Skip to main content
Log in

Changes in regulation of cell—cell adhesion during tumor transformation

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Cadherin-mediated cell—cell adhesion defines the integrity of most tissues. Cell—cell adherens junctions are dynamic structures whose functional state is regulated by interactions of cadherin with β-catenin, p120, and actin cytoskeleton structures. Small GTPases of the Rho family and GTPase Rap1 play the central role in the formation and maintenance of cell—cell adhesion. Aberrant activation of signaling pathways, transcriptional repression of the E-cadherin gene, ectopic expression of N-cadherin, and disturbances in regulation of adhesive and transcriptional functions of β-catenin stimulate tumor progression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AJ:

cell—cell adherens junctions

EGF:

epidermal growth factor

EMT:

epithelial-mesenchymal transformation

FGF:

fibroblast growth factor

GEFs:

guanine nucleotide exchange factors

HGF/SF:

hepatocyte growth factor/scatter factor

PDGF:

platelet-derived growth factor

References

  1. Willert, K., and Jones, K. A. (2007) Genes Dev., 20, 1394–1404.

    Article  CAS  Google Scholar 

  2. Perez-Moreno, M., and Fuchs, E. (2006) Dev. Cell, 11, 601–612.

    Article  PubMed  CAS  Google Scholar 

  3. Katoh, M., and Katoh, M. (2006) Cancer Biol. Ther., 5, 1059–1064.

    PubMed  CAS  Google Scholar 

  4. Erez, N., Bershadsky, A., and Geiger, B. (2005) Eur. J. Cell. Biol., 84, 235–244.

    Article  PubMed  CAS  Google Scholar 

  5. Polakis, P. (2007) Curr. Opin. Genet. Dev., 17, 45–51.

    Article  PubMed  CAS  Google Scholar 

  6. Takeichi, M. (1995) Curr. Opin. Cell. Biol., 7, 619–627.

    Article  PubMed  CAS  Google Scholar 

  7. Gumbiner, B. M. (2000) J. Cell Biol., 148, 399–404.

    Article  PubMed  CAS  Google Scholar 

  8. Gooding, J. M., Yap, K. L., and Ikura, M. (2004) BioEssays, 26, 497–511.

    Article  PubMed  CAS  Google Scholar 

  9. Troyanovsky, S. (2005) Eur. J. Cell. Biol., 84, 225–233.

    Article  PubMed  CAS  Google Scholar 

  10. Nagafuchi, A. (2001) Curr. Opin. Cell. Biol., 13, 600–603.

    Article  PubMed  CAS  Google Scholar 

  11. Shapiro, L., Fannon, A. M., Kwong, P. D., Thompson, A., Lehmann, M. S., Grubel, G., Legrand, J. F., Als-Nielsen, J., Colman, D. R., and Hendrickson, W. A. (1995) Nature, 374, 327–337.

    Article  PubMed  CAS  Google Scholar 

  12. Kobielak, A., and Fuchs, E. (2004) Nat. Rev. Mol. Cell. Biol., 5, 614–625.

    Article  PubMed  CAS  Google Scholar 

  13. Kemler, R. (1993) Trends Genet., 9, 317–321.

    Article  PubMed  CAS  Google Scholar 

  14. Rimm, D. L., Koslov, E. R., Kebriaei, P., Cianci, C. D., and Morrow, J. S. (1995) Proc. Natl. Acad. Sci. USA, 92, 8813–8817.

    Article  PubMed  CAS  Google Scholar 

  15. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J., and Weis, W. I. (2005) Cell, 123, 903–915.

    Article  PubMed  CAS  Google Scholar 

  16. Yamada, S., Pokutta, S., Drees, F., Weis, W. I., and Nelson, W. J. (2005) Cell, 123, 889–901.

    Article  PubMed  CAS  Google Scholar 

  17. Chu, Y. S., Thomas, W. A., Eder, O., Pincet, F., Perez, E., Thiery, J. P., and Dufour, S. (2004) J. Cell Biol., 167, 1183–1194.

