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Journal of Oncology
Volume 2010, Article ID 174715, 9 pages
http://dx.doi.org/10.1155/2010/174715
Review Article

The Misregulation of Cell Adhesion Components during Tumorigenesis: Overview and Commentary

Department of Surgery and Cancer Biology, Vanderbilt University, Nashville, TN 37232, USA

Received 8 July 2010; Revised 23 August 2010; Accepted 10 September 2010

Academic Editor: Ala-Eddin Al Moustafa

Copyright © 2010 Claudia D. Andl. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Hartsock and W. J. Nelson, “Adherens and tight junctions: structure, function and connections to the actin cytoskeleton,” Biochimica et Biophysica Acta, vol. 1778, no. 3, pp. 660–669, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. A. Tamura, Y. Kitano, M. Hata et al., “Megaintestine in claudin-15-deficient mice,” Gastroenterology, vol. 134, no. 2, pp. 523–534, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. M. Furuse, M. Hata, K. Furuse et al., “Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice,” Journal of Cell Biology, vol. 156, no. 6, pp. 1099–1111, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. T. Nitta, M. Hata, S. Gotoh et al., “Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice,” Journal of Cell Biology, vol. 161, no. 3, pp. 653–660, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. M. Lioni, P. Brafford, C. Andl et al., “Dysregulation of claudin-7 leads to loss of E-cadherin expression and the increased invasion of esophageal squamous cell carcinoma cells,” American Journal of Pathology, vol. 170, no. 2, pp. 709–721, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. P. Dhawan, A. B. Singh, N. G. Deane et al., “Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer,” Journal of Clinical Investigation, vol. 115, no. 7, pp. 1765–1776, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. X. Y. Pan, B. Wang, Y. C. Che, Z. P. Weng, H. Y. Dai, and W. Peng, “Expression of claudin-3 and claudin-4 in normal, hyperplastic, and malignant endometrial tissue,” International Journal of Gynecological Cancer, vol. 17, no. 1, pp. 233–241, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. M. Nita-Lazar, I. Rebustini, J. Walker, and M. A. Kukuruzinska, “Hypoglycosylated E-cadherin promotes the assembly of tight junctions through the recruitment of PP2A to adherens junctions,” Experimental Cell Research, vol. 316, no. 11, pp. 1871–1884, 2010. View at Publisher · View at Google Scholar · View at PubMed
  9. A. B. Singh, A. Sharma, and P. Dhawan, “Claudin family of proteins and cancer: an overview,” Jounral of Oncology, vol. 2010, p. 11, 2010. View at Publisher · View at Google Scholar · View at PubMed
  10. E. Delva, D. K. Tucker, and A. P. Kowalczyk, “The desmosome,” Cold Spring Harbor Perspectives in Biology, vol. 1, no. 2, Article ID a002543, 2009. View at Google Scholar
  11. L. M. Godsel, S. Getsios, A. C. Huen, and K. J. Green, “The molecular composition and function of desmosomes,” Handbook of Experimental Pharmacology, pp. 137–193, 2004. View at Google Scholar
  12. R. B. Troyanovsky, N. A. Chitaev, and S. M. Troyanovsky, “Cadherin binding sites of plakoglobin: localization, specificity and role in targeting to adhering junctions,” Journal of Cell Science, vol. 109, no. 13, pp. 3069–3078, 1996. View at Google Scholar
  13. J. K. Wahl, P. A. Sacco, T. M. McGranahan-Sadler, L. M. Sauppé, M. J. Wheelock, and K. R. Johnson, “Plakoglobin domains that define its association with the desmosomal cadherins and the classical cadherins: identification of unique and shared domains,” Journal of Cell Science, vol. 109, no. 5, pp. 1143–1154, 1996. View at Google Scholar
  14. P. Cowin, H.-P. Kapprell, W. W. Franke, J. Tamkun, and R. O. Hynes, “Plakoglobin: a protein common to different kinds of intercellular adhering junctions,” Cell, vol. 46, no. 7, pp. 1063–1073, 1986. View at Google Scholar
  15. D. Salomon, O. Ayalon, R. Patel-King, R. O. Hynes, and B. Geiger, “Extrajunctional distribution of N-cadherin in cultured human endothelial cells,” Journal of Cell Science, vol. 102, no. 1, pp. 7–17, 1992. View at Google Scholar
  16. S. Miravet, J. Piedra, F. Miró, E. Itarte, A. Garcia de Herreros, and M. Duñach, “The transcriptional factor Tcf-4 contains different binding sites for β-catenin and plakoglobin,” Journal of Biological Chemistry, vol. 277, no. 3, pp. 1884–1891, 2002. View at Publisher · View at Google Scholar · View at PubMed
