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Vertebrate Myogenesis pp 187–198Cite as

Cadherins in Skeletal Muscle Development

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Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 38))

Abstract

One essential step in the complex process of myogenesis is the fusion of mononuclear myoblast cells into polynuclear myotubes. This fusion process is promoted by cadherins, a multigene family of transmembrane cell adhesion glycoproteins that mediate homophilic interactions in a calcium-dependent manner, thus selectively associating cells into specific tissues. In the absence of calcium the cadherin molecular conformation is changed, leading to proteolytic digestion of the proteins (Ringwald et al. 1987; Takeichi 1991; Geiger and Ayalon 1992; Huber et al. 1996). Because the expression of cadherins is tissue-specific, many of these molecules have been classified according to the tissues from which they were isolated, such as P-cadherin from placenta, E-cadherin first isolated from epithelial cells or M-cadherin from muscle.

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References

  • Anastasiadis PZ, Reynolds AB (2000) The p120(ctn) catenin family: complex roles in adhesion, signaling and cancer. J Cell Sci 113: 1319–1334

    PubMed  CAS  Google Scholar 

  • Antin P, Forry-Schaudies S, Friedmann TM, Tapscott SJ, Holtzer H (1981) Taxol induces postmitotic myoblasts to assemble interdigitating microtubule-myosin arrays that exclude actin-filaments. J Cell Biol 90: 300–308

    Article  PubMed  CAS  Google Scholar 

  • Aono S, Nakagawa S, Reynolds AB, Takeichi M (1999) p120(ctn) acts as an inhibitory regulator of cadherin function in colon carcinoma cells. J Cell Biol 145(3):551–562

    Google Scholar 

  • Barker N, Clevers H (2000) Catenins, Wnt signaling and cancer. Bioessays 22 (11): 961–965

    Article  PubMed  CAS  Google Scholar 

  • Barth AI, Nathke IS, Nelson WJ (1997) Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr Opin Cell Biol 9 (5): 683–690

    Article  PubMed  CAS  Google Scholar 

  • Behrens J (1999) Cadherins and catenins: role in signal transduction and tumor progression. Cancer Metastasis Rev 18 (1): 15–30

    Article  PubMed  CAS  Google Scholar 

  • Bornemann A, Schmalbruch H (1994) Immunocytochemistry of M-cadherin in mature and regenerating rat muscle. Anat Rec 239: 119–125

    Article  PubMed  CAS  Google Scholar 

  • Brand-Saberi B, Gamel AJ, Krenn V, Müller TS, Wilting J, Christ B (1996) N-cadherin is involved

    Google Scholar 

  • in myoblast migration and muscle differentiation in the avian limb bud. Dev Biol 178:160–173 Butz S, Kemler R (1994) Distinct cadherin-catenin complexes in Ca (2+) -dependent cell-cell adhesion. FEBS Lett 355: 195–200

    Google Scholar 

  • Charlton CA, Mohler WA, Radice G, Hynes RO, Blau H (1997) Fusion competence of myoblasts rendered genetically null for N-cadherin in culture. J Cell Biol 138: 331–336

    Article  PubMed  CAS  Google Scholar 

  • Chothia C, Jones EY (1997) The molecular structure of cell adhesion molecules. Annu Rev Biochem 66: 823–862

    Article  PubMed  CAS  Google Scholar 

  • Cornelison DD, Olwin BB, Rudnicki MA, Wold BJ (2000) MyoD(-/-) satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev Biol 15: 122–137

    Article  Google Scholar 

  • Donalies M, Cramer M, Ringwald M, Starzinski-Powitz A (1991) Expression of M-cadherin, a member of the cadherin multigene family, correlates with differentiation of skeletal muscle cells. Proc Natl Acad Sci USA 88: 8024–8028