    Article  PubMed  CAS  Google Scholar 

  18. Sakisaka, T., Ikeda, W., Ogita, H., Fujita, N., and Takai, Y. (2007) Curr. Opin. Cell. Biol., 19, 593–602.

    Article  PubMed  CAS  Google Scholar 

  19. Gloushankova, N. A., Alieva, N. O., Krendel, M. F., Bonder, E. M., Feder, H. H., Vasiliev, J. M., and Gelfand, I. M. (1997) Proc. Natl. Acad. Sci. USA, 94, 879–883.

    Article  PubMed  CAS  Google Scholar 

  20. Krendel, M. F., and Bonder, E. M. (1999) Cell Motil. Cytoskeleton, 43, 296–309.

    Article  PubMed  CAS  Google Scholar 

  21. Yonemura, S., Itoh, M., Nagafuchi, A., and Tsukita, S. (1995) J. Cell Sci., 108, 127–142.

    PubMed  CAS  Google Scholar 

  22. Gloushankova, N. A., Krendel, M. F., Alieva, N. O., Bonder, E. M., Feder, H. H., Vasiliev, J. M., and Gelfand, I. M. (1998) Proc. Natl. Acad. Sci. USA, 95, 4362–4367.

    Article  PubMed  CAS  Google Scholar 

  23. Krendel, M. F., Gloushankova, N. A., Alieva, N. O., Bonder, E. M., Feder, H. H., Vasiliev, J. M., and Gelfand, I. M. (1999) Proc. Natl. Acad. Sci. USA, 96, 9666–9670.

    Article  PubMed  CAS  Google Scholar 

  24. Vasioukhin, V., Bauer, C., Yin, M., and Fuchs, E. (2000) Cell, 100, 209–219.

    Article  PubMed  CAS  Google Scholar 

  25. Helwani, F. M., Kovacs, E. M., Paterson, A. D., Verma, S., Ali, R. G., Fanning, A. S., Weed, S. A., and Yap, A. S. (2004) J. Cell Biol., 164, 899–910.

    Article  PubMed  CAS  Google Scholar 

  26. Verma, S., Shewan, A. M., Scott, J. A., Helwani, F. M., den Elzen, N. R., Miki, H., Takenawa, T., and Yap, A. S. (2004) J. Biol. Chem., 279, 34062–34070.

    Article  PubMed  CAS  Google Scholar 

  27. Ivanov, A. I., Hunt, D., Utech, M., Nusrat, A., and Parkos, C. A. (2005) Mol. Biol. Cell, 16, 2636–2650.

    Article  PubMed  CAS  Google Scholar 

  28. Higgs, H. N., and Pollard, T. D. (2001) Annu. Rev. Biochem., 70, 649–676.

    Article  PubMed  CAS  Google Scholar 

  29. Kovacs, E. M., Goodwin, M., Ali, R. G., Paterson, A. D., and Yap, A. S. (2002) Curr. Biol., 12, 379–382.

    Article  PubMed  CAS  Google Scholar 

  30. El Sayegh, T. Y., Arora, P. D., Laschinger, C. A., Lee, W., Morrison, C., Overall, C. M., Kapus, A., and McCulloch, C. A. (2004) J. Cell Sci., 117, 5117–5131.

