N-Cadherin-mediated adhesion and signaling from development to disease: Lessons from mice

Progress in Molecular Biology and Translational Science

Volumn 116, Issue , 2013, Pages 263-289

  Radice, Glenn L ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Adherens junction; Arrhythmia; Cancer; Cardiac intercalated disc; Cardiomyopathy; Connexin43; Gap junction

Indexed keywords

EID: 84875248707     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394311-8.00012-1     Document Type: Chapter

References (96)

1. G.B. Grunwald, R.S. Pratt, and J. Lilien Enzymic dissection of embryonic cell adhesive mechanisms. III. Immunological identification of a component of the calcium-dependent adhesive system of embryonic chick neural retina cells J Cell Sci 55 1982 69 83
2. T. Volk, and B. Geiger A 135-kd membrane protein of intercellular adherens junctions EMBO J 3 1984 2249 2260
3. K. Hatta, T.S. Okada, and M. Takeichi A monoclonal antibody disrupting calcium-dependent cell-cell adhesion of brain tissues: possible role of its target antigen in animal pattern formation Proc Natl Acad Sci USA 82 1985 2789 2793
4. K. Hatta, A. Nose, A. Nagafuchi, and M. Takeichi Cloning and expression of cDNA encoding a neural calcium-dependent cell adhesion molecule: its identity in the cadherin gene family J Cell Biol 106 1988 873 881
5. L. Shapiro, A.M. Fannon, P.D. Kwong, A. Thompson, M.S. Lehmann, and G. Grubel Structural basis of cell-cell adhesion by cadherins Nature 374 1995 327 337
6. U. Dahl, A. Sjodin, L. Larue, G.L. Radice, S. Cajander, and M. Takeichi Genetic dissection of cadherin function during nephrogenesis Mol Cell Biol 22 2002 1474 1487
7. A. Hollnagel, C. Grund, W.W. Franke, and H.H. Arnold The cell adhesion molecule M-cadherin is not essential for muscle development and regeneration Mol Cell Biol 22 2002 4760 4770
8. G.L. Radice, M.C. Ferreira-Cornwell, S.D. Robinson, H. Rayburn, L.A. Chodosh, and M. Takeichi Precocious mammary gland development in P-cadherin-deficient mice J Cell Biol 139 1997 1025 1032
9. G.L. Radice, H. Rayburn, H. Matsunami, K.A. Knudsen, M. Takeichi, and R.O. Hynes Developmental defects in mouse embryos lacking N-cadherin Dev Biol 181 1997 64 78
10. Y. Luo, M. Ferreira-Cornwell, H. Baldwin, I. Kostetskii, J. Lenox, and M. Lieberman Rescuing the N-cadherin knockout by cardiac-specific expression of N- or E-cadherin Development 128 2001 459 469
11. K. Horikawa, G. Radice, M. Takeichi, and O. Chisaka Adhesive subdivisions intrinsic to the epithelial somites Dev Biol 215 1999 182 189
12. J. Li, M.D. Levin, Y. Xiong, N. Petrenko, V.V. Patel, and G.L. Radice N-Cadherin haploinsufficiency affects cardiac gap junctions and arrhythmic susceptibility J Mol Cell Cardiol 44 2008 597 606
13. C.F. Lai, S.L. Cheng, G. Mbalaviele, C. Donsante, M. Watkins, and G.L. Radice Accentuated ovariectomy-induced bone loss and altered osteogenesis in heterozygous N-cadherin null mice J Bone Miner Res 21 2006 1897 1906
14. A. Di Benedetto, M. Watkins, S. Grimston, V. Salazar, C. Donsante, and G. Mbalaviele N-Cadherin and cadherin 11 modulate postnatal bone growth and osteoblast differentiation by distinct mechanisms J Cell Sci 123 2010 2640 2648
15. I. Kostetskii, J. Li, Y. Xiong, R. Zhou, V.A. Ferrari, and V.V. Patel Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure Circ Res 96 2005 346 354
16. J. Li, V.V. Patel, I. Kostetskii, Y. Xiong, A.F. Chu, and J.T. Jacobson Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis Circ Res 97 2005 474 481
17. L. Cheng, A. Yung, M. Covarrubias, and G.L. Radice Cortactin is required for N-cadherin regulation of Kv1.5 channel function J Biol Chem 286 2011 20478 20489
