell 73, 673–686
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Combinatorial signals from the neural tube, floor plate and notochord induce myogenic bHLH gene expression in the somite
A.E. Munsterberg, A.B. Lassar
Development 1995 121: 651-660;
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