    Article  PubMed  CAS  Google Scholar 

  31. Yamazaki, D., Oikawa, T., and Takenawa, T. (2007) J. Cell. Sci., 120, 86–100.

    Article  PubMed  CAS  Google Scholar 

  32. Goode, B. L., and Eck, M. J. (2007) Annu. Rev. Biochem., 76, 593–627.

    Article  PubMed  CAS  Google Scholar 

  33. Kobielak, A., Pasolli, H. A., and Fuchs, E. (2004) Nat. Cell. Biol., 6, 21–30.

    Article  PubMed  CAS  Google Scholar 

  34. Carramusa, L., Ballestrem, C., Zilberman, Y., and Bershadsky, A. D. (2007) J. Cell Sci., 120, 3870–3882.

    Article  PubMed  CAS  Google Scholar 

  35. Zigmond, S. H. (2004) Curr. Opin. Cell Biol., 16, 99–105.

    Article  PubMed  CAS  Google Scholar 

  36. Xu, Y., Moseley, J. B., Sagot, I., Poy, F., Pellman, D., Goode, B. L., and Eck, M. J. (2004) Cell, 116, 711–723.

    Article  PubMed  CAS  Google Scholar 

  37. Higashida, C., Miyoshi, T., Fujita, A., Oceguera-Yanez, F., Monypenny, J., Andou, Y., Narumiya, S., and Watanabe, N. (2004) Science, 303, 2007–2010.

    Article  PubMed  CAS  Google Scholar 

  38. Takaishi, K., Sasaki, T., Kotani, H., Nishioka, H., and Takai, Y. (1997) J. Cell Biol., 139, 1047–1059.

    Article  PubMed  CAS  Google Scholar 

  39. Braga, V. M. M., Machesky, L. M., Hall, A., and Hotchin, N. A. (1997) J. Cell Biol., 137, 1421–1431.

    Article  PubMed  CAS  Google Scholar 

  40. Kim, S. H., Li, Z., and Sacks, D. B. (2000) J. Biol. Chem., 275, 36999–37005.

    Article  PubMed  CAS  Google Scholar 

  41. Kovacs, E. M., Ali, R. G., McCormack, A. J., and Yap, A. S. (2002) J. Biol. Chem., 277, 6708–6718.

    Article  PubMed  CAS  Google Scholar 

  42. Ehrlich, J. S., Hansen, M. D., and Nelson, W. J. (2002) Dev. Cell, 3, 259–270.

    Article  PubMed  CAS  Google Scholar 

  43. Fukata, M., and Kaibuchi, K. (2001) Nat. Rev. Mol. Cell. Biol., 2, 887–897.

    Article  PubMed  CAS  Google Scholar 

  44. Welch, H. C., Coadwell, W. J., Stephens, L. R., and Hawkins, P. T. (2003) FEBS Lett., 546, 93–97.

    Article  PubMed  CAS  Google Scholar 

  45. Stradal, T. E., Rottner, K., Disanza, A., Confalonieri, S., Innocenti, M., and Scita, G. (2004) Trends Cell Biol., 14, 303–311.

    Article  PubMed  CAS  Google Scholar 

  46. Price, L. S., and Collard, J. G. (2001) Semin. Cancer Biol., 11, 167–173.

    Article  PubMed  CAS  Google Scholar 

  47. Noritake, J., Watanabe, T., Sato, K., Wang, S., and Kaibuchi, K. (2005) J. Cell Sci., 118, 2085–2092.

    Article  PubMed  CAS  Google Scholar 

  48. Kitayama, H., Sugimoto, Y., Matsuzaki, T., Ikawa, Y., and Noda, M. (1989) Cell, 56, 77–84.

    Article  PubMed  CAS  Google Scholar 

  49. Yajnik, V., Paulding, C., Sordella, R., McClatchey, A. I., Saito, M., Wahrer, D. C., Reynolds, P., Bell, D. W., Lake, R., van den Heuvel, S., Settleman, J., and Haber, D. A. (2003) Cell, 112, 673–684.

    Article  PubMed  CAS  Google Scholar 

  50. Kooistra, M. R., Dube, N., and Bos, J. L. (2007) J. Cell. Sci., 120, 17–22.

    Article  PubMed  CAS  Google Scholar 

  51. Fukuyama, T., Ogita, H., Kawakatsu, T., Fukuhara, T., Yamada, T., Sato, T., Shimizu, K., Nakamura, T., Matsuda, M., and Takai, Y. (2005) J. Biol. Chem., 280, 815–825.

    PubMed  CAS  Google Scholar 

  52. Kawajiri, A., Itoh, N., Fukata, M., Nakagawa, M., Yamaga, M., Iwamatsu, A., and Kaibuchi, K. (2000) Biochem. Biophys. Res. Commun., 273, 712–717.

