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.
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
Willert, K., and Jones, K. A. (2007) Genes Dev., 20, 1394–1404.
Perez-Moreno, M., and Fuchs, E. (2006) Dev. Cell, 11, 601–612.
Katoh, M., and Katoh, M. (2006) Cancer Biol. Ther., 5, 1059–1064.
Erez, N., Bershadsky, A., and Geiger, B. (2005) Eur. J. Cell. Biol., 84, 235–244.
Polakis, P. (2007) Curr. Opin. Genet. Dev., 17, 45–51.
Takeichi, M. (1995) Curr. Opin. Cell. Biol., 7, 619–627.
Gumbiner, B. M. (2000) J. Cell Biol., 148, 399–404.
Gooding, J. M., Yap, K. L., and Ikura, M. (2004) BioEssays, 26, 497–511.
Troyanovsky, S. (2005) Eur. J. Cell. Biol., 84, 225–233.
Nagafuchi, A. (2001) Curr. Opin. Cell. Biol., 13, 600–603.
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.
Kobielak, A., and Fuchs, E. (2004) Nat. Rev. Mol. Cell. Biol., 5, 614–625.
Kemler, R. (1993) Trends Genet., 9, 317–321.
Rimm, D. L., Koslov, E. R., Kebriaei, P., Cianci, C. D., and Morrow, J. S. (1995) Proc. Natl. Acad. Sci. USA, 92, 8813–8817.
Drees, F., Pokutta, S., Yamada, S., Nelson, W. J., and Weis, W. I. (2005) Cell, 123, 903–915.
Yamada, S., Pokutta, S., Drees, F., Weis, W. I., and Nelson, W. J. (2005) Cell, 123, 889–901.
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.
Sakisaka, T., Ikeda, W., Ogita, H., Fujita, N., and Takai, Y. (2007) Curr. Opin. Cell. Biol., 19, 593–602.
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.
Krendel, M. F., and Bonder, E. M. (1999) Cell Motil. Cytoskeleton, 43, 296–309.
Yonemura, S., Itoh, M., Nagafuchi, A., and Tsukita, S. (1995) J. Cell Sci., 108, 127–142.
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.
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.
Vasioukhin, V., Bauer, C., Yin, M., and Fuchs, E. (2000) Cell, 100, 209–219.
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.
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.
Ivanov, A. I., Hunt, D., Utech, M., Nusrat, A., and Parkos, C. A. (2005) Mol. Biol. Cell, 16, 2636–2650.
Higgs, H. N., and Pollard, T. D. (2001) Annu. Rev. Biochem., 70, 649–676.
Kovacs, E. M., Goodwin, M., Ali, R. G., Paterson, A. D., and Yap, A. S. (2002) Curr. Biol., 12, 379–382.
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.
Yamazaki, D., Oikawa, T., and Takenawa, T. (2007) J. Cell. Sci., 120, 86–100.
Goode, B. L., and Eck, M. J. (2007) Annu. Rev. Biochem., 76, 593–627.
Kobielak, A., Pasolli, H. A., and Fuchs, E. (2004) Nat. Cell. Biol., 6, 21–30.
Carramusa, L., Ballestrem, C., Zilberman, Y., and Bershadsky, A. D. (2007) J. Cell Sci., 120, 3870–3882.
Zigmond, S. H. (2004) Curr. Opin. Cell Biol., 16, 99–105.
Xu, Y., Moseley, J. B., Sagot, I., Poy, F., Pellman, D., Goode, B. L., and Eck, M. J. (2004) Cell, 116, 711–723.
Higashida, C., Miyoshi, T., Fujita, A., Oceguera-Yanez, F., Monypenny, J., Andou, Y., Narumiya, S., and Watanabe, N. (2004) Science, 303, 2007–2010.
Takaishi, K., Sasaki, T., Kotani, H., Nishioka, H., and Takai, Y. (1997) J. Cell Biol., 139, 1047–1059.
Braga, V. M. M., Machesky, L. M., Hall, A., and Hotchin, N. A. (1997) J. Cell Biol., 137, 1421–1431.
Kim, S. H., Li, Z., and Sacks, D. B. (2000) J. Biol. Chem., 275, 36999–37005.
Kovacs, E. M., Ali, R. G., McCormack, A. J., and Yap, A. S. (2002) J. Biol. Chem., 277, 6708–6718.
Ehrlich, J. S., Hansen, M. D., and Nelson, W. J. (2002) Dev. Cell, 3, 259–270.
Fukata, M., and Kaibuchi, K. (2001) Nat. Rev. Mol. Cell. Biol., 2, 887–897.
Welch, H. C., Coadwell, W. J., Stephens, L. R., and Hawkins, P. T. (2003) FEBS Lett., 546, 93–97.
Stradal, T. E., Rottner, K., Disanza, A., Confalonieri, S., Innocenti, M., and Scita, G. (2004) Trends Cell Biol., 14, 303–311.
Price, L. S., and Collard, J. G. (2001) Semin. Cancer Biol., 11, 167–173.
Noritake, J., Watanabe, T., Sato, K., Wang, S., and Kaibuchi, K. (2005) J. Cell Sci., 118, 2085–2092.
Kitayama, H., Sugimoto, Y., Matsuzaki, T., Ikawa, Y., and Noda, M. (1989) Cell, 56, 77–84.
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.
Kooistra, M. R., Dube, N., and Bos, J. L. (2007) J. Cell. Sci., 120, 17–22.
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.