18. O.O. Piven, I.E. Kostetskii, L.L. Macewicz, Y.M. Kolomiets, G.L. Radice, and L.L. Lukash Requirement for N-cadherin-catenin complex in heart development Exp Biol Med (Maywood) 236 2011 816 822
19. Y. Luo, and G.L. Radice N-Cadherin acts upstream of VE-cadherin in controlling vascular morphogenesis J Cell Biol 169 2005 29 34
20. Y. Luo, F.A. High, J.A. Epstein, and G.L. Radice N-Cadherin is required for neural crest remodeling of the cardiac outflow tract Dev Biol 299 2006 517 528
21. M. Kadowaki, S. Nakamura, O. Machon, S. Krauss, G.L. Radice, and M. Takeichi N-Cadherin mediates cortical organization in the mouse brain Dev Biol 304 2007 22 33
22. J.K. Johansson, U. Voss, G. Kesavan, I. Kostetskii, N. Wierup, and G.L. Radice N-Cadherin is dispensable for pancreas development but required for beta-cell granule turnover Genesis 48 2010 374 381
23. F. Broders-Bondon, P. Paul-Gilloteaux, C. Carlier, G.L. Radice, and S. Dufour N-Cadherin and beta1-integrins cooperate during the development of the enteric nervous system Dev Biol 364 2012 178 191
24. G.F. Pontoriero, A.N. Smith, L.A. Miller, G.L. Radice, J.A. West-Mays, and R.A. Lang Co-operative roles for E-cadherin and N-cadherin during lens vesicle separation and lens epithelial cell survival Dev Biol 326 2009 403 417
25. A.D. Himes, R.M. Fiddler, and L.T. Raetzman N-Cadherin loss in POMC-expressing cells leads to pituitary disorganization Mol Endocrinol 25 2011 482 491
26. R.O. Hynes Targeted mutations in cell adhesion genes: what have we learned from them? Dev Biol 180 1996 402 412
27. K.K. Linask, K.A. Knudsen, and Y.H. Gui N-Cadherin-catenin interaction: necessary component of cardiac cell compartmentalization during early vertebrate heart development Dev Biol 185 1997 148 164
28. M.I. Garcia-Castro, E. Vielmetter, and M. Bronner-Fraser N-Cadherin, a cell adhesion molecule involved in establishment of embryonic left-right asymmetry Science 288 2000 1047 1051
29. I. Shiraishi, T. Takamatsu, and S. Fujita 3-D observation of N-cadherin expression during cardiac myofibrillogenesis of the chick embryo using a confocal laser scanning microscope Anat Embryol (Berl) 187 1993 115 120
30. L.L. Ong, N. Kim, T. Mima, L. Cohen-Gould, and T. Mikawa Trabecular myocytes of the embryonic heart require N-cadherin for migratory unit identity Dev Biol 193 1998 1 9
31. I. Kostetskii, R. Moore, R. Kemler, and G.L. Radice Differential adhesion leads to segregation and exclusion of N-cadherin-deficient cells in chimeric embryos Dev Biol 234 2001 72 79
32. Y. Luo, and G.L. Radice Cadherin-mediated adhesion is essential for myofibril continuity across the plasma membrane but not for assembly of the contractile apparatus J Cell Sci 116 2003 1471 1479
33. E.J. Goncharova, Z. Kam, and B. Geiger The involvement of adherens junction components in myofibrillogenesis in cultured cardiac myocytes Development 114 1992 173 183
34. A.P. Soler, and K.A. Knudsen N-Cadherin involvement in cardiac myocyte interaction and myofibrillogenesis Dev Biol 162 1994 9 17
35. C.M. Hertig, M. Eppenberger-Eberhardt, S. Koch, and H.M. Eppenberger 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 Pt. 1 1996 1 10
36. P. Navarro, L. Ruco, and E. Dejana Differential localization of VE- and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization J Cell Biol 140 1998 1475 1484
37. P. Carmeliet, M.G. Lampugnani, L. Moons, F. Breviario, V. Compernolle, and F. Bono Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis Cell 98 1999 147 157
38. S. Gory-Faure, M.H. Prandini, H. Pointu, V. Roullot, I. Pignot-Paintrand, and M. Vernet Role of vascular endothelial-cadherin in vascular morphogenesis Development 126 1999 2093 2102