  17. O. Maeda, N. Usami, M. Kondo et al., “Plakoglobin (γ-catenin) has TCF/LEF family-dependent transcriptional activity in β-catenin-deficient cell line,” Oncogene, vol. 23, no. 4, pp. 964–972, 2004. View at Publisher · View at Google Scholar · View at PubMed
  18. J. Depondt, E.-H. Shabana, F. Walker, L. Pibouin, F. Lezot, and A. Berdal, “Nasal inverted papilloma expresses the muscle segment homeobox gene Msx2: possible prognostic implications,” Human Pathology, vol. 39, no. 3, pp. 350–358, 2008. View at Publisher · View at Google Scholar · View at PubMed
  19. H. Pang, B. G. Rowan, M. Al-Dhaheri, and L. E. Faber, “Epidermal growth factor suppresses induction by progestin of the adhesion protein desmoplakin in T47D breast cancer cells,” Breast Cancer Research, vol. 6, no. 3, pp. R239–R245, 2004. View at Google Scholar
  20. X. Zhou, A. Stuart, L. E. Dettin, G. Rodriguez, B. Hoel, and G. I. Gallicano, “Desmoplakin is required for microvascular tube formation in culture,” Journal of Cell Science, vol. 117, no. 15, pp. 3129–3140, 2004. View at Publisher · View at Google Scholar · View at PubMed
  21. J. R. Stanley, “Autoantibodies against adhesion molecules and structures in blistering skin diseases,” Journal of Experimental Medicine, vol. 181, no. 1, pp. 1–4, 1995. View at Publisher · View at Google Scholar
  22. J. Waschke, V. Spindler, P. Bruggeman, D. Zillikens, G. Schmidt, and D. Drenckhahn, “Inhibition of Rho A activity causes pemphigus skin blistering,” Journal of Cell Biology, vol. 175, no. 5, pp. 721–727, 2006. View at Publisher · View at Google Scholar · View at PubMed
  23. L. Eshkind, Q. Tian, A. Schmidt, W. W. Franke, R. Windoffer, and R. E. Leube, “Loss of desmoglein 2 suggests essential functions for early embryonic development and proliferation of embryonal stem cells,” European Journal of Cell Biology, vol. 81, no. 11, pp. 592–598, 2002. View at Google Scholar
  24. P. J. Koch, M. G. Mahoney, H. Ishikawa et al., “Targeted disruption of the pemphigus vulgaris antigen (desmoglein 3) gene in mice causes loss of keratinocyte cell adhesion with a phenotype similar to pemphigus vulgaris,” Journal of Cell Biology, vol. 137, no. 5, pp. 1091–1102, 1997. View at Publisher · View at Google Scholar
  25. L. Pulkkinen, Y. W. Choi, A. Simpson et al., “Loss of cell adhesion in Dsg3bal-Pas mice with homozygous deletion mutation (2079del14) in the desmoglein 3 gene,” Journal of Investigative Dermatology, vol. 119, no. 6, pp. 1237–1243, 2002. View at Publisher · View at Google Scholar · View at PubMed
  26. C. Bierkamp, K. J. McLaughlin, H. Schwarz, O. Huber, and R. Kemler, “Embryonic heart and skin defects in mice lacking plakoglobin,” Developmental Biology, vol. 180, no. 2, pp. 780–785, 1996. View at Publisher · View at Google Scholar · View at PubMed
  27. V. Vasioukhin, E. Bowers, C. Bauer, L. Degenstein, and E. Fuchs, “Desmoplakin is essential in epidermal sheet formation,” Nature Cell Biology, vol. 3, no. 12, pp. 1076–1085, 2001. View at Publisher · View at Google Scholar · View at PubMed
  28. M. P. Wong, M. Cheang, E. Yorida et al., “Loss of desmoglein 1 expression associated with worse prognosis in head and neck squamous cell carcinoma patients,” Pathology, vol. 40, no. 6, pp. 611–616, 2008. View at Publisher · View at Google Scholar · View at PubMed
  29. D. Brennan and M. G. Mahoney, “Increased expression of Dsg2 in malignant skin carcinomas: a tissue-microarray based study,” Cell Adhesion and Migration, vol. 3, no. 2, pp. 148–154, 2009. View at Google Scholar
  30. A. E. Bass-Zubek, L. M. Godsel, M. Delmar, and K. J. Green, “Plakophilins: multifunctional scaffolds for adhesion and signaling,” Current Opinion in Cell Biology, vol. 21, no. 5, pp. 708–716, 2009. View at Publisher · View at Google Scholar · View at PubMed
  31. A. P. South, H. Wan, M. G. Stone et al., “Lack of plakophilin 1 increases keratinocyte migration and reduces desmosome stability,” Journal of Cell Science, vol. 116, no. 16, pp. 3303–3314, 2003. View at Publisher · View at Google Scholar · View at PubMed
  32. T. Sobolik-Delmaire, D. Katafiasz, S. A. Keim, M. G. Mahoney, and J. K. Wahl III, “Decreased plakophilin-1 expression promotes increased motility in head and neck squamous cell carcinoma cells,” Cell Communication and Adhesion, vol. 14, no. 2-3, pp. 99–109, 2007. View at Publisher · View at Google Scholar · View at PubMed