Kawajiri, A., Itoh, N., Fukata, M., Nakagawa, M., Yamaga, M., Iwamatsu, A., and Kaibuchi, K. (2000) Biochem. Biophys. Res. Commun., 273, 712–717.
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.
Fukuyama, T., Ogita, H., Kawakatsu, T., Inagaki, M., and Takai, Y. (2006) Oncogene, 25, 8–19.
Xiao, K., Oas, R. G., Chiasson, C. M., and Kowalczyk, A. P. (2007) Biochim. Biophys. Acta, 1773, 8–16.
Retta, S. F., Balzac, F., and Avolio, M. (2006) Eur. J. Cell. Biol., 85, 283–293.
Hirohashi, S. (1998) Am. J. Pathol., 153, 333–339.
Berx, G., and van Roy, F. (2001) Breast Cancer Res., 3, 289–293.
Cavallaro, U., and Christofori, G. (2004) Nat. Rev. Cancer, 4, 118–132.
Hoschuetzky, H., Aberle, H., and Kemler, R. (1994) J. Cell. Biol., 127, 1375–1380.
Boerner, J. L., Biscardi, J. S., Silva, C. M., and Parsons, S. J. (2005) Mol. Carcinog., 44, 262–273.
Perrais, M., Chen, X., Perez-Moreno, M., and Gumbiner, B. M. (2007) Mol. Biol. Cell, 18, 2013–2025.
Van Hengel, J., and van Roy, F. (2007) Biochim. Biophys. Acta, 1773, 78–88.
Thiery, J. P. (2002) Nat. Rev. Cancer, 2, 442–454.
Yoshiura, K., Kanai, Y., Ochiai, A., Shimoyama, Y., Sugimura, T., and Hirohashi, S. (1995) Proc. Natl. Acad. Sci. USA, 92, 7416–7419.
Berx, G., Becker, K. F., Hofler, H., and van Roy, F. (1998) Hum. Mutat., 12, 226–237.
Hajra, K. M., Ji, X., and Fearon, E. R. (1999) Oncogene, 18, 7274–7279.
Di Croce, L., and Pelicci, P. G. (2003) Eur. J. Cancer, 39, 413–414.
Peinado, H., Portillo, F., and Cano, A. (2004) Int. J. Dev. Biol., 48, 365–375.
Koizume, S., Tachibana, K., Sekiya, T., Hirohashi, S., and Shiraishi, M. (2002) Nucleic Acids Res., 30, 4770–4780.
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.
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.
Bolos, V., Peinado, H., Perez-Moreno, M. A., Fraga, M. F., Esteller, M., and Cano, A. (2003) J. Cell Sci., 116, 499–511.
Blanco, M. J., Moreno-Bueno, G., Sarrio, D., Locascio, A., Cano, A., Palacios, J., and Nieto, M. A. (2002) Oncogene, 21, 3241–3246.
Jiao, W., Miyazaki, K., and Kitajima, Y. (2002) Br. J. Cancer, 86, 98–101.
Batlle, E., Sancho, E., Franci, C., Dominguez, D., Monfar, M., Baulida, J., and Garcia de Herreros, A. (2000) Nat. Cell Biol., 2, 84–89.
Barrallo-Gimeno, A., and Nieto, M. A. (2005) Development, 132, 3151–3161.
Peinado, H., Olmeda, D., and Cano, A. (2007) Nat. Rev. Cancer, 7, 415–428.
Larue, L., and Bellacosa, A. (2005) Oncogene, 24, 7443–7454.
Alexander, N. R., Tran, N. L., Rekapally, H., Summers, C. E., Glackin, C., and Heimark, R. L. (2006) Cancer Res., 66, 3365–3369.
De Craene, B., Gilbert, B., Stove, C., Bruyneel, E., van Roy, F., and Berx, G. (2005) Cancer Res., 65, 6237–6244.
Reynolds, A. B. (2007) Biochim. Biophys. Acta, 1773, 2–7.
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.
Hoshino, T., Sakisaka, T., Baba, T., Yamada, T., Kimura, T., and Takai, Y. (2005) J. Biol. Chem., 280, 42801–42808.
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.
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.
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.
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.
Bryant, D. M., Wylie, F. G., and Stow, J. L. (2005) Mol. Biol. Cell, 16, 14–23.
Kimura, T., Sakisaka, T., Baba, T., Yamada, T., and Takai, Y. (2006) J. Biol. Chem., 281, 10598–10609.
Suzuki, K., and Takahashi, K. (2006) Biochem. Biophys. Res. Commun., 349, 255–260.
Downing, J. R., and Reynolds, A. B. (1991) Oncogene, 6, 607–613.
Palacios, F., Tushir, J. S., Fujita, Y., and D’souza-Schorey, C. (2005) Mol. Cell. Biol., 25, 389–402.
Mariner, D. J., Anastasiadis, P., Keilhack, H., Bohmer, F. D., Wang, J., and Reynolds, A. B. (2001) J. Biol. Chem., 276, 28006–28013.
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.
Thoreson, M. A., and Reynolds, A. B. (2002) Differentiation, 70, 583–589.
Chen, Y. T., Stewart, D. B., and Nelson, W. J. (1999) J. Cell Biol., 144, 687–699.
Lilien, J., and Balsamo, J. (2005) Curr. Opin. Cell Biol., 17, 459–465.
Roura, S., Miravet, S., Piedra, J., Garcia de Herreros, A., and Dunach, M. (1999) