Crossref journal-article
The Company of Biologists
Journal of Cell Science (237)
Abstract

The strong coordinated contraction of heart muscle is dependent on the correct alignment and connection of the myofibrils across the plasma membrane. Previous studies indicate that N-cadherin is involved in cardiac myocyte adhesion and myofibrillogenesis. To investigate whether N-cadherin is specifically required for normal myocyte structure and function, we cultured myocytes from wild-type, N-cadherin-null and mutant embryos expressing the epithelial cadherin E-cadherin. In contrast to previous studies in chicken using N-cadherin-perturbing antibodies, our in vitro studies with mouse cells demonstrate that N-cadherin is not required for myofibrillogenesis, but is critical for myofibril organization. That is, N-cadherin-deficient myocytes beat and myofibrils were well formed; however, alignment of the myofibrils through regions of cell-cell contact was lost, resulting in their random orientation. Gap junctions were perturbed in the N-cadherin-null myocytes. By contrast, focal contacts appeared normal in the mutant cells. Furthermore,E-cadherin restored normal cell morphology and behavior to the N-cadherin-deficient myocytes, including proper alignment of the myofibrils. We conclude that a different adhesive system, most probably integrin, is responsible for myofibrillogenesis in the N-cadherin-null myocytes.

Bibliography

Luo, Y., & Radice, G. L. (2003). Cadherin-mediated adhesion is essential for myofibril continuity across the plasma membrane but not for assembly of the contractile apparatus. Journal of Cell Science, 116(8), 1471–1479.

Authors 2 University of Pennsylvania
  1. Yang Luo (first) University of Pennsylvania
  2. Glenn L. Radice (additional) University of Pennsylvania
References 51 Referenced 66
  1. Anastasiadis, P. Z. and Reynolds, A. B. (2000). The p120 catenin family: complex roles in adhesion, signaling and cancer. J. Cell Sci.113,1319-1334. (10.1242/jcs.113.8.1319)
  2. Carver, W., Price, R. L., Raso, D. S., Terracio, L. and Borg, T. K. (1994). Distribution of beta-1 integrin in the developing rat heart. J. Histochem. Cytochem.42,167-175. (10.1177/42.2.8288862)
  3. Conacci-Sorrell, M., Zhurinsky, J. and Ben-Ze'ev, A.(2002). The cadherin-catenin adhesion system in signaling and cancer. J. Clin. Invest.109,987-991. (10.1172/JCI0215429)
  4. Dlugosz, A. A., Antin, P. B., Nachmias, V. T. and Holtzer,H. (1984). The relationship between stress fiber-like structures and nascent myofibrils in cultured cardiac myocytes. J. Cell Biol.99,2268-2278. (10.1083/jcb.99.6.2268)
  5. Duband, J. L., Volberg, T., Sabanay, I., Thiery, J. P. and Geiger, B. (1988). Spatial and temporal distribution of the adherens-junction-associated adhesion molecule A-CAM during avian embryogenesis. Development103,325-344. (10.1242/dev.103.2.325)
  6. Epstein, H. F. and Fischman, D. A. (1991). Molecular analysis of protein assembly in muscle development. Science251,1039-1044. (10.1126/science.1998120)
  7. Fassler, R., Rohwedel, J., Maltsev, V., Bloch, W., Lentini, S.,Guan, K., Gullberg, D., Hescheler, J., Addicks, K. and Wobus, A. M.(1996). Differentiation and integrity of cardiac muscle cells are impaired in the absence of beta 1 integrin. J. Cell Sci.109,2989-2999. (10.1242/jcs.109.13.2989)
  8. Ferreira-Cornwell, M. C., Luo, Y., Narula, N., Lenox, J. M.,Lieberman, M. and Radice, G. L. (2002). Remodeling the intercalated disc leads to cardiomyopathy in mice misexpressing cadherins in the heart. J. Cell Sci.115,1623-1634. (10.1242/jcs.115.8.1623)
