Abstract
The body musculature of higher vertebrates is composed of the epaxial muscles, associated with the vertebral column, and of the hypaxial muscles of the limbs and ventro-lateral body wall. Both sets of muscles arise from different cell populations within the dermomyotomal component of the somite. Myogenesis first occurs in the medial somitic cells that will form the epaxial muscles and starts with a significant delay in cells derived from the lateral somitic moiety that migrate to yield the hypaxial muscles. The newly formed somite is mostly composed of unspecified cells, and the determination of somitic compartments toward specific lineages is controlled by environmental cues. In this report, we show that determinant signals for lateral somite specification are provided by the lateral plate. They result in a blockade of the myogenic program, which maintains the lateral somitic cells as undifferentiated muscle progenitors expressing the Pax-3 gene, and represses the activation of the MyoD family genes. In vivo, this mechanism could account for the delay observed in the onset of myogenesis between muscles of the epaxial and hypaxial domains.
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- Bober E., Brand-Saberi B., Ebensperger C., Wilting J., Balling R., Paterson B. M., Arnold H. H., Christ B. Initial steps of myogenesis in somites are independent of influence from axial structures. Development. 1994 Nov;120(11):3073–3082. doi: 10.1242/dev.120.11.3073. [DOI] [PubMed] [Google Scholar]
- Bober E., Franz T., Arnold H. H., Gruss P., Tremblay P. Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development. 1994 Mar;120(3):603–612. doi: 10.1242/dev.120.3.603. [DOI] [PubMed] [Google Scholar]
- Buckingham M. Making muscle in mammals. Trends Genet. 1992 Apr;8(4):144–148. doi: 10.1016/0168-9525(92)90373-C. [DOI] [PubMed] [Google Scholar]
- Buffinger N., Stockdale F. E. Myogenic specification in somites: induction by axial structures. Development. 1994 Jun;120(6):1443–1452. doi: 10.1242/dev.120.6.1443. [DOI] [PubMed] [Google Scholar]
- Christ B., Brand-Saberi B., Grim M., Wilting J. Local signalling in dermomyotomal cell type specification. Anat Embryol (Berl) 1992 Oct;186(5):505–510. doi: 10.1007/BF00185464. [DOI] [PubMed] [Google Scholar]
- Chédotal A., Pourquié O., Sotelo C. Initial tract formation in the brain of the chick embryo: selective expression of the BEN/SC1/DM-GRASP cell adhesion molecule. Eur J Neurosci. 1995 Feb 1;7(2):198–212. doi: 10.1111/j.1460-9568.1995.tb01056.x. [DOI] [PubMed] [Google Scholar]
- Couly G. F., Coltey P. M., Le Douarin N. M. The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development. 1992 Jan;114(1):1–15. doi: 10.1242/dev.114.1.1. [DOI] [PubMed] [Google Scholar]
- Emerson C. P., Jr Embryonic signals for skeletal myogenesis: arriving at the beginning. Curr Opin Cell Biol. 1993 Dec;5(6):1057–1064. doi: 10.1016/0955-0674(93)90092-5. [DOI] [PubMed] [Google Scholar]
- Goulding M., Lumsden A., Paquette A. J. Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development. 1994 Apr;120(4):957–971. doi: 10.1242/dev.120.4.957. [DOI] [PubMed] [Google Scholar]
- Kalcheim C., Neufeld G. Expression of basic fibroblast growth factor in the nervous system of early avian embryos. Development. 1990 May;109(1):203–215. doi: 10.1242/dev.109.1.203. [DOI] [PubMed] [Google Scholar]
- Kenny-Mobbs T., Thorogood P. Autonomy of differentiation in avian branchial somites and the influence of adjacent tissues. Development. 1987 Jul;100(3):449–462. doi: 10.1242/dev.100.3.449. [DOI] [PubMed] [Google Scholar]
- Millan F. A., Denhez F., Kondaiah P., Akhurst R. J. Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo. Development. 1991 Jan;111(1):131–143. doi: 10.1242/dev.111.1.131. [DOI] [PubMed] [Google Scholar]
- Olson E. N. Interplay between proliferation and differentiation within the myogenic lineage. Dev Biol. 1992 Dec;154(2):261–272. doi: 10.1016/0012-1606(92)90066-p. [DOI] [PubMed] [Google Scholar]
- Ordahl C. P., Le Douarin N. M. Two myogenic lineages within the developing somite. Development. 1992 Feb;114(2):339–353. doi: 10.1242/dev.114.2.339. [DOI] [PubMed] [Google Scholar]
- Pelton R. W., Saxena B., Jones M., Moses H. L., Gold L. I. Immunohistochemical localization of TGF beta 1, TGF beta 2, and TGF beta 3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development. J Cell Biol. 1991 Nov;115(4):1091–1105. doi: 10.1083/jcb.115.4.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Piette J., Huchet M., Duclert A., Fujisawa-Sehara A., Changeux J. P. Localization of mRNAs coding for CMD1, myogenin and the alpha-subunit of the acetylcholine receptor during skeletal muscle development in the chicken. Mech Dev. 1992 Mar;37(1-2):95–106. doi: 10.1016/0925-4773(92)90018-f. [DOI] [PubMed] [Google Scholar]
- Pourquié O., Coltey M., Teillet M. A., Ordahl C., Le Douarin N. M. Control of dorsoventral patterning of somitic derivatives by notochord and floor plate. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5242–5246. doi: 10.1073/pnas.90.11.5242. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pownall M. E., Emerson C. P., Jr Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Dev Biol. 1992 May;151(1):67–79. doi: 10.1016/0012-1606(92)90214-2. [DOI] [PubMed] [Google Scholar]
- Rong P. M., Teillet M. A., Ziller C., Le Douarin N. M. The neural tube/notochord complex is necessary for vertebral but not limb and body wall striated muscle differentiation. Development. 1992 Jul;115(3):657–672. doi: 10.1242/dev.115.3.657. [DOI] [PubMed] [Google Scholar]
- Selleck M. A., Stern C. D. Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. Development. 1991 Jun;112(2):615–626. doi: 10.1242/dev.112.2.615. [DOI] [PubMed] [Google Scholar]
- Teillet M. A., Le Douarin N. M. Consequences of neural tube and notochord excision on the development of the peripheral nervous system in the chick embryo. Dev Biol. 1983 Jul;98(1):192–211. doi: 10.1016/0012-1606(83)90349-4. [DOI] [PubMed] [Google Scholar]
- Vivarelli E., Cossu G. Neural control of early myogenic differentiation in cultures of mouse somites. Dev Biol. 1986 Sep;117(1):319–325. doi: 10.1016/0012-1606(86)90374-x. [DOI] [PubMed] [Google Scholar]
- Weintraub H., Davis R., Tapscott S., Thayer M., Krause M., Benezra R., Blackwell T. K., Turner D., Rupp R., Hollenberg S. The myoD gene family: nodal point during specification of the muscle cell lineage. Science. 1991 Feb 15;251(4995):761–766. doi: 10.1126/science.1846704. [DOI] [PubMed] [Google Scholar]
- Williams B. A., Ordahl C. P. Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development. 1994 Apr;120(4):785–796. doi: 10.1242/dev.120.4.785. [DOI] [PubMed] [Google Scholar]