  33. S. T. Kundu, P. Gosavi, N. Khapare et al., “Plakophilin3 downregulation leads to a decrease in cell adhesion and promotes metastasis,” International Journal of Cancer, vol. 123, no. 10, pp. 2303–2314, 2008. View at Publisher · View at Google Scholar · View at PubMed
  34. S. Pieperhoff, M. Barth, S. Rickelt, and W. W. Franke, “Desmosomal molecules in and out of adhering junctions: normal and diseased States of epidermal, cardiac and mesenchymally derived cells,” Dermatology Research and Practice, vol. 2010, Article ID 139167, 12 pages, 2010. View at Publisher · View at Google Scholar · View at PubMed
  35. S. Pieperhoff, C. Borrmann, C. Grund, M. Barth, S. Rizzo, and W. W. Franke, “The area composita of adhering junctions connecting heart muscle cells of vertebrates. VII. The different types of lateral junctions between the special cardiomyocytes of the conduction system of ovine and bovine hearts,” European Journal of Cell Biology, vol. 89, no. 5, pp. 365–378, 2010. View at Publisher · View at Google Scholar · View at PubMed
  36. L. Larue, M. Ohsugi, J. Hirchenhain, and R. Kemler, “E-cadherin null mutant embryos fail to form a trophectoderm epithelium,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 17, pp. 8263–8267, 1994. View at Publisher · View at Google Scholar
  37. H. Haegel, L. Larue, M. Ohsugi, L. Fedorov, K. Herrenknecht, and R. Kemler, “Lack of β-catenin affects mouse development at gastrulation,” Development, vol. 121, no. 11, pp. 3529–3537, 1995. View at Google Scholar
  38. G. L. Radice, H. Rayburn, H. Matsunami, K. A. Knudsen, M. Takeichi, and R. O. Hynes, “Developmental defects in mouse embryos lacking N-cadherin,” Developmental Biology, vol. 181, no. 1, pp. 64–78, 1997. View at Publisher · View at Google Scholar · View at PubMed
  39. D. Vittet, T. Buchou, A. Schweitzer, E. Dejana, and P. Huber, “Targeted null-mutation in the vascular endothelial-cadherin gene impairs the organization of vascular-like structures in embryoid bodies,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 12, pp. 6273–6278, 1997. View at Publisher · View at Google Scholar
  40. P. Young, O. Boussadia, H. Halfter et al., “E-cadherin controls adherens junctions in the epidermis and the renewal of hair follicles,” EMBO Journal, vol. 22, no. 21, pp. 5723–5733, 2003. View at Publisher · View at Google Scholar · View at PubMed
  41. G. Calì, M. Zannini, P. Rubini et al., “Conditional inactivation of the E-cadherin gene in thyroid follicular cells affects gland development but does not impair junction formation,” Endocrinology, vol. 148, no. 6, pp. 2737–2746, 2007. View at Publisher · View at Google Scholar · View at PubMed
  42. C. L. Tinkle, T. Lechler, H. A. Pasolli, and E. Fuchs, “Conditional targeting of E-cadherin in skin: insights into hyperproliferative and degenerative responses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 2, pp. 552–557, 2004. View at Publisher · View at Google Scholar · View at PubMed
  43. T. T. Onder, P. B. Gupta, S. A. Mani, J. Yang, E. S. Lander, and R. A. Weinberg, “Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways,” Cancer Research, vol. 68, no. 10, pp. 3645–3654, 2008. View at Publisher · View at Google Scholar · View at PubMed
  44. Y. Kam and V. Quaranta, “Cadherin-bound β-catenin feeds into the Wnt pathway upon adherens junctions dissociation: evidence for an intersection between β-catenin pools,” PLoS ONE, vol. 4, no. 2, article e4580, 2009. View at Publisher · View at Google Scholar · View at PubMed
  45. A. S. T. Wong and B. M. Gumbiner, “Adhesion-independent mechanism for suppression of tumor cell invasion by E-cadherin,” Journal of Cell Biology, vol. 161, no. 6, pp. 1191–1203, 2003. View at Publisher · View at Google Scholar · View at PubMed
  46. K. Strumane, G. Berx, and F. van Roy, “Cadherins in cancer,” Handbook of Experimental Pharmacology, pp. 69–103, 2004. View at Google Scholar
  47. M. Mareel, K. Vleminckx, S. Vermeulen, G. Yan, M. Bracke, and F. van Roy, “Downregulation in vivo of the invasion-suppressor molecule E-cadherin in experimental and clinical cancer,” Princess Takamatsu Symposia, vol. 24, pp. 63–80, 1994. View at Google Scholar
  48. Y. Kanai, T. Oda, Y. Shimoyama et al., “Alterations of the cadherin-catenin cell adhesion system in cancers,” Princess Takamatsu Symposia, vol. 24, pp. 51–62, 1994. View at Google Scholar