  9. Frenzel, E. M. and Johnson, R. G. (1996). Gap junction formation between cultured embryonic lens cells is inhibited by antibody to N-cadherin. Dev. Biol.179, 1-16. (10.1006/dbio.1996.0237)
  10. Geiger, B. (1979). A 130K protein from chicken gizzard: its localization at the termini of microfilament bundles in cultured chicken cells. Cell18,193-205. (10.1016/0092-8674(79)90368-4)
  11. Goncharova, E. J., Kam, Z. and Geiger, B.(1992). The involvement of adherens junction components in myofibrillogenesis in cultured cardiac myocytes. Development114,173-183. (10.1242/dev.114.1.173)
  12. Gulick, J., Subramaniam, A., Neumann, J. and Robbins, J.(1991). Isolation and characterization of the mouse cardiac myosin heavy chain genes. J. Biol. Chem.266,9180-9185. (10.1016/S0021-9258(18)31568-0)
  13. Gumbiner, B. M. (2000). Regulation of cadherin adhesive activity. J. Cell Biol.148,399-403. (10.1083/jcb.148.3.399)
  14. Hatta, K., Takagi, S., Fujisawa, H. and Takeichi, M.(1987). Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos. Dev. Biol.120,215-227. (10.1016/0012-1606(87)90119-9)
  15. Hertig, C. M., Butz, S., Koch, S., Eppenberger-Eberhardt, M.,Kemler, R. and Eppenberger, H. M. (1996a). N-cadherin in adult rat cardiomyocytes in culture. II. Spatio-temporal appearance of proteins involved in cell-cell contact and communication. Formation of two distinct N-cadherin/catenin complexes. J. Cell Sci.109, 11-20. (10.1242/jcs.109.1.11)
  16. Hertig, C. M., Eppenberger-Eberhardt, M., Koch, S. and Eppenberger, H. M. (1996b). N-cadherin in adult rat cardiomyocytes in culture. I. Functional role of N-cadherin and impairment of cell-cell contact by a truncated N-cadherin mutant. J. Cell Sci.109,1-10. (10.1242/jcs.109.1.1)
  17. Hilenski, L. L., Ma, X. H., Vinson, N., Terracio, L. and Borg,T. K. (1992). The role of beta 1 integrin in spreading and myofibrillogenesis in neonatal rat cardiomyocytes in vitro. Cell Motil. Cytoskeleton21,87-100. (10.1002/cm.970210202)
  18. Huttenlocher, A., Lakonishok, M., Kinder, M., Wu, S., Truong,T., Knudsen, K. A. and Horwitz, A. F. (1998). Integrin and cadherin synergy regulates contact inhibition of migration and motile activity. J. Cell Biol.141,515-526. (10.1083/jcb.141.2.515)
  19. Imanaka-Yoshida, K., Knudsen, K. A. and Linask, K. K.(1998). N-cadherin is required for the differentiation and initial myofibrillogenesis of chick cardiomyocytes. Cell Motil. Cytoskeleton39,52-62. (10.1002/(SICI)1097-0169(1998)39:1<52::AID-CM5>3.0.CO;2-I)
  20. Imanaka-Yoshida, K., Enomoto-Iwamoto, M., Yoshida, T. and Sakakura, T. (1999). Vinculin, talin, integrinα6β1 and laminin can serve as components of attachment complex mediating contraction force transmission from cardiomyocytes to extracellular matrix. Cell Motil. Cytoskeleton42, 1-11.
  21. Iwai, Y., Usui, T., Hirano, S., Steward, R., Takeichi, M. and Uemura, T. (1997). Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron19,77-89. (10.1016/S0896-6273(00)80349-9)
  22. Janssens, B., Goossens, S., Staes, K., Gilbert, B., van Hengel,J., Colpaert, C., Bruyneel, E., Mareel, M. and van Roy, F.(2001). αT-catenin: a novel tissue-specific beta-catenin-binding protein mediating strong cell-cell adhesion. J. Cell Sci.114,3177-3188. (10.1242/jcs.114.17.3177)
  23. Jongen, W. M., Fitzgerald, D. J., Asamoto, M., Piccoli, C.,Slaga, T. J., Gros, D., Takeichi, M. and Yamasaki, H.(1991). Regulation of connexin 43-mediated gap junctional intercellular communication by Ca2+ in mouse epidermal cells is controlled by E-cadherin. J. Cell Biol.114,545-555. (10.1083/jcb.114.3.545)
