Abstract
The somite and its intermediate derivatives, sclerotome and dermomyotome (DM), are composed of distinct subdomains based on lineage analysis and gene expression patterns. This sets the grounds for elucidating the mechanisms underlying differential cell specification and morphogenesis. By examining the in vivo roles of N-cadherin on discrete domains of the somitic epithelium at various times, our recent studies highlight the existence of a regional and temporal heterogeneity in cellular responsiveness. As examples of this assortment, we document a coupling between asymmetric cell division and fate segregation in the DM sheet, sequential effects of N-cadherin-mediated adhesion on early myogenic specification compared to later myofiber patterning, and a differential behavior of pioneer myoblasts compared to later myogenic waves.
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References
Ben-Yair R, Kalcheim C (2005) Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates. Development 132:689–701
Ben-Yair R, Kahane N, Kalcheim C (2003) Coherent development of dermomyotome and dermis from the entire mediolateral extent of the dorsal somite. Development 130:4325–4336
Brand-Saberi B, Christ B (2002) Evolution and development of distinct cell lineages derived from somites. Curr Top Dev Biol 48:1–42
Brent AE, Tabin CJ (2002) Developmental regulation of somite derivatives: muscle, cartilage and tendon. Curr Opin Genet Dev 12:548–557
Christ B, Huang R, Scaal M (2004) Formation and differentiation of the avian sclerotome. Anat Embryol (Berl) 208:333–350
Cinnamon Y, Kahane N, Kalcheim C (1999) Characterization of the early development of specific hypaxial muscles from the ventrolateral myotome. Development 126:4305–4315
Cinnamon Y, Kahane N, Bachelet I, Kalcheim C (2001) The sub-lip domain—a distinct pathway for myotome precursors that demonstrate rostral-caudal migration. Development 128:341–351
Cinnamon Y, Ben-Yair R, Kalcheim C (2006) Differential effects of N-cadherin-mediated adhesion on the development of myotomal waves. Development 133:1101–1112
Cole F, Zhang W, Geyra A, Kang JS, Krauss RS (2004) Positive regulation of myogenic bHLH factors and skeletal muscle development by the cell surface receptor CDO. Dev Cell 7:843–854
Cortes F, Daggett D, Bryson-Richardson RJ, Neyt C, Maule J, Gautier P, Hollway GE, Keenan D, Currie PD (2003) Cadherin-mediated differential cell adhesion controls slow muscle cell migration in the developing zebrafish myotome. Dev Cell 5:865–876
Duband JL, Dufour S, Hatta K, Takeichi M, Edelman GM, Thiery JP (1987) Adhesion molecules during somitogenesis in the avian embryo. J Cell Biol 104:1361–1374
Duband JL, Volberg T, Sabanay I, Thiery JP, Geiger B (1988) Spatial and temporal distribution of the adherens-junction-associated adhesion molecule A-CAM during avian embryogenesis. Development 103:325–344
George-Weinstein M, Gerhart J, Blitz J, Simak E, Knudsen KA (1997) N-cadherin promotes the commitment and differentiation of skeletal muscle precursor cells. Dev Biol 185:14–24
Goichberg P, Geiger B (1998) Direct involvement of N-cadherin-mediated signaling in muscle differentiation. Mol Biol Cell 9:3119–3131
Gros J, Scaal M, Marcelle C (2004) A two-step mechanism for myotome formation in chick. Dev Cell 6:875–882
Gros J, Manceau M, Thome V, Marcelle C (2005) A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435:954–958
Gumbiner BM (2000) Regulation of cadherin adhesive activity. J Cell Biol 148:399–404
Holt CE, Lemaire P, Gurdon JB (1994) Cadherin-mediated cell interactions are necessary for the activation of MyoD in Xenopus mesoderm. Proc Natl Acad Sci USA 91:10844–10848
Horikawa K, Takeichi M (2001) Requirement of the juxtamembrane domain of the cadherin cytoplasmic tail for morphogenetic cell rearrangement during myotome development. J Cell Biol 155:1297–1306
Horikawa K, Radice G, Takeichi M, Chisaka O (1999) Adhesive subdivisions intrinsic to the epithelial somites. Dev Biol 215:182–189
Huang R, Christ B (2000) Origin of the epaxial and hypaxial myotome in avian embryos. Anat Embryol (Berl) 202:369–374
Huang RJ, Zhi QX, Patel K, Wilting J, Christ B (2000) Dual origin and segmental organisation of the avian scapula. Development 127:3789–3794
Kaehn K, Jacob HJ, Christ B, Hinrichsen K, Poelmann RE (1988) The onset of myotome formation in the chick. Anat Embryol 177:191–201
Kahane N, Cinnamon Y, Kalcheim C (1998a) The cellular mechanism by which the dermomyotome contributes to the second wave of myotome development. Development 125:4259–4271
Kahane N, Cinnamon Y, Kalcheim C (1998b) The origin and fate of pioneer myotomal cells in the avian embryo. Mech Dev 74:59–73
Kahane N, Cinnamon Y, Bachelet I, Kalcheim C (2001) The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development. Development 128:2187–2198
Kahane N, Cinnamon Y, Kalcheim C (2002) The roles of cell migration and myofiber intercalation in patterning formation of the postmitotic myotome. Development 129:2675–2287
Kalcheim C, Ben-Yair R (2005) Cell rearrangements during development of the somite and its derivatives. Curr Opin Genet Dev 15:1–10
Kalcheim C, Cinnamon Y, Kahane N (1999) Myotome formation: a multistage process. Cell Tissue Res 296:161–173
Kassar-Duchosoy L, Giacone E, Gayraud-Morel B, Jory A, Gomes D, Tajbakhsh S (2005) Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev 19:1426–1431
Knudsen KA, Myers L, McElwee SA (1990) A role for the Ca2(+)-dependent adhesion molecule, N-cadherin, in myoblast interaction during myogenesis. Exp Cell Res 188:175–184
Krauss RS, Cole F, Gaio U, Takaesu G, Zhang W, Kang JS (2005) Close encounters: regulation of vertebrate skeletal myogenesis by cell–cell contact. J Cell Sci 118:2355–2362
Linask KK, Ludwig C, Han MD, Liu X, Radice GL, Knudsen KA (1998) N-cadherin/catenin-mediated morphoregulation of somite formation. Dev Biol 202:85–102
Nelson WJ, Nusse R (2004) Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303:1483–1487
Radice GL, Rayburn H, Matsunami H, Knudsen KA, Takeichi M, Hynes RO (1997) Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181:64–78
Relaix F, Rocancourt D, Mansouri A, Buckingham M (2005) A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435:948–953
Scaal M, Christ B (2004) Formation and differentiation of the avian dermomyotome. Anat Embryol (Berl) 208:411–424
Acknowledgments
We thank M. Takeichi for the N-cadherin DNAs and D. Duprez for MyoD. This work was supported by grants from the Israel Science Foundation, the EEU 6th Framework program Network of Excellence MYORES, the March of Dimes and DFG (SFB 488) to C.K.
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Yuval Cinnamon and Raz Ben-Yair have equally contributed data presented in this study.
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Kalcheim, C., Kahane, N., Cinnamon, Y. et al. Mechanisms of lineage segregation in the avian dermomyotome. Brain Struct Funct 211 (Suppl 1), 31–36 (2006). https://doi.org/10.1007/s00429-006-0116-y
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DOI: https://doi.org/10.1007/s00429-006-0116-y