  49. S. Tsukita, S. Tsukita, A. Nagafuchi, and S. Yonemura, “Possible involvement of adherens junction plaque proteins in tumorigenesis and metastasis,” Princess Takamatsu Symposia, vol. 24, pp. 38–50, 1994. View at Google Scholar
  50. J. Stappert and R. Kemler, “A short core region of E-cadherin is essential for catenin binding and is highly phosphorylated,” Cell Adhesion and Communication, vol. 2, no. 4, pp. 319–327, 1994. View at Google Scholar
  51. M. A. Thoreson, P. Z. Anastasiadis, J. M. Daniel et al., “Selective uncoupling of p120(ctn) from E-cadherin disrupts strong adhesion,” Journal of Cell Biology, vol. 148, no. 1, pp. 189–201, 2000. View at Publisher · View at Google Scholar
  52. N. Rudini and E. Dejana, “Adherens junctions,” Current Biology, vol. 18, no. 23, pp. R1080–R1082, 2008. View at Publisher · View at Google Scholar · View at PubMed
  53. C. J. Gottardi and B. M. Gumbiner, “Distinct molecular forms of β-catenin are targeted to adhesive or transcriptional complexes,” Journal of Cell Biology, vol. 167, no. 2, pp. 339–349, 2004. View at Publisher · View at Google Scholar · View at PubMed
  54. H. Clevers, “Wnt/β-catenin signaling in development and disease,” Cell, vol. 127, no. 3, pp. 469–480, 2006. View at Publisher · View at Google Scholar · View at PubMed
  55. J. Behrens, “Control of β-catenin signaling in tumor development,” Annals of the New York Academy of Sciences, vol. 910, pp. 21–35, 2000. View at Google Scholar
  56. V. J. M. Wielenga, R. Smits, V. Korinek et al., “Expression of CD44 in Apc and Tcf mutant mice implies regulation by the WNT pathway,” American Journal of Pathology, vol. 154, no. 2, pp. 515–523, 1999. View at Google Scholar
  57. R. Fodde and T. Brabletz, “Wnt/β-catenin signaling in cancer stemness and malignant behavior,” Current Opinion in Cell Biology, vol. 19, no. 2, pp. 150–158, 2007. View at Publisher · View at Google Scholar · View at PubMed
  58. J. Schneikert and J. Behrens, “The canonical Wnt signalling pathway and its APC partner in colon cancer development,” Gut, vol. 56, no. 3, pp. 417–425, 2007. View at Publisher · View at Google Scholar · View at PubMed
  59. J. M. Daniel and A. B. Reynolds, “The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor,” Molecular and Cellular Biology, vol. 19, no. 5, pp. 3614–3623, 1999. View at Google Scholar
  60. J.-I. Park, H. Ji, S. Jun et al., “Frodo links dishevelled to the p120-catenin/Kaiso pathway: distinct catenin subfamilies promote Wnt signals,” Developmental Cell, vol. 11, no. 5, pp. 683–695, 2006. View at Publisher · View at Google Scholar · View at PubMed
  61. J.-I. Park, S. W. Kim, J. P. Lyons et al., “Kaiso/p120-catenin and TCF/β-catenin complexes coordinately regulate canonical Wnt gene targets,” Developmental Cell, vol. 8, no. 6, pp. 843–854, 2005. View at Publisher · View at Google Scholar · View at PubMed
  62. S. W. Kim, J.-I. Park, C. M. Spring et al., “Non-canonical Wnt signals are modulated by the Kaiso transcriptional repressor and p120-catenin,” Nature Cell Biology, vol. 6, no. 12, pp. 1212–1220, 2004. View at Publisher · View at Google Scholar · View at PubMed
  63. P. Z. Anastasiadis, “p120-ctn: a nexus for contextual signaling via Rho GTPases,” Biochimica et Biophysica Acta, vol. 1773, no. 1, pp. 34–46, 2007. View at Publisher · View at Google Scholar · View at PubMed
  64. G. A. Wildenberg, M. R. Dohn, R. H. Carnahan et al., “p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho,” Cell, vol. 127, no. 5, pp. 1027–1039, 2006. View at Publisher · View at Google Scholar · View at PubMed
  65. M. Yanagisawa, D. Huveldt, P. Kreinest et al., “A p120 catenin isoform switch affects rho activity, induces tumor cell invasion, and predicts metastatic disease,” Journal of Biological Chemistry, vol. 283, no. 26, pp. 18344–18354, 2008. View at Publisher · View at Google Scholar · View at PubMed
  66. L. W. T. Cheung, P. C. K. Leung, and A. S. T. Wong, “Cadherin switching and activation of p120 catenin signaling are mediators of gonadotropin-releasing hormone to promote tumor cell migration and invasion in ovarian cancer,” Oncogene, vol. 29, no. 16, pp. 2427–2440, 2010. View at Publisher · View at Google Scholar · View at PubMed
  67. N. T. Chartier, C. I. Oddou, M. G. Lainé et al., “Cyclin-dependent kinase 2/cyclin E complex is involved in p120 catenin (p120ctn)-dependent cell growth control: a new role for p120ctn in cancer,” Cancer Research, vol. 67, no. 20, pp. 9781–9790, 2007. View at Publisher · View at Google Scholar · View at PubMed