    Article  PubMed  CAS  Google Scholar 

  • Eng H, Herrenknecht K, Semb H, Starzinski-Powitz A, Ringertz N, Gullberg D (1997) Effects of divalent cations on M-cadherin expression and distribution during primary rat myogenesis in vitro. Differentiation 61 (3): 169–176

    Article  PubMed  CAS  Google Scholar 

  • Geiger B,Ayalon 0 (1992) Cadherins. Annu Rev Cell Biol 8: 307–332

    Article  CAS  Google Scholar 

  • George-Weinstein M, Gerhart J, Blitz J, Simak E, Knudsen K (1997) N-cadherin promotes the com- mitment 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 dif- ferentiation. Mol Biol Cell 9 (11): 3119–3131

    Google Scholar 

  • Hazan RB, Phillips GR, Qiao RF, Norton L, Aaronson SA (2000) Exogenous expression of Ncadherin in breast cancer cells induces cell migration, invasion, and metastasis. J Cell Biol 148 (4): 779–790

    Article  PubMed  CAS  Google Scholar 

  • Hertig CM, Butz S, Koch S, Eppenberger-Ebehardt M, Kemler R, Eppenberger HM (1996) Ncadherin in adult rat cardiomyocytes in culture. II. Spatio-temporal appearance of proteins involved in cell-cell contact communication. Formation of two distinct N-cadherin/catenin complexes. J Cell Sci 109: 11–20

    Google Scholar 

  • Hinck L, Näthke IS, Papkoff J Nelson WJ (1994) Dynamics of cadherin-catenin complex formation: novel protein interactions and pathways of complex assembly. J Cell Biol 125: 1327–1340

    Article  PubMed  CAS  Google Scholar 

  • Hirano S, Kimoto N, Shimoyama Y, Hirohashi S Takeichi M (1992) Identification of a neural alphacatenin as a key regulator of cadherin function and multicellular organization. Cell 70: 293–301

    Article  PubMed  CAS  Google Scholar 

  • Holtzer H, Forry-Schaudies S, Dlugosz A, Antin P, Dubyak G (1985) Interaction between intermediate filaments, microtubules, and myofibrils in fibrogenic and myogenic cells. Ann NY Acad Sci 455: 106–125

    Article  PubMed  CAS  Google Scholar 

  • Huber O, Bierkamp C, Kemler R (1996) Cadherins and catenins in development. Curr Opin Cell Biol 8: 685–691

    Article  PubMed  Google Scholar 

  • Humphries MJ, Newham P (1998) The structure of cell-adhesion molecules. Trends Cell Biol 8 (2): 78–83

    Article  PubMed  CAS  Google Scholar 

  • Hutton J, Christofori G, Chi W, Edman U, Guest P, Hanahan D, Kelly RB (1993) Molecular cloning of mouse pancreatic islet R-cadherin: differential expression in endocrine and exocrine tissue. Mol Endocrinol 7: 1151–1160

    Article  PubMed  CAS  Google Scholar 

  • Inuzuka H, Miyatani S, Takeichi M (1991) R-cadherin: a novel Ca (2+)-dependent cell-cell adhesion molecule expressed in the retina. Neuron 7: 69–79

    Article  PubMed  CAS  Google Scholar 

  • Irintchev A, Zeschnigk M, Starzinski-Powitz A, Wernig A (1994) Expression pattern of M- Cadherin in normal, denervated and regenerating mouse muscle. Dev Dyn 199:326–337 Kaufmann U, Martin B, Link D, Witt K, Zeitler R, Reinhard S, Starzinski-Powitz A (1999a) M- cadherin and its sisters in development of striated muscle. Cell Tissue Res 296:191–198 Kaufmann U, Kirsch J, Irintchev A, Wernig A, Starzinski-Powitz A (1999b) The M-cadher in catenin

    Google Scholar 

  • complex interacts with microtubules in skeletal muscle cells: implications for the fusion of myoblasts. J Cell Sci 112:55–67