    Article  PubMed  CAS  Google Scholar 

  53. Hogan, C., Serpente, N., Cogram, P., Hosking, C. R., Bialucha, C. U., Feller, S. M., Braga, V. M., Birchmeier, W., and Fujita, Y. (2004) Mol. Cell. Biol., 24, 6690–6700.

    Article  PubMed  CAS  Google Scholar 

  54. Fukuyama, T., Ogita, H., Kawakatsu, T., Inagaki, M., and Takai, Y. (2006) Oncogene, 25, 8–19.

    PubMed  CAS  Google Scholar 

  55. Xiao, K., Oas, R. G., Chiasson, C. M., and Kowalczyk, A. P. (2007) Biochim. Biophys. Acta, 1773, 8–16.

    Article  PubMed  CAS  Google Scholar 

  56. Retta, S. F., Balzac, F., and Avolio, M. (2006) Eur. J. Cell. Biol., 85, 283–293.

    Article  PubMed  CAS  Google Scholar 

  57. Hirohashi, S. (1998) Am. J. Pathol., 153, 333–339.

    PubMed  CAS  Google Scholar 

  58. Berx, G., and van Roy, F. (2001) Breast Cancer Res., 3, 289–293.

    Article  PubMed  CAS  Google Scholar 

  59. Cavallaro, U., and Christofori, G. (2004) Nat. Rev. Cancer, 4, 118–132.

    PubMed  CAS  Google Scholar 

  60. Hoschuetzky, H., Aberle, H., and Kemler, R. (1994) J. Cell. Biol., 127, 1375–1380.

    Article  PubMed  CAS  Google Scholar 

  61. Boerner, J. L., Biscardi, J. S., Silva, C. M., and Parsons, S. J. (2005) Mol. Carcinog., 44, 262–273.

    Article  PubMed  CAS  Google Scholar 

  62. Perrais, M., Chen, X., Perez-Moreno, M., and Gumbiner, B. M. (2007) Mol. Biol. Cell, 18, 2013–2025.

    Article  PubMed  CAS  Google Scholar 

  63. Van Hengel, J., and van Roy, F. (2007) Biochim. Biophys. Acta, 1773, 78–88.

    Article  PubMed  CAS  Google Scholar 

  64. Thiery, J. P. (2002) Nat. Rev. Cancer, 2, 442–454.

    Article  PubMed  CAS  Google Scholar 

  65. Yoshiura, K., Kanai, Y., Ochiai, A., Shimoyama, Y., Sugimura, T., and Hirohashi, S. (1995) Proc. Natl. Acad. Sci. USA, 92, 7416–7419.

    Article  PubMed  CAS  Google Scholar 

  66. Berx, G., Becker, K. F., Hofler, H., and van Roy, F. (1998) Hum. Mutat., 12, 226–237.

    Article  PubMed  CAS  Google Scholar 

  67. Hajra, K. M., Ji, X., and Fearon, E. R. (1999) Oncogene, 18, 7274–7279.

    Article  PubMed  CAS  Google Scholar 

  68. Di Croce, L., and Pelicci, P. G. (2003) Eur. J. Cancer, 39, 413–414.

    Article  PubMed  Google Scholar 

  69. Peinado, H., Portillo, F., and Cano, A. (2004) Int. J. Dev. Biol., 48, 365–375.

    Article  PubMed  CAS  Google Scholar 

  70. Koizume, S., Tachibana, K., Sekiya, T., Hirohashi, S., and Shiraishi, M. (2002) Nucleic Acids Res., 30, 4770–4780.

    Article  PubMed  CAS  Google Scholar 

  71. Cano, A., Perez-Moreno, M. A., Rodrigo, I., Locasciop, A., Blanco, M. J., del Barrio, M. G., Portillo, F., and Nieto, M. A. (2000) Nat. Cell Biol., 2, 76–83.

