Development, Vol 125, Issue 21 4259-4271, Copyright © 1998 by Company of Biologists

JOURNAL ARTICLES

The cellular mechanism by which the dermomyotome contributes to the second wave of myotome development

N Kahane, Y Cinnamon and C Kalcheim
Department of Anatomy and Cell Biology, Hebrew University-Hadassah Medical School, Jerusalem 91120, PO Box 12272, Israel.

We have shown that a subset of early postmitotic progenitors that originates along the medial part of the epithelial somite gives rise to the primary myotome (Kahane, N., Cinnamon, Y. and Kalcheim, C. (1998). Mech. Dev. 74, 59-73). Because of its postmitotic nature, further myotome expansion must be achieved by cell addition from extrinsic sources. Here we investigate the mechanism whereby the dermomyotome contributes to this process. Using several different methods we found that cell addition occurs from both rostral and caudal edges of the dermomyotome, but not directly from its dorsomedial lip (DML). First, labeling of quail embryos with [3H]thymidine revealed a time-dependent entry of radiolabeled nuclei into the myotome from the entire rostral and caudal lips of the dermomyotome, but not from the DML. Second, fluorescent vital dyes were injected at specific sites in the dermomyotome lips and the fate of dye-labeled cells followed by confocal microscopy. Consistent with the nucleotide labeling experiments, dye-labeled myofibers directly emerged from injected epithelial cells from either rostral or caudal lips. In contrast, injected cells from the DML first translocated along the medial boundary, reached the rostral or caudal dermomyotome lips and only then elongated into the myotome. These growing myofibers had always one end attached to either lip from which they elongated in the opposite direction. Third, following establishment of the primary myotome, cells along the extreme dermomyotome edges, but not the DML, expressed QmyoD, supporting the notion that rostral and caudal boundaries generate myofibers. Fourth, ablation of the DML had only a limited effect on myotomal cell number. Thus, cells deriving from the extreme dermomyotome lips contribute to uniform myotome growth in the dorsoventral extent of the myotome. They also account for its expansion in the transverse plane and this is achieved by myoblast addition in a lateral to medial direction (from the dermal to the sclerotomal sides), restricting the pioneer myofibers to the dermal side of the myotome. Taken together, the data suggest that myotome formation is a multistage process. A first wave of pioneers establishes the primary structure. A second wave generated from specific dermomyotome lips contributes to its expansion. Because dermomyotome lip progenitors are mitotically active within the epithelia of origin but exit the cell cycle upon myotome colonization, they can only provide for limited myotome growth and subsequent waves must take over to ensure further muscle development.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				C. Anderson, S. Thorsteinsdottir, and A.-G. Borycki Sonic hedgehog-dependent synthesis of laminin {alpha}1 controls basement membrane assembly in the myotome Development, October 15, 2009; 136(20): 3495 - 3504. [Abstract] [Full Text] [PDF]

				R. Ben-Yair and C. Kalcheim Notch and bone morphogenetic protein differentially act on dermomyotome cells to generate endothelium, smooth, and striated muscle J. Cell Biol., February 6, 2008; 180(3): 607 - 618. [Abstract] [Full Text] [PDF]

				F. Bajanca, M. Luz, K. Raymond, G. G. Martins, A. Sonnenberg, S. Tajbakhsh, M. Buckingham, and S. Thorsteinsdottir Integrin {alpha}6{beta}1-laminin interactions regulate early myotome formation in the mouse embryo Development, May 1, 2006; 133(9): 1635 - 1644. [Abstract] [Full Text] [PDF]

				Y. Cinnamon, R. Ben-Yair, and C. Kalcheim Differential effects of N-cadherin-mediated adhesion on the development of myotomal waves Development, March 15, 2006; 133(6): 1101 - 1112. [Abstract] [Full Text] [PDF]

				R. Grifone, J. Demignon, C. Houbron, E. Souil, C. Niro, M. J. Seller, G. Hamard, and P. Maire Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo Development, May 1, 2005; 132(9): 2235 - 2249. [Abstract] [Full Text] [PDF]