    Google Scholar 

  • Kaufmann U, Zuppinger C, Waibler Z, Rudiger M, Urbich C, Martin B, Jockusch BM, Eppenberger H, Starzinski-Powitz A (2000) The armadillo repeat region targets ARVCF to cadherin-based cellular junctions. J Cell Sci 113: 4121–4135

    PubMed  CAS  Google Scholar 

  • Knudsen KA, Myers L, McElwere SA (1990) A role for the Ca 2+-dependent adhesion molecule, Ncadherin, in myoblast interaction during myogenesis. Exp Cell Res 188: 175–184

    Google Scholar 

  • Knudsen KA, Soler AP, Johnson KR, Wheelock MJ (1995) Interaction of alpha-actinin with the cadherin/catenin cell-cell adhesion complex via alpha-catenin. J Cell Biol 130: 67–77

    Article  PubMed  CAS  Google Scholar 

  • Kuch C,Winnekendonk D, Butz S, Unvericht U, Kemler R, Starzinski-Powitz A (1997) M-cadherinmediated cell adhesion and complex formation with the catenins in myogenic mouse cells. Exp Cell Res 232: 331–338

    Article  PubMed  CAS  Google Scholar 

  • Li H, Choudhary SK, Milner DJ, Munir MI, Kuisk IR, Capetanaki Y (1994) Inhibition of desmin expression blocks myoblast fusion and interferes with myogenic regulator MyoD and myogenin. J Cell Biol 124: 827–841

    Article  PubMed  CAS  Google Scholar 

  • Linask KK, Knudsen KA, Gui YH (1997) N-cadherin-catenin interaction: necessary component of cardiac cell compartmentalization during early vertebrate heart development. Dev Biol 185 (2): 148–164

    Article  PubMed  CAS  Google Scholar 

  • Linask KK, Ludwig C, Han MD, Liu X, Radice GL, Knudsen KA (1998) N-cadherin/cateninmediated morphoregulation of somite formation. Dev Biol 202 (1): 85–102

    Article  PubMed  CAS  Google Scholar 

  • Mariner DJ, Wang J, Reynolds AB (2000) ARVCF localizes to the nucleus and adherens junction and is mutually exclusive with p120(ctn)(ctn) in E-cadherin complexes. J Cell Sci 113: 1481–8490

    PubMed  CAS  Google Scholar 

  • Matsunami H, Miyatani S, Inoue T, Copland NG, Gilbert DJ, Jenkins NA, Takeichi M (1993) Cell binding specificity of mouse R-cadherin and chromosomal mapping of the gene. J Cell Sci 106: 401–409

    PubMed  CAS  Google Scholar 

  • Mège RM, Goudou D, Diaz C, Nicolet M, Garcia L, Geraud G, Rieger F (1992) N-cadherin and N-CAM in myoblast fusion: compared localisation and effect of blockade by peptides and antibodies. J Cell Sci 103: 897–906

    PubMed  Google Scholar 

  • Miller JR, Moon RT (1996) Signal transduction through beta-catenin and specification of cell fate during embryogenesis. Genes Dev 10 (20): 2527–2539

    Article  PubMed  CAS  Google Scholar 

  • Moore R, Walsh F (1993) The cell adhesion molecule M-cadherin is specifically expressed in devel- oping and regenerating, but not denervated skeletal muscle. Development 117:1409–1420 Nose A, Tsuji K, Takeichi M (1990) Localization of specificity determining sites in cadherin cell adhesion molecules. Cell 61 (1): 147–155

    Google Scholar 

  • Ontell M, Kozeka K (1984) The organogenesis of murine striated muscle: a cytoarchitectural study. Am J Anat 171: 133–148

    Article  PubMed  CAS  Google Scholar 

  • Ozawa M, Kemler R (1990) Correct proteolytic cleavage is required for the cell adhesive function of uvomorulin. J Cell Biol 111 (4): 1645–1650