  68. M. Perez-Moreno, W. Song, H. A. Pasolli, S. E. Williams, and E. Fuchs, “Loss of p120 catenin and links to mitotic alterations, inflammation, and skin cancer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 40, pp. 15399–15404, 2008. View at Publisher · View at Google Scholar · View at PubMed
  69. W. G. Smalley-Freed, A. Efimov, P. E. Burnett et al., “p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice,” Journal of Clinical Investigation, vol. 120, no. 6, pp. 1824–1835, 2010. View at Publisher · View at Google Scholar · View at PubMed
  70. D. M. Bryant, F. G. Wylie, and J. L. Stow, “Regulation of endocytosis, nuclear translocation, and signaling of fibroblast growth factor receptor 1 by E-cadherin,” Molecular Biology of the Cell, vol. 16, no. 1, pp. 14–23, 2005. View at Publisher · View at Google Scholar · View at PubMed
  71. R. B. Hazan, R. Qiao, R. Keren, I. Badano, and K. Suyama, “Cadherin switch in tumor progression,” Annals of the New York Academy of Sciences, vol. 1014, pp. 155–163, 2004. View at Publisher · View at Google Scholar
  72. M. J. Wheelock, Y. Shintani, M. Maeda, Y. Fukumoto, and K. R. Johnson, “Cadherin switching,” Journal of Cell Science, vol. 121, no. 6, pp. 727–735, 2008. View at Publisher · View at Google Scholar · View at PubMed
  73. S. Pece and J. S. Gutkind, “Signaling from E-cadharins to the MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation,” Journal of Biological Chemistry, vol. 275, no. 52, pp. 41227–41233, 2000. View at Publisher · View at Google Scholar · View at PubMed
  74. H. Hoschuetzky, H. Aberle, and R. Kemler, “β-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor,” Journal of Cell Biology, vol. 127, no. 5, pp. 1375–1380, 1994. View at Publisher · View at Google Scholar
  75. A. Bremm, A. Walch, M. Fuchs et al., “Enhanced activation of epidermal growth factor receptor caused by tumor-derived E-cadherin mutations,” Cancer Research, vol. 68, no. 3, pp. 707–714, 2008. View at Publisher · View at Google Scholar · View at PubMed
  76. G. Berx, A.-M. Cleton-Jansen, F. Nollet et al., “E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers,” EMBO Journal, vol. 14, no. 24, pp. 6107–6115, 1995. View at Google Scholar
  77. M. Perrais, X. Chen, M. Perez-Moreno, and B. M. Gumbiner, “E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions,” Molecular Biology of the Cell, vol. 18, no. 6, pp. 2013–2025, 2007. View at Publisher · View at Google Scholar · View at PubMed
  78. X. Qian, T. Karpova, A. M. Sheppard, J. McNally, and D. R. Lowy, “E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases,” EMBO Journal, vol. 23, no. 8, pp. 1739–1748, 2004. View at Publisher · View at Google Scholar · View at PubMed
  79. S. Getsios, C. L. Simpson, S.-I. Kojima et al., “Desmoglein 1-dependent suppression of EGFR signaling promotes epidermal differentiation and morphogenesis,” Journal of Cell Biology, vol. 185, no. 7, pp. 1243–1258, 2009. View at Publisher · View at Google Scholar · View at PubMed
  80. E. Dejana, “Endothelial cell-cell junctions: happy together,” Nature Reviews Molecular Cell Biology, vol. 5, no. 4, pp. 261–270, 2004. View at Publisher · View at Google Scholar · View at PubMed
  81. M. G. Lampugnani, F. Orsenigo, M. C. Gagliani, C. Tacchetti, and E. Dejana, “Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments,” Journal of Cell Biology, vol. 174, no. 4, pp. 593–604, 2006. View at Publisher · View at Google Scholar · View at PubMed
  82. N. Rudini, A. Felici, C. Giampietro et al., “VE-cadherin is a critical endothelial regulator of TGF-β signalling,” EMBO Journal, vol. 27, no. 7, pp. 993–1004, 2008. View at Publisher · View at Google Scholar · View at PubMed
  83. S. Liebner, A. Cattelino, R. Gallini et al., “β-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse,” Journal of Cell Biology, vol. 166, no. 3, pp. 359–367, 2004. View at Publisher · View at Google Scholar · View at PubMed
  84. L.-W. Qian, W. Greene, F. Ye, and S.-J. Gao, “Kaposi's sarcoma-associated herpesvirus disrupts adherens junctions and increases endothelial permeability by inducing degradation of VE-cadherin,” Journal of Virology, vol. 82, no. 23, pp. 11902–11912, 2008. View at Publisher · View at Google Scholar · View at PubMed
  85. E. Lara-Pezzi, S. Roche, O. M. Andrisani, F. Sánchez-Madrid, and M. López-Cabrera, “The hepatitis B virus HBx protein induces adherens junction disruption in a src-dependent manner,” Oncogene, vol. 20, no. 26, pp. 3323–3331, 2001. View at Publisher · View at Google Scholar · View at PubMed