  24. Knudsen, K. A., Soler, A. P., Johnson, K. R. and Wheelock, M. J. (1995). Interaction of α-actinin with the cadherin/catenin cell-cell adhesion complex via α-catenin. J. Cell Biol.130,67-77. (10.1083/jcb.130.1.67)
  25. Kostetskii, I., Moore, R., Kemler, R. and Radice, G. L.(2001). Differential adhesion leads to segregation and exclusion of N-cadherin-deficient cells in chimeric embryos. Dev. Biol.234,72-79. (10.1006/dbio.2001.0250)
  26. Kostin, S., Hein, S., Bauer, E. P. and Schaper, J.(1999). Spatiotemporal development and distribution of intercellular junctions in adult rat cardiomyocytes in culture. Circ. Res.85,154-167. (10.1161/01.RES.85.2.154)
  27. Lin, Z. X., Holtzer, S., Schultheiss, T., Murray, J., Masaki,T., Fischman, D. A. and Holtzer, H. (1989). Polygons and adhesion plaques and the disassembly and assembly of myofibrils in cardiac myocytes. J. Cell Biol.108,2355-2367. (10.1083/jcb.108.6.2355)
  28. Lu, M. H., DiLullo, C., Schultheiss, T., Holtzer, S., Murray, J. M., Choi, J., Fischman, D. A. and Holtzer, H. (1992). The vinculin/sarcomeric-alpha-actinin/alpha-actin nexus in cultured cardiac myocytes. J. Cell Biol.117,1007-1022. (10.1083/jcb.117.5.1007)
  29. Luo, Y., Ferreira-Cornwell, M., Baldwin, H., Kostetskii, I.,Lenox, J., Lieberman, M. and Radice, G. (2001). Rescuing the N-cadherin knockout by cardiac-specific expression of N- or E-cadherin. Development128,459-469. (10.1242/dev.128.4.459)
  30. Meyer, R. A., Laird, D. W., Revel, J. P. and Johnson, R. G.(1992). Inhibition of gap junction and adherens junction assembly by connexin and A-CAM antibodies. J. Cell Biol.119,179-189. (10.1083/jcb.119.1.179)
  31. Miyatani, S., Shimamura, K., Hatta, M., Nagafuchi, A., Nose, A. and Matsunaga, M. (1989). Neural cadherin: role in selective cell-cell adhesion. Science245,631-635. (10.1126/science.2762814)
  32. Monier-Gavelle, F. and Duband, J. L. (1997). Cross talk between adhesion molecules: control of N-cadherin activity by intracellular signals elicited by β1 and β3 integrins in migrating neural crest cells. J. Cell Biol.137,1663-1681. (10.1083/jcb.137.7.1663)
  33. Pardo, J. V., Siliciano, J. D. and Craig, S. W.(1983). Vinculin is a component of an extensive network of myofibril-sarcolemma attachment regions in cardiac muscle fibers. J. Cell Biol.97,1081-1088. (10.1083/jcb.97.4.1081)
  34. Peralta Soler, A. and Knudsen, K. A. (1994). N-cadherin involvement in cardiac myocyte interaction and myofibrillogenesis. Dev. Biol.162,9-17. (10.1006/dbio.1994.1062)
  35. Radice, G. L., Rayburn, H., Matsunami, H., Knudsen, K. A.,Takeichi, M. and Hynes, R. O. (1997). Developmental defects in mouse embryos lacking N-cadherin. Dev. Biol.181, 64-78. (10.1006/dbio.1996.8443)
  36. Rhee, D., Sanger, J. M. and Sanger, J. W.(1994). The premyofibril: evidence for its role in myofibrillogenesis. Cell Motil. Cytoskeleton28, 1-24. (10.1002/cm.970280102)
  37. Rimm, D. L., Koslov, E. R., Kebriaei, P., Cianci, C. D. and Morrow, J. S. (1995). α1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc. Natl. Acad. Sci. USA92,8813-8817. (10.1073/pnas.92.19.8813)
  38. Ross, R. S. and Borg, T. K. (2001). Integrins and the myocardium. Circ. Res.88,1112-1119. (10.1161/hh1101.091862)
  39. Shai, S. Y., Harpf, A. E., Babbitt, C. J., Jordan, M. C.,Fishbein, M. C., Chen, J., Omura, M., Leil, T. A., Becker, K. D., Jiang, M. et al. (2002). Cardiac myocyte-specific excision of the β1 integrin gene results in myocardial fibrosis and cardiac failure. Circ. Res.90,458-464. (10.1161/hh0402.105790)