    Article  PubMed  CAS  Google Scholar 

  • Ozawa M, Baribault H Kemler R (1989) The cytoplasmatic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8: 1711–1717

    PubMed  CAS  Google Scholar 

  • Pouliot Y, Gravel M, Holland PC (1994) Developmental regulation of M-cadherin in the terminal differentiation of skeletal myoblasts. Dev Dyn 200: 305–312

    Article  PubMed  CAS  Google Scholar 

  • Provost E, Rimm DL (1999) Controversies at the cytoplasmic face of the cadherin-based adhesion complex. Curr Opin Cell Biol 11 (5): 567–572

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Redfield A, Nieman MT, Knudsen KA (1997) Cadherins promote skeletal muscle differentiation in three-dimensional cultures. J Cell Sci 138: 1323–1331

    CAS  Google Scholar 

  • Redies C, Takeichi M (1993) N- and R-cadherin expression in the optic nerve of the chicken embryo. Glia 8 (3): 161–171

    Article  PubMed  CAS  Google Scholar 

  • Reynolds AB, Daniel J, McCrea PD, Wheelock MJ, Wu J, Zhang Z (1994) Identification of a new catenin: the tyrosine kinase substrate p120(ctn)cas associates with E-cadherin complexes. Mol Cell Biol 14 (12): 8333–8342

    PubMed  CAS  Google Scholar 

  • Ringwald M, Schuh R, Vestweber D, Eistetter H, Lottspeich F, Engel J, Dölz R, Jähnig F, Epplen J, Mayer S, Müller C, Kemler R (1987) The structure of the cell adhesion molecule uvomorulin. Insights into the molecular mechanism of Ca’ dependent cell adhesion. EMBO J 6: 3647–3653

    Google Scholar 

  • Rose O, Rohwedel J, Reinhard S, Bachmann M, Cramer M, Rotter M, Wobus A, Starzinski-Powitz A (1994) Expression of M-cadherin protein in myogenic cells during prenatal mouse development and differentiation of embryonic stem cells in culture. Dev Dyn 201: 245–259

    Article  PubMed  CAS  Google Scholar 

  • Rose O, Grund C, Reinhardt S, Starzinski-Powitz A, Franke WW (1995) Contactus adhaerens, a special type of plaque-bearing adhering junction containing M-cadherin, in the granule layer of the cerebellar glomerulus. Proc Natl Acad Sci USA 92: 6022–6026

    Article  PubMed  CAS  Google Scholar 

  • Rosenberg P, Esni F, Sjodin A, Larue L, Carlsson L, Gullberg D, Takeichi M, Kemler R, Semb H (1997) A potential role of R-cadherin in striated muscle formation. Dev Biol 187: 55–70

    Article  PubMed  CAS  Google Scholar 

  • Sabourin LA, Girgis-Gabardo A, Seale P, Asakura A, Rudnicki MA (1999) Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle. J Cell Biol 22: 631–643

    Article  Google Scholar 

  • Saitoh O, Aria T, Obinata T (1988) Distribution of microtubules and other cytoskeletal filaments during myotube elongation as revealed by fluorescence microscopy. Cell Tissue Res 252: 263–273

    Article  PubMed  CAS  Google Scholar 

  • Seghatoleslami MR, Myers L, Knudsen KA (2000) Upregulation of myogenin by N-cadherin adhesion in three-dimensional cultures of skeletal myogenic BHK cells. J Cell Biochem 77 (2): 252–264

    Article  PubMed  CAS  Google Scholar 

  • Shan WS, Tanaka H, Phillips GR, Arndt K, Yoshida M, Colman DR, Shapiro L (2000) Functional cis-heterodimers of N- and R-cadherins. J Cell Biol 148 (3): 579–590

    Article  PubMed  CAS  Google Scholar 

  • Shapiro L, Fannon AM, Kwong PD, Thompson A, Lehmann MS, Grübel G, Legrand IP, Als-Nielsen J, Colman DR, Hendrickson WA (1995) Structural basis of cell-cell adhesion by cadherins. Nature 374: 327–336