  86. S. Niemhom, S. Kitazawa, R. Kitazawa, S. Maeda, and J. Leopairat, “Hypermethylation of epithelial-cadherin gene promoter is associated with Epstein-Barr virus in nasopharyngeal carcinoma,” Cancer Detection and Prevention, vol. 32, no. 2, pp. 127–134, 2008. View at Publisher · View at Google Scholar · View at PubMed
  87. J. Laurson, S. Khan, R. Chung, K. Cross, and K. Raj, “Epigenetic repression of E-cadherin by human papillomavirus 16 E7 protein,” Carcinogenesis, vol. 31, no. 5, pp. 918–926, 2010. View at Publisher · View at Google Scholar · View at PubMed
  88. K. Hellner, J. Mar, F. Fang, J. Quackenbush, and K. Münger, “HPV16 E7 oncogene expression in normal human epithelial cells causes molecular changes indicative of an epithelial to mesenchymal transition,” Virology, vol. 391, no. 1, pp. 57–63, 2009. View at Publisher · View at Google Scholar · View at PubMed
  89. J. Wilding, K. H. Vousden, W. P. Soutter, P. D. McCrea, R. Del Buono, and M. Pignatelli, “E-cadherin transfection down-regulates the epidermal growth factor receptor and reverses the invasive phenotype of human papilloma virus- transfected keratinocytes,” Cancer Research, vol. 56, no. 22, pp. 5285–5292, 1996. View at Google Scholar
  90. A.-E. Al Moustafa, A. Kassab, A. Darnel, and A. Yasmeen, “High-risk HPV/ErbB-2 interaction on E-cadherin/catenin regulation in human carcinogenesis,” Current Pharmaceutical Design, vol. 14, no. 22, pp. 2159–2172, 2008. View at Publisher · View at Google Scholar
  91. A. Yasmeen, A. Alachkar, H. Dekhil, C. Gambacorti-Passerini, and A. E. Al Moustafa, “Locking Src/Abl tyrosine kinase activities regulate cell differentiation and invasion of human cervical cancer cells expressing E6/E7 oncoproteins of high-risk HPV,” Jounral of Oncology, vol. 2010, p. 10, 2010. View at Publisher · View at Google Scholar · View at PubMed
  92. K. H. Y. Shair, C. I. Schnegg, and N. Raab-Traub, “Epstein-Barr virus latent membrane protein-1 effects on junctional plakoglobin and induction of a cadherin switch,” Cancer Research, vol. 69, no. 14, pp. 5734–5742, 2009. View at Publisher · View at Google Scholar · View at PubMed
  93. O. Schmalhofer, S. Brabletz, and T. Brabletz, “E-cadherin, β-catenin, and ZEB1 in malignant progression of cancer,” Cancer and Metastasis Reviews, vol. 28, no. 1-2, pp. 151–166, 2009. View at Publisher · View at Google Scholar · View at PubMed
  94. U. Tepass, K. Truong, D. Godt, M. Ikura, and M. Peifer, “Cadherins in embryonic and neural morphogenesis,” Nature Reviews Molecular Cell Biology, vol. 1, no. 2, pp. 91–100, 2000. View at Google Scholar
  95. L. Larue and A. Bellacosa, “Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3 kinase/AKT pathways,” Oncogene, vol. 24, no. 50, pp. 7443–7454, 2005. View at Publisher · View at Google Scholar · View at PubMed
  96. J. P. Their, “Epithelial-mesenchymal transitions in tumor progression,” Nature Reviews Cancer, vol. 2, no. 6, pp. 442–454, 2002. View at Google Scholar
  97. P. J. Miettinen, R. Ebner, A. R. Lopez, and R. Derynck, “TGF-β induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors,” Journal of Cell Biology, vol. 127, no. 6, pp. 2021–2036, 1994. View at Publisher · View at Google Scholar
  98. M. Oft, K.-H. Heider, and H. Beug, “TGFβ signaling is necessary for carcinoma cell invasiveness and metastasis,” Current Biology, vol. 8, no. 23, pp. 1243–1252, 1998. View at Google Scholar
  99. M. Oft, J. Peli, C. Rudaz, H. Schwarz, H. Beug, and E. Reichmann, “TGF-β1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells,” Genes and Development, vol. 10, no. 19, pp. 2462–2477, 1996. View at Google Scholar
  100. G. Portella, S. A. Cumming, J. Liddell et al., “Transforming growth factor β is essential for spindle cell conversion of mouse skin carcinoma in vivo: implications for tumor invasion,” Cell Growth and Differentiation, vol. 9, no. 5, pp. 393–404, 1998. View at Google Scholar
  101. N. A. Bhowmick, M. Ghiassi, A. Bakin et al., “Transforming growth factor-β1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism,” Molecular Biology of the Cell, vol. 12, no. 1, pp. 27–36, 2001. View at Google Scholar
  102. E. Piek, A. Moustakas, A. Kurisaki, C.-H. Heldin, and P. ten Dijke, “TGF-β type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells,” Journal of Cell Science, vol. 112, no. 24, pp. 4557–4568, 1999. View at Google Scholar