  40. Shan, W. S., Tanaka, H., Phillips, G. R., Arndt, K., Yoshida,M., Colman, D. R. and Shapiro, L. (2000). Functional cis-heterodimers of N- and R-cadherins. J. Cell Biol.148,579-590. (10.1083/jcb.148.3.579)
  41. Shiraishi, I., Simpson, D. G., Carver, W., Price, R., Hirozane,T., Terracio, L. and Borg, T. K. (1997). Vinculin is an essential component for normal myofibrillar arrangement in fetal mouse cardiac myocytes. J. Mol. Cell. Cardiol.29,2041-2052. (10.1006/jmcc.1997.0438)
  42. Tepass, U., Gruszynski-DeFeo, E., Haag, T. A., Omatyar, L.,Torok, T. and Hartenstein, V. (1996). shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neuroectoderm and other morphogenetically active epithelia. Genes Dev.10,672-685. (10.1101/gad.10.6.672)
  43. Tepass, U., Truong, K., Godt, D., Ikura, M. and Peifer, M.(2000). Cadherins in embryonic and neural morphogenesis. Nat. Rev. Mol. Cell. Biol.1, 91-100. (10.1038/35040042)
  44. Terracio, L., Rubin, K., Gullberg, D., Balog, E., Carver, W.,Jyring, R. and Borg, T. K. (1991). Expression of collagen binding integrins during cardiac development and hypertrophy. Circ. Res.68,734-744. (10.1161/01.RES.68.3.734)
  45. Volk, T. and Geiger, B. (1984). A 135-kd membrane protein of intercellular adherens junctions. EMBO J.3,2249-2260. (10.1002/j.1460-2075.1984.tb02123.x)
  46. Volk, T. and Geiger, B. (1986). A-CAM: a 135-kD receptor of intercellular adherens junctions. I. Immunoelectron microscopic localization and biochemical studies. J. Cell Biol.103,1441-1450.
  47. Watabe-Uchida, M., Uchida, N., Imamura, Y., Nagafuchi, A.,Fujimoto, K., Uemura, T., Vermeulen, S., van Roy, F., Adamson, E. D. and Takeichi, M. (1998). alpha-Catenin-vinculin interaction functions to organize the apical junctional complex in epithelial cells. J. Cell Biol.142,847-857. (10.1083/jcb.142.3.847)
  48. Wu, J.-C., Chung, T.-H., Tseng, Y.-Z. and Wang, S.-M.(1999). N-cadherin/catenin-based costameres in cultured chicken cardiomyocytes. J. Cell. Biochem.75, 93-104. (10.1002/(SICI)1097-4644(19991001)75:1<93::AID-JCB10>3.0.CO;2-O)
  49. Wu, J.-C., Sung, H.-C., Chung, T.-H. and DePhilip, R. M.(2002). Role of N-cadherin- and integrin-based costameres in the development of rat cardiomyocytes. J. Cell. Biochem.84,717-724. (10.1002/jcb.10092)
  50. Xu, X., Li, W. E., Huang, G. Y., Meyer, R., Chen, T., Luo, Y.,Thomas, M. P., Radice, G. L. and Lo, C. W. (2001). Modulation of mouse neural crest cell motility by N-cadherin and connexin 43 gap junctions. J. Cell Biol.154,217-230. (10.1083/jcb.200105047)
  51. Zuppinger, C., Schaub, M. C. and Eppenberger, H. M.(2000). Dynamics of early contact formation in cultured adult rat cardiomyocytes studied by N-cadherin fused to green fluorescent protein. J. Mol. Cell. Cardiol.32,539-555. (10.1006/jmcc.1999.1086)
Dates
Type When
Created 22 years, 5 months ago (March 14, 2003, 12:08 p.m.)
Deposited 1 year, 7 months ago (Jan. 9, 2024, 12:55 a.m.)
Indexed 11 months, 3 weeks ago (Sept. 7, 2024, 7:53 p.m.)
Issued 22 years, 4 months ago (April 15, 2003)
Published 22 years, 4 months ago (April 15, 2003)
Published Print 22 years, 4 months ago (April 15, 2003)
Funders 0

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@article{Luo_2003, title={Cadherin-mediated adhesion is essential for myofibril continuity across the plasma membrane but not for assembly of the contractile apparatus}, volume={116}, ISSN={0021-9533}, url={http://dx.doi.org/10.1242/jcs.00339}, DOI={10.1242/jcs.00339}, number={8}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={Luo, Yang and Radice, Glenn L.}, year={2003}, month=apr, pages={1471–1479} }