    Article  PubMed  CAS  Google Scholar 

  • Shin CS, Lecanda F, Sheikh S, Weitzmann L, Cheng SL, Civitelli R (2000) Relative abundance of different cadherins defines differentiation of mesenchymal precursors into osteogenic, myogenic, or adipogenic pathways. J Cell Biochem 78 (4): 566–577

    Article  PubMed  CAS  Google Scholar 

  • Soler AP, Knudsen KA (1994) N-cadherin involvement in cardiac myocyte interaction and myofibrillogenesis. Dev Biol 162 (1): 9–17

    Article  PubMed  CAS  Google Scholar 

  • Steinberg MS, McNutt PM (1999) Cadherins and their connections: adhesion junctions have broader functions. Curr Opin Cell Bioll l(5): 554–560

    Google Scholar 

  • Tachibana K, Nakanishi H, Mandai K, Ozaki K, Ikeda W, Yamamoto Y, Nagafuchi A, Tsukita S, Takai Y (2000) Two cell adhesion molecules, nectin and cadherin, interact through their cytoplasmic domain-associated proteins. J Cell Biol 150 (5): 1161–1176

    Article  PubMed  CAS  Google Scholar 

  • Takeda H, Shimoyama Y, Nagafuchi A, Hirohashi S (1999) E-cadherin functions as a cis-dimer at the cell-cell adhesive interface in vivo. Nat Struct Biol 6 (4): 310–312

    Article  PubMed  CAS  Google Scholar 

  • Takeichi M (1991) Cadherin cell adhesion receptors as a morphogenic regulator. Science 251: 1451–1455

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Shan WS, Hendrickson WA, Colman DR, Shapiro L (1998) Structure-function analysis of cell adhesion by neuronal ( N-) cadherin. Neuron 20: 1153–1163

    Google Scholar 

  • Tao J, Wallace I (1991) Site-specific antibodies block kinase A phosphorylation of desmin in vitro and inhibit incorporation of myoblasts into myotubes. Cell Motil Cytoskel 19:109–120

    Article  CAS  Google Scholar 

  • Tepass U (1999) Genetic analysis of cadherin function in animal morphogenesis. Curr Op in Cell Biol 11:540–548

    Article  CAS  Google Scholar 

  • Toyama Y, Forry-Scahudies S, Hoffmann B, Holtzer H (1982) Effects of taxol and colcemid on myofibrillogenesis. Proc Nat Sci USA 79: 6556–6560

    Article  CAS  Google Scholar 

  • Yap AS, Niessen CM, Gumbiner BM (1998) The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening, and interaction with p120(ctn)ctn. J Cell Biol 141 (3): 779–789

    Article  PubMed  CAS  Google Scholar 

  • Zeschnigk M, Kozian D, Kuch C, Schmoll M, Starzinski-Powitz A (1995) Involvement of M- cadherin in fusion and terminal differentiation of myogenic cells. J Cell Sci 108: 2973–2981

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institut für Anthropologie und Humangenetik für Biologen, Johann Wolfgang Goethe Universität, Siesmayerstr. 70, 60323, Frankfurt am Main, Germany

    Anna Starzinski-Powitz

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  1. Zoe Waibler
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Editors and Affiliations

  1. Institute of Anatomy II, Albert Ludwigs University Freiburg, Albertstraße 17, 79104, Freiburg, Germany

    Beate Brand-Saberi

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© 2002 Springer-Verlag Berlin Heidelberg

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Waibler, Z., Starzinski-Powitz, A. (2002). Cadherins in Skeletal Muscle Development. In: Brand-Saberi, B. (eds) Vertebrate Myogenesis. Results and Problems in Cell Differentiation, vol 38. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-45686-5_9

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  • DOI: https://doi.org/10.1007/978-3-540-45686-5_9

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