  103. B. Deng, X. Yang, J. Liu, F. He, Z. Zhu, and C. Zhang, “Focal adhesion kinase mediates TGF-β1-induced renal tubular epithelial-to-mesenchymal transition in vitro,” Molecular and Cellular Biochemistry, vol. 340, no. 1-2, pp. 21–29, 2010. View at Publisher · View at Google Scholar · View at PubMed
  104. J. Zhong, A. Paul, S. J. Kellie, and G. M. O'Neill, “Mesenchymal migration as a therapeutic target in glioblastoma,” Jounral of Oncology, vol. 2010, p. 17, 2010. View at Publisher · View at Google Scholar · View at PubMed
  105. J. Chunthapong, E. A. Seftor, Z. Khalkhali-Ellis et al., “Dual roles of E-cadherin in prostate cancer invasion,” Journal of Cellular Biochemistry, vol. 91, no. 4, pp. 649–661, 2004. View at Publisher · View at Google Scholar · View at PubMed
  106. C. C. Lynch, T. Vargo-Gogola, L. M. Matrisian, and B. Fingleton, “Cleavage of e-cadherin by matrix metalloproteinase-7 promotes cellular proliferation in nontransformed cell lines via activation of RhoA,” Jounral of Oncology, vol. 2010, p. 11, 2010. View at Publisher · View at Google Scholar · View at PubMed
  107. S. H. Ngalim, A. Magenau, G. Le Saux, J. J. Gooding, and K. Gaus, “How do cells make decisions: engineering micro- and nanoenvironments for cell migration,” Jounral of Oncology, vol. 2010, p. 7, 2010. View at Publisher · View at Google Scholar · View at PubMed
  108. S. Josson, S. Sharp, S. Y. Sung et al., “Tumor-stromal interactions influence radiation sensitivity in epithelial- versus mesenchymal-like prostate cancer cells,” Jounral of Oncology, vol. 2010, p. 10, 2010. View at Publisher · View at Google Scholar · View at PubMed
  109. H. Yamashita, M. Tripathi, J. Jourquin et al., “Lysophosphatidic acid upregulates laminin-332 expression during A431 cell colony dispersal,” Jounral of Oncology, vol. 2010, p. 8, 2010. View at Publisher · View at Google Scholar · View at PubMed
  110. L. Ma, J. Young, H. Prabhala et al., “MiR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis,” Nature Cell Biology, vol. 12, no. 3, pp. 247–256, 2010. View at Publisher · View at Google Scholar · View at PubMed
  111. M. Sachdeva and Y.-Y. Mo, “MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1,” Cancer Research, vol. 70, no. 1, pp. 378–387, 2010. View at Publisher · View at Google Scholar · View at PubMed
  112. V. Gabarra-Niecko, M. D. Schaller, and J. M. Dunty, “FAK regulates biological processes important for the pathogenesis of cancer,” Cancer and Metastasis Reviews, vol. 22, no. 4, pp. 359–374, 2003. View at Publisher · View at Google Scholar
  113. T. P. Hecker and C. L. Gladson, “Focal adhesion kinase in cancer,” Frontiers in Bioscience, vol. 8, pp. s705–s714, 2003. View at Google Scholar
  114. M. Canel, P. Secades, J.-P. Rodrigo et al., “Overexpression of focal adhesion kinase in head and neck squamous cell carcinoma is independent of fak gene copy number,” Clinical Cancer Research, vol. 12, no. 11 I, pp. 3272–3279, 2006. View at Publisher · View at Google Scholar · View at PubMed
  115. S. K. Hanks, L. Ryzhova, N.-Y. Shin, and J. Brábek, “Focal adhesion kinase signaling activities and their implications in the control of cell survival and motility,” Frontiers in Bioscience, vol. 8, pp. d982–d996, 2003. View at Google Scholar
  116. J. T. Parsons, “Focal adhesion kinase: the first ten years,” Journal of Cell Science, vol. 116, no. 8, pp. 1409–1416, 2003. View at Publisher · View at Google Scholar
  117. D. Ilic, Y. Furuta, S. Kanazawa et al., “Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice,” Nature, vol. 377, no. 6549, pp. 539–544, 1995. View at Google Scholar
  118. J. D. Owen, P. J. Ruest, D. W. Fry, and S. K. Hanks, “Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2,” Molecular and Cellular Biology, vol. 19, no. 7, pp. 4806–4818, 1999. View at Google Scholar
  119. M. Raftopoulou and A. Hall, “Cell migration: Rho GTPases lead the way,” Developmental Biology, vol. 265, no. 1, pp. 23–32, 2004. View at Publisher · View at Google Scholar
  120. A. Hamadi, T. B. Deramaudt, K. Takeda, and P. Rondé, “Hyperphosphorylated FAK delocalizes from focal adhesions to membrane ruffles,” Jounral of Oncology, vol. 2010, p. 10, 2010. View at Publisher · View at Google Scholar · View at PubMed