39. C.M. Borrmann, C. Grund, C. Kuhn, I. Hofmann, S. Pieperhoff, and W.W. Franke The area composita of adhering junctions connecting heart muscle cells of vertebrates. II. Colocalizations of desmosomal and fascia adhaerens molecules in the intercalated disk Eur J Cell Biol 85 2006 469 485
40. W.W. Franke, C.M. Borrmann, C. Grund, and S. Pieperhoff The area composita of adhering junctions connecting heart muscle cells of vertebrates. I. Molecular definition in intercalated disks of cardiomyocytes by immunoelectron microscopy of desmosomal proteins Eur J Cell Biol 85 2006 69 82
41. S. Pieperhoff, and W.W. Franke The area composita of adhering junctions connecting heart muscle cells of vertebrates. VI. Different precursor structures in non-mammalian species Eur J Cell Biol 87 2008 413 430
42. J.E. Saffitz, K.Y. Hames, and S. Kanno Remodeling of gap junctions in ischemic and nonischemic forms of heart disease J Membr Biol 218 2007 65 71
43. J.E. Saffitz Arrhythmogenic cardiomyopathy and abnormalities of cell-to-cell coupling Heart Rhythm 6 2009 S62 S65
44. N.J. Severs, A.F. Bruce, E. Dupont, and S. Rothery Remodelling of gap junctions and connexin expression in diseased myocardium Cardiovasc Res 80 2008 9 19
45. M.A. Beardslee, J.G. Laing, E.C. Beyer, and J.E. Saffitz Rapid turnover of connexin43 in the adult rat heart Circ Res 83 1998 629 635
46. R.M. Shaw, A.J. Fay, M.A. Puthenveedu, M. von Zastrow, Y.N. Jan, and L.Y. Jan Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions Cell 128 2007 547 560
47. J.L. Solan, and P.D. Lampe Connexin43 phosphorylation: structural changes and biological effects Biochem J 419 2009 261 272
48. D.E. Gutstein, G.E. Morley, H. Tamaddon, D. Vaidya, M.D. Schneider, and J. Chen Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43 Circ Res 88 2001 333 339
49. T. Toyofuku, M. Yabuki, K. Otsu, T. Kuzuya, M. Hori, and M. Tada Direct association of the gap junction protein connexin-43 with ZO-1 in cardiac myocytes J Biol Chem 273 1998 12725 12731
50. A.W. Hunter, R.J. Barker, C. Zhu, and R.G. Gourdie Zonula occludens-1 alters connexin43 gap junction size and organization by influencing channel accretion Mol Biol Cell 16 2005 5686 5698
51. J.W. Smyth, T.T. Hong, D. Gao, J.M. Vogan, B.C. Jensen, and T.S. Fong Limited forward trafficking of connexin 43 reduces cell-cell coupling in stressed human and mouse myocardium J Clin Invest 120 2010 266 279
52. K.K. Linask, C. Ludwig, M.D. Han, X. Liu, G.L. Radice, and K.A. Knudsen N-Cadherin/catenin-mediated morphoregulation of somite formation Dev Biol 202 1998 85 102
53. Y. Kimura, H. Matsunami, T. Inoue, K. Shimamura, N. Uchida, and T. Ueno Cadherin-11 expressed in association with mesenchymal morphogenesis in the head, somite, and limb bud of early mouse embryos Dev Biol 169 1995 347 358
54. J. Kawaguchi, Y. Azuma, K. Hoshi, I. Kii, S. Takeshita, and T. Ohta Targeted disruption of cadherin-11 leads to a reduction in bone density in calvaria and long bone metaphyses J Bone Miner Res 16 2001 1265 1271
55. D.M. Lee, H.P. Kiener, S.K. Agarwal, E.H. Noss, G.F. Watts, and O. Chisaka Cadherin-11 in synovial lining formation and pathology in arthritis Science 315 2007 1006 1010
56. C.H. Castro, C.S. Shin, J.P. Stains, S.L. Cheng, S. Sheikh, and G. Mbalaviele Targeted expression of a dominant-negative N-cadherin in vivo delays peak bone mass and increases adipogenesis J Cell Sci 117 2004 2853 2864
57. Y. Luo, I. Kostetskii, and G.L. Radice N-Cadherin is not essential for limb mesenchymal chondrogenesis Dev Dyn 232 2005 336 344