    Article  PubMed  CAS  Google Scholar 

  72. Comijn, J., Berx, G., Vermassen, P., Verschueren, K., van Grunsven, L., Bruyneel, E., Mareel, M., Huylebroeck, D., and van Roy, F. (2001) Mol. Cell, 7, 1267–1278.

    Article  PubMed  CAS  Google Scholar 

  73. Bolos, V., Peinado, H., Perez-Moreno, M. A., Fraga, M. F., Esteller, M., and Cano, A. (2003) J. Cell Sci., 116, 499–511.

    Article  PubMed  CAS  Google Scholar 

  74. Blanco, M. J., Moreno-Bueno, G., Sarrio, D., Locascio, A., Cano, A., Palacios, J., and Nieto, M. A. (2002) Oncogene, 21, 3241–3246.

    Article  PubMed  CAS  Google Scholar 

  75. Jiao, W., Miyazaki, K., and Kitajima, Y. (2002) Br. J. Cancer, 86, 98–101.

    Article  PubMed  CAS  Google Scholar 

  76. Batlle, E., Sancho, E., Franci, C., Dominguez, D., Monfar, M., Baulida, J., and Garcia de Herreros, A. (2000) Nat. Cell Biol., 2, 84–89.

    Article  PubMed  CAS  Google Scholar 

  77. Barrallo-Gimeno, A., and Nieto, M. A. (2005) Development, 132, 3151–3161.

    Article  PubMed  CAS  Google Scholar 

  78. Peinado, H., Olmeda, D., and Cano, A. (2007) Nat. Rev. Cancer, 7, 415–428.

    Article  PubMed  CAS  Google Scholar 

  79. Larue, L., and Bellacosa, A. (2005) Oncogene, 24, 7443–7454.

    Article  PubMed  CAS  Google Scholar 

  80. Alexander, N. R., Tran, N. L., Rekapally, H., Summers, C. E., Glackin, C., and Heimark, R. L. (2006) Cancer Res., 66, 3365–3369.

    Article  PubMed  CAS  Google Scholar 

  81. De Craene, B., Gilbert, B., Stove, C., Bruyneel, E., van Roy, F., and Berx, G. (2005) Cancer Res., 65, 6237–6244.

    Article  PubMed  Google Scholar 

  82. Reynolds, A. B. (2007) Biochim. Biophys. Acta, 1773, 2–7.

    Article  PubMed  CAS  Google Scholar 

  83. Ireton, R. C., Davis, M. A., van Hengel, J., Mariner, D. J., Barnes, K., Thoreson, M. A., Anastasiadis, P. Z., Matrisian, L., Bundy, L. M., Sealy, L., Gilbert, B., van Roy, F., and Reynolds, A. B. (2002) J. Cell Biol., 159, 465–476.

    Article  PubMed  CAS  Google Scholar 

  84. Hoshino, T., Sakisaka, T., Baba, T., Yamada, T., Kimura, T., and Takai, Y. (2005) J. Biol. Chem., 280, 42801–42808.

    Article  PubMed  CAS  Google Scholar 

  85. Fujita, Y., Krause, G., Scheffner, M., Zechner, D., Leddy, H. E., Behrens, J., Sommer, T., and Birchmeier, W. (2002) Nat. Cell Biol., 4, 222–231.

    Article  PubMed  CAS  Google Scholar 

  86. Dupre-Crochet, S., Figueroa, A., Hogan, C., Ferber, E. C., Bialucha, C. U., Adams, J., Richardson, E. C., and Fujita, Y. (2007) Mol. Cell. Biol., 27, 3804–3816.

    Article  PubMed  CAS  Google Scholar 

  87. Kamei, T., Matozaki, T., Sakisaka, T., Kodama, A., Yokoyama, S., Peng, Y. F., Nakano, K., Takaishi, K., and Takai, Y. (1999) Oncogene, 18, 6776–6784.