  121. H. Yano, Y. Mazaki, K. Kurokawa, S. K. Hanks, M. Matsuda, and H. Sabe, “Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion,” Journal of Cell Biology, vol. 166, no. 2, pp. 283–295, 2004. View at Publisher · View at Google Scholar · View at PubMed
  122. A. S. Yap and E. M. Kovacs, “Direct cadherin-activated cell signaling: a view from the plasma membrane,” Journal of Cell Biology, vol. 160, no. 1, pp. 11–16, 2003. View at Publisher · View at Google Scholar · View at PubMed
  123. S. Charrasse, M. Meriane, F. Comunale, A. Blangy, and C. Gauthier-Rouvière, “N-cadherin-dependent cell-cell contact regulates Rho GTPases and β-catenin localization in mouse C2C12 myoblasts,” Journal of Cell Biology, vol. 158, no. 5, pp. 953–965, 2002. View at Publisher · View at Google Scholar · View at PubMed
  124. V. M. Golubovskaya and W. Cance, “Focal adhesion kinase and p53 signal transduction pathways in cancer,” Frontiers in Bioscience, vol. 15, pp. 901–912, 2010. View at Google Scholar
  125. T. Sakisaka and Y. Takai, “Biology and pathology of nectins and nectin-like molecules,” Current Opinion in Cell Biology, vol. 16, no. 5, pp. 513–521, 2004. View at Publisher · View at Google Scholar · View at PubMed
  126. A. Yamada, K. Irie, A. Fukuhara, T. Ooshio, and Y. Takai, “Requirement of the actin cytoskeleton for the association of nectins with other cell adhesion molecules at adherens and tight junctions in MDCK cells,” Genes to Cells, vol. 9, no. 9, pp. 843–855, 2004. View at Publisher · View at Google Scholar · View at PubMed
  127. H. Ogita, Y. Rikitake, J. Miyoshi, and Y. Takai, “Cell adhesion molecules nectins and associating proteins: implications for physiology and pathology,” Proceedings of the Japan Academy B, vol. 86, no. 6, pp. 621–629, 2010. View at Publisher · View at Google Scholar
  128. H. Ogita and Y. Takai, “Cross-talk among integrin, cadherin, and growth factor receptor: roles of nectin and nectin-like molecule,” International Review of Cytology, vol. 265, pp. 1–54, 2008. View at Publisher · View at Google Scholar · View at PubMed
  129. T. Ooshio, R. Kobayashi, W. Ikeda et al., “Involvement of the interaction of afadin with ZO-1 in the formation of tight junctions in Madin-Darby canine kidney cells,” Journal of Biological Chemistry, vol. 285, no. 7, pp. 5003–5012, 2010. View at Publisher · View at Google Scholar · View at PubMed
  130. T. Hoshino, T. Sakisaka, T. Baba, T. Yamada, T. Kimura, and Y. Takai, “Regulation of E-cadherin endocytosis by nectin through afadin, Rap1, and p120ctn,” Journal of Biological Chemistry, vol. 280, no. 25, pp. 24095–24103, 2005. View at Publisher · View at Google Scholar · View at PubMed
  131. T. Hoshino, K. Shimizu, T. Honda et al., “A novel role of nectins in inhibition of the E-cadherin-induced activation of Rac and formation of cell-cell adherens junctions,” Molecular Biology of the Cell, vol. 15, no. 3, pp. 1077–1088, 2004. View at Publisher · View at Google Scholar · View at PubMed
  132. T. Sato, N. Fujita, A. Yamada et al., “Regulation of the assembly and adhesion activity of E-cadherin by nectin and afadin for the formation of adherens junctions in Madin-Darby canine kidney cells,” Journal of Biological Chemistry, vol. 281, no. 8, pp. 5288–5299, 2006. View at Publisher · View at Google Scholar · View at PubMed
  133. H. Nakanishi and Y. Takai, “Roles of nectins in cell adhesion, migration and polarization,” Biological Chemistry, vol. 385, no. 10, pp. 885–892, 2004. View at Publisher · View at Google Scholar · View at PubMed
  134. M. Matsuda, J. K. Yamashita, S. Tsukita, and M. Furuse, “abLIM3 is a novel component of adherens junctions with actin-binding activity,” European Journal of Cell Biology, vol. 89, no. 11, pp. 807–816, 2010. View at Publisher · View at Google Scholar · View at PubMed
  135. D. Schreiner and J. A. Weiner, “Combinatorial homophilic interaction between γ-protocadherin multimers greatly expands the molecular diversity of cell adhesion,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, pp. 14893–14898, 2010. View at Google Scholar
  136. M. Frank and R. Kemler, “Protocadherins,” Current Opinion in Cell Biology, vol. 14, no. 5, pp. 557–562, 2002. View at Publisher · View at Google Scholar
  137. A. P. LaFlamme SEK, Ed., Cell Junctions. Adhesion, Development and Disease, Wiley-VCH, GmbH, Weinheim, Germany, 2008.
  138. U. Cavallaro and G. Christofori, “Cell adhesion and signalling by cadherins and Ig-CAMs in cancer,” Nature Reviews Cancer, vol. 4, no. 2, pp. 118–132, 2004. View at Google Scholar