58. M.A. Huber, N. Kraut, and H. Beug Molecular requirements for epithelial-mesenchymal transition during tumor progression Curr Opin Cell Biol 17 2005 548 558
59. M.J. Wheelock, Y. Shintani, M. Maeda, Y. Fukumoto, and K.R. Johnson Cadherin switching J Cell Sci 121 2008 727 735
60. M. Maeda, K.R. Johnson, and M.J. Wheelock Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition J Cell Sci 118 2005 873 887
61. A.M. Kotb, A. Hierholzer, and R. Kemler Replacement of E-cadherin by N-cadherin in the mammary gland leads to fibrocystic changes and tumor formation Breast Cancer Res 13 2011 R104
62. V.P. Eswarakumar, I. Lax, and J. Schlessinger Cellular signaling by fibroblast growth factor receptors Cytokine Growth Factor Rev 16 2005 139 149
63. R.B. Hazan, G.R. Phillips, R.F. Qiao, L. Norton, and S.A. Aaronson Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis J Cell Biol 148 2000 779 790
64. J. Hulit, K. Suyama, S. Chung, R. Keren, G. Agiostratidou, and W. Shan N-Cadherin signaling potentiates mammary tumor metastasis via enhanced extracellular signal-regulated kinase activation Cancer Res 67 2007 3106 3116
65. M.T. Nieman, R.S. Prudoff, K.R. Johnson, and M.J. Wheelock N-Cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression J Cell Biol 147 1999 631 644
66. K. Suyama, I. Shapiro, M. Guttman, and R.B. Hazan A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor Cancer Cell 2 2002 301 314
67. S. Chung, J. Yao, K. Suyama, S. Bajaj, X. Qian, and O.D. Loudig N-Cadherin regulates mammary tumor cell migration through Akt3 suppression Oncogene 32 2013 422 430
68. S.R. Hingorani, L. Wang, A.S. Multani, C. Combs, T.B. Deramaudt, and R.H. Hruban Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice Cancer Cell 7 2005 469 483
69. Y. Su, J. Li, A.K. Witkiewicz, D. Brennan, T. Neill, and J. Talarico N-Cadherin haploinsufficiency increases survival in a mouse model of pancreatic cancer Oncogene 31 2012 4484 4489
70. A. Fukuda, S.C. Wang, J.P.T. Morris, A.E. Folias, A. Liou, and G.E. Kim Stat3 and MMP7 contribute to pancreatic ductal adenocarcinoma initiation and progression Cancer Cell 19 2011 441 455
71. T. Ishiwata, H. Friess, M.W. Buchler, M.E. Lopez, and M. Korc Characterization of keratinocyte growth factor and receptor expression in human pancreatic cancer Am J Pathol 153 1998 213 222
72. M. Wagner, M.E. Lopez, M. Cahn, and M. Korc Suppression of fibroblast growth factor receptor signaling inhibits pancreatic cancer growth in vitro and in vivo Gastroenterology 114 1998 798 807
73. S. Nomura, H. Yoshitomi, S. Takano, T. Shida, S. Kobayashi, and M. Ohtsuka FGF10/FGFR2 signal induces cell migration and invasion in pancreatic cancer Br J Cancer 99 2008 305 313
74. Y. Shintani, M.A. Hollingsworth, M.J. Wheelock, and K.R. Johnson Collagen I promotes metastasis in pancreatic cancer by activating c-Jun NH(2)-terminal kinase 1 and up-regulating N-cadherin expression Cancer Res 66 2006 11745 11753
75. J. Qi, N. Chen, J. Wang, and C.H. Siu Transendothelial migration of melanoma cells involves N-cadherin-mediated adhesion and activation of the beta-catenin signaling pathway Mol Biol Cell 16 2005 4386 4397
76. J.M. Drake, G. Strohbehn, T.B. Bair, J.G. Moreland, and M.D. Henry ZEB1 enhances transendothelial migration and represses the epithelial phenotype of prostate cancer cells Mol Biol Cell 20 2009 2207 2217
77. J. Qi, J. Wang, O. Romanyuk, and C.H. Siu Involvement of Src family kinases in N-cadherin phosphorylation and beta-catenin dissociation during transendothelial migration of melanoma cells Mol Biol Cell 17 2006 1261 1272