    Article  PubMed  CAS  Google Scholar 

  88. Xiao, K., Allison, D. F., Buckley, K. M., Kottke, M. D., Vincent, P. A., Faundez, V., and Kowalczyk, A. P. (2003) J. Cell Biol., 163, 535–545.

    Article  PubMed  CAS  Google Scholar 

  89. Bryant, D. M., Wylie, F. G., and Stow, J. L. (2005) Mol. Biol. Cell, 16, 14–23.

    Article  PubMed  CAS  Google Scholar 

  90. Kimura, T., Sakisaka, T., Baba, T., Yamada, T., and Takai, Y. (2006) J. Biol. Chem., 281, 10598–10609.

    Article  PubMed  CAS  Google Scholar 

  91. Suzuki, K., and Takahashi, K. (2006) Biochem. Biophys. Res. Commun., 349, 255–260.

    Article  PubMed  CAS  Google Scholar 

  92. Downing, J. R., and Reynolds, A. B. (1991) Oncogene, 6, 607–613.

    PubMed  CAS  Google Scholar 

  93. Palacios, F., Tushir, J. S., Fujita, Y., and D’souza-Schorey, C. (2005) Mol. Cell. Biol., 25, 389–402.

    Article  PubMed  CAS  Google Scholar 

  94. Mariner, D. J., Anastasiadis, P., Keilhack, H., Bohmer, F. D., Wang, J., and Reynolds, A. B. (2001) J. Biol. Chem., 276, 28006–28013.

    Article  PubMed  CAS  Google Scholar 

  95. Yang, J. Y., Zong, C. S., Xia, W., Wei, Y., Ali-Seyed, M., Li, Z., Broglio, K., Berry, D. A., and Hung, M. C. (2006) Mol. Cell. Biol., 26, 7269–7282.

    Article  PubMed  CAS  Google Scholar 

  96. Thoreson, M. A., and Reynolds, A. B. (2002) Differentiation, 70, 583–589.

    Article  PubMed  CAS  Google Scholar 

  97. Chen, Y. T., Stewart, D. B., and Nelson, W. J. (1999) J. Cell Biol., 144, 687–699.

    Article  PubMed  CAS  Google Scholar 

  98. Lilien, J., and Balsamo, J. (2005) Curr. Opin. Cell Biol., 17, 459–465.

    Article  PubMed  CAS  Google Scholar 

  99. Roura, S., Miravet, S., Piedra, J., Garcia de Herreros, A., and Dunach, M. (1999) J. Biol. Chem., 274, 36734–36740.

    Article  PubMed  CAS  Google Scholar 

  100. Piedra, J., Miravet, S., Castano, J., Palmer, H. G., Heisterkamp, N., Garcia de Herreros, A., and Dunach, M. (2003) Mol. Cell. Biol., 23, 2287–2297.

    Article  PubMed  CAS  Google Scholar 

  101. Behrens, J., von Kries, J. P., Kuhl, M., Bruhn, L., Wedlich, D., Grosschedl, R., and Birchmeier, W. (1996) Nature, 382, 638–642.

    Article  PubMed  CAS  Google Scholar 

  102. Huber, O., Korn, R., McLaughlin, J., Ohsugi, M., Herrmann, B. G., and Kemler, R. (1996) Mech. Dev., 59, 3–10.

    Article  PubMed  CAS  Google Scholar 

  103. He, T. C., Sparks, A. B., Rago, C., Hermeking, H., Zawel, L., da Costa, L. T., Morin, P. J., Vogelstein, B., and Kinzler, K. W. (1998) Science, 281, 1509–1512.

    Article  PubMed  CAS  Google Scholar 

  104. Shtutman, M., Zhurinsky, J., Simcha, I., Albanese, C., D’Amico, M., Pestell, R., and Ben-Ze’ev, A. (1999) Proc. Natl. Acad. Sci. USA, 96, 5522–5527.