				R. Ben-Yair and C. Kalcheim Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates Development, February 15, 2005; 132(4): 689 - 701. [Abstract] [Full Text] [PDF]

				C. Linker, C. Lesbros, M. R. Stark, and C. Marcelle Intrinsic signals regulate the initial steps of myogenesis in vertebrates Development, October 15, 2003; 130(20): 4797 - 4807. [Abstract] [Full Text] [PDF]

				R. Ben-Yair, N. Kahane, and C. Kalcheim Coherent development of dermomyotome and dermis from the entire mediolateral extent of the dorsal somite Development, September 15, 2003; 130(18): 4325 - 4336. [Abstract] [Full Text] [PDF]

				S. J. Venters and C. P. Ordahl Persistent myogenic capacity of the dermomyotome dorsomedial lip and restriction of myogenic competence Development, March 10, 2003; 129(16): 3873 - 3885. [Abstract] [Full Text] [PDF]

				I. Marics, F. Padilla, J.-F. Guillemot, M. Scaal, and C. Marcelle FGFR4 signaling is a necessary step in limb muscle differentiation Development, January 10, 2002; 129(19): 4559 - 4569. [Abstract] [Full Text] [PDF]

				N. Kahane, Y. Cinnamon, and C. Kalcheim The roles of cell migration and myofiber intercalation in patterning formation of the postmitotic myotome Development, January 6, 2002; 129(11): 2675 - 2687. [Abstract] [Full Text] [PDF]

				S. Eloy-Trinquet and J.-F. Nicolas Clonal separation and regionalisation during formation of the medial and lateral myotomes in the mouse embryo Development, January 1, 2002; 129(1): 111 - 122. [Abstract] [Full Text] [PDF]

				N. Kahane, Y. Cinnamon, I. Bachelet, and C. Kalcheim The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development Development, June 15, 2001; 128(12): 2187 - 2198. [Abstract] [Full Text] [PDF]

				C. Ordahl, E Berdougo, S. Venters, and W. Denetclaw The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium Development, January 5, 2001; 128(10): 1731 - 1744. [Abstract] [PDF]

				W. Denetclaw, E Berdougo, S. Venters, and C. Ordahl Morphogenetic cell movements in the middle region of the dermomyotome dorsomedial lip associated with patterning and growth of the primary epaxial myotome Development, January 5, 2001; 128(10): 1745 - 1755. [Abstract] [PDF]

				Y Cinnamon, N Kahane, I Bachelet, and C Kalcheim The sub-lip domain--a distinct pathway for myotome precursors that demonstrate rostral-caudal migration Development, January 2, 2001; 128(3): 341 - 351. [Abstract] [PDF]

				E Hirsinger, P Malapert, J Dubrulle, M. Delfini, D Duprez, D Henrique, D Ish-Horowicz, and O Pourquie Notch signalling acts in postmitotic avian myogenic cells to control MyoD activation Development, January 1, 2001; 128(1): 107 - 116. [Abstract] [PDF]

				W. Denetclaw and C. Ordahl The growth of the dermomyotome and formation of early myotome lineages in thoracolumbar somites of chicken embryos Development, January 2, 2000; 127(4): 893 - 905. [Abstract] [PDF]

				J Wilson-Rawls, C. Hurt, S. Parsons, and A Rawls Differential regulation of epaxial and hypaxial muscle development by paraxis Development, January 12, 1999; 126(23): 5217 - 5229. [Abstract] [PDF]

				Y Cinnamon, N Kahane, and C Kalcheim Characterization of the early development of specific hypaxial muscles from the ventrolateral myotome Development, January 10, 1999; 126(19): 4305 - 4315. [Abstract] [PDF]

				H Amthor, B Christ, and K Patel A molecular mechanism enabling continuous embryonic muscle growth - a balance between proliferation and differentiation Development, January 2, 1999; 126(5): 1041 - 1053. [Abstract] [PDF]