78. O.W. Blaschuk, R. Sullivan, S. David, and Y. Pouliot Identification of a cadherin cell adhesion recognition sequence Dev Biol 139 1990 227 229
79. E. Williams, G. Williams, B.J. Gour, O.W. Blaschuk, and P. Doherty A novel family of cyclic peptide antagonists suggests that N-cadherin specificity is determined by amino acids that flank the HAV motif J Biol Chem 275 2000 4007 4012
80. Y. Shintani, Y. Fukumoto, N. Chaika, P.M. Grandgenett, M.A. Hollingsworth, and M.J. Wheelock ADH-1 suppresses N-cadherin-dependent pancreatic cancer progression Int J Cancer 122 2008 71 77
81. C.K. Augustine, Y. Yoshimoto, M. Gupta, P.A. Zipfel, M.A. Selim, and P. Febbo Targeting N-cadherin enhances antitumor activity of cytotoxic therapies in melanoma treatment Cancer Res 68 2008 3777 3784
82. H. Tanaka, E. Kono, C.P. Tran, H. Miyazaki, J. Yamashiro, and T. Shimomura Monoclonal antibody targeting of N-cadherin inhibits prostate cancer growth, metastasis and castration resistance Nat Med 16 2010 1414 1420
83. M. Takeichi The cadherins: cell-cell adhesion molecules controlling animal morphogenesis Development 102 1988 639 655
84. L. Larue, M. Ohsugi, J. Hirchenhain, and R. Kemler E-Cadherin null mutant embryos fail to form a trophectoderm epithelium Proc Natl Acad Sci USA 91 1994 8263 8267
85. S. Miyatani, K. Shimamura, M. Hatta, A. Nagafuchi, A. Nose, and M. Matsunaga Neural cadherin: role in selective cell-cell adhesion Science 245 1989 631 635
86. M.C. Ferreira-Cornwell, Y. Luo, N. Narula, J.M. Lenox, M. Lieberman, and G.L. Radice Remodeling the intercalated disc leads to cardiomyopathy in mice misexpressing cadherins in the heart J Cell Sci 115 2002 1623 1634
87. M.A. Craig, M.W. McBride, G. Smith, S.J. George, and A. Baker Dysregulation of cadherins in the intercalated disc of the spontaneously hypertensive stroke-prone rat J Mol Cell Cardiol 48 2010 1121 1128
88. Y.S. Chu, W.A. Thomas, O. Eder, F. Pincet, E. Perez, and J.P. Thiery Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42 J Cell Biol 167 2004 1183 1194
89. Y.S. Chu, O. Eder, W.A. Thomas, I. Simcha, F. Pincet, and A. Ben-Ze'ev Prototypical type I E-cadherin and type II cadherin-7 mediate very distinct adhesiveness through their extracellular domains J Biol Chem 281 2006 2901 2910
90. N.G. Kan, M.P. Stemmler, D. Junghans, B. Kanzler, W.N. de Vries, and M. Dominis Gene replacement reveals a specific role for E-cadherin in the formation of a functional trophectoderm Development 134 2007 31 41
91. L. Libusova, M.P. Stemmler, A. Hierholzer, H. Schwarz, and R. Kemler N-Cadherin can structurally substitute for E-cadherin during intestinal development but leads to polyp formation Development 137 2010 2297 2305
92. D. Pinto, A. Gregorieff, H. Begthel, and H. Clevers Canonical Wnt signals are essential for homeostasis of the intestinal epithelium Genes Dev 17 2003 1709 1713
93. G.F. Weber, M.A. Bjerke, and D.W. DeSimone Integrins and cadherins join forces to form adhesive networks J Cell Sci 124 2011 1183 1193
94. X. Xu, W.E. Li, G.Y. Huang, R. Meyer, T. Chen, and Y. Luo Modulation of mouse neural crest cell motility by N-cadherin and connexin 43 gap junctions J Cell Biol 154 2001 217 230
95. T.B. Deramaudt, M. Takaoka, R. Upadhyay, M.J. Bowser, J. Porter, and A. Lee N-Cadherin and keratinocyte growth factor receptor mediate the functional interplay between Ki-RASG12V and p53V143A in promoting pancreatic cell migration, invasion, and tissue architecture disruption Mol Cell Biol 26 2006 4185 4200
96. J.W. Smyth, J.M. Vogan, P.J. Buch, S.S. Zhang, T.S. Fong, and T.T. Hong Actin cytoskeleton rest stops regulate anterograde traffic of connexin 43 vesicles to the plasma membrane Circ Res 110 2012 978 989