    Article  PubMed  CAS  Google Scholar 

  105. Tetsu, O., and McCormick, F. (1999) Nature, 398, 422–426.

    Article  PubMed  CAS  Google Scholar 

  106. Shimokawa, T., Furukawa, Y., Sakai, M., Li, M., Miwa, N., Lin, Y. M., and Nakamura, Y. (2003) Cancer Res., 63, 6116–6120.

    PubMed  CAS  Google Scholar 

  107. Gavert, N., and Ben-Ze’ev, A. (2007) J. Cell. Biochem., 102, 820–828.

    Article  PubMed  CAS  Google Scholar 

  108. Brembeck, F. H., Rosario, M., and Birchmeier, W. (2006) Curr. Opin. Genet. Dev., 16, 51–59.

    Article  PubMed  CAS  Google Scholar 

  109. Brembeck, F. H., Schwarz-Romond, T., Bakkers, J., Wilhelm, S., Hammerschmidt, M., and Birchmeier, W. (2004) Genes Dev., 18, 2225–2230.

    Article  PubMed  CAS  Google Scholar 

  110. Behrens, J., Jerchow, B. A., Wurtele, M., Grimm, J., Asbrand, C., Wirtz, R., Kuhl, M., Wedlich, D., and Birchmeier, W. (1998) Science, 280, 596–599.

    Article  PubMed  CAS  Google Scholar 

  111. Kishida, S., Yamamoto, H., Ikeda, S., Kishida, M., Sakamoto, I., Koyama, S., and Kikuchi, A. (1998) J. Biol. Chem., 273, 10823–10826.

    Article  PubMed  CAS  Google Scholar 

  112. Liu, C., Li, Y., Semenov, M., Han, C., Baeg, G. H., Tan, Y., Zhang, Z., Lin, X., and He, X. (2002) Cell, 108, 837–847.

    Article  PubMed  CAS  Google Scholar 

  113. Pinson, K. I., Brennan, J., Monkley, S., Avery, B. J., and Skarnes, W. C. (2000) Nature, 407, 535–538.

    Article  PubMed  CAS  Google Scholar 

  114. Tolwinski, N. S., Wehrli, M., Rives, A., Erdeniz, N., DiNardo, S., and Wieschaus, E. (2003) Dev. Cell, 4, 407–418.

    Article  PubMed  CAS  Google Scholar 

  115. Kramps, T., Peter, O., Brunner, E., Nellen, D., Froesch, B., Chatterjee, S., Murone, M., Zullig, S., and Basler, K. (2002) Cell, 109, 47–60.

    Article  PubMed  CAS  Google Scholar 

  116. Townsley, F. M., Cliffe, A., and Bienz, M. (2004) Nat. Cell. Biol., 6, 626–633.

    Article  PubMed  CAS  Google Scholar 

  117. Adachi, S., Jigami, T., Yasui, T., Nakano, T., Ohwada, S., Omori, Y., Sugano, S., Ohkawara, B., Shibuya, H., Nakamura, T., and Akiyama, T. (2004) Cancer Res., 64, 8496–8501.

    Article  PubMed  CAS  Google Scholar 

  118. Herzig, M., Savarese, F., Novatchkova, M., Semb, H., and Christofori, G. (2007) Oncogene, 26, 2290–2298.

    Article  PubMed  CAS  Google Scholar 

  119. Morin, P. J., Sparks, A. B., Korinek, V., Barker, N., Clevers, H., Vogelstein, B., and Kinzler, K. W. (1997) Science, 275, 1787–1790.

    Article  PubMed  CAS  Google Scholar 

  120. De La Coste, A., Romagnolo, B., Billuart, P., Renard, C. A., Buendia, M. A., Soubrane, O., Fabre, M., Chelly, J., Beldjord, C., Kahn, A., and Perret, C. (1998) Proc. Natl. Acad. Sci. USA, 95, 8847–8851.

    Article  Google Scholar 

  121. Satoh, S., Daigo, Y., Furukawa, Y., Kato, T., Miwa, N., Nishiwaki, T., Kawasoe, T., Ishiguro, H., Fujita, M., Tokino, T., Sasaki, Y., Imaoka, S., Murata, M., Shimano, T., Yamaoka, Y., and Nakamura, Y. (2000) Nat. Genet., 24, 245–250.

    Article  PubMed  CAS  Google Scholar 

  122. Groden, J., Thliveris, A., Samowitz, W., Carlson, M., Gelbert, L., Albertsen, H., Joslyn, G., Stevens, J., Spirio, L., and Robertson, M. (1991) Cell, 66, 589–600.

    Article  PubMed  CAS  Google Scholar 

  123. Kawasaki, Y., Sato, R., and Akiyama, T. (2003) Nat. Cell. Biol., 5, 211–215.

    Article  PubMed  CAS  Google Scholar 

  124. Zhou, B. P., Deng, J., Xia, W., Xu, J., Li, Y. M., Gunduz, M., and Hung, M. C. (2004) Nat. Cell Biol., 6, 931–940.

    Article  PubMed  CAS  Google Scholar 

  125. Frame, S., and Cohen, P. (2001) Biochem. J., 359, 1–16.

    Article  PubMed  CAS  Google Scholar 

  126. Ciruna, B., and Sleeman, J. (2006) Dev. Cell, 1, 37–49.

    Article  Google Scholar 

  127. Thiery, J. P., and Sleeman, J. (2006) Nat. Rev. Mol. Cell. Biol., 7, 131–142.

    Article  PubMed  CAS  Google Scholar 

  128. Chamorro, M. N., Schwartz, D. R., Vonica, A., Brivanlou, A. H., Cho, K. R., and Varmus, H. E. (2005) EMBO J., 24, 73–84.

    Article  PubMed  CAS  Google Scholar 

  129. Katoh, M., and Katoh, M. (2006) Int. J. Oncol., 29, 163–168.

    PubMed  CAS  Google Scholar 

  130. El Sayegh, T. Y., Kapus, A., and McCulloch, C. A. (2007) FEBS Lett., 581, 167–174.

    Article  PubMed  CAS  Google Scholar 

  131. El Sayegh, T. Y., Arora, P. D., Fan, L., Laschinger, C. A., Lee, W., Greer, P. A., Christopher, A., McCulloch, C. A., and Kapus, A. (2004) Mol. Biol. Cell, 16, 5514–5527.

    Article  CAS  Google Scholar 

  132. Derycke, L. D. M., and Bracke, M. E. (2004) Int. J. Dev., 48, 463–476.

    Article  CAS  Google Scholar 

  133. Nieman, M. T., Prudoff, R. S., Johnson, K. R., and Wheelock, M. J. (1999) J. Cell Biol., 147, 631–644.

    Article  PubMed  CAS  Google Scholar 

  134. Hazan, R. B., Phillips, G. R., Qiao, R. F., Norton, L., and Aaronson, S. A. (2000) J. Cell Biol., 148, 779–790.

    Article  PubMed  CAS  Google Scholar 

  135. Gaggioli, C., Hooper, S., Hidalgo-Carcedo, C., Grosse, R., Marshall, J. F., Harrington, K., and Sahai, E. (2007) Nat. Cell. Biol., 9, 1392–1400.

    Article  PubMed  CAS  Google Scholar 

  136. Suyama, K., Shapiro, I., Guttman, M., and Hazan, R. B. (2002) Cancer Cell, 2, 301–314.

    Article  PubMed  CAS  Google Scholar 

  137. Theisen, C. S., Wahl, J. K., III, Johnson, K. R., and Wheelock, M. J. (2007) Mol. Biol. Cell, 18, 1220–1232.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. A. Gloushankova.

Additional information

Original Russian Text © N. A. Gloushankova, 2008, published in Biokhimiya, 2008, Vol. 73, No. 7, pp. 925–934.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gloushankova, N.A. Changes in regulation of cell—cell adhesion during tumor transformation. Biochemistry Moscow 73, 742–750 (2008). https://doi.org/10.1134/S000629790807002X

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S000629790807002X

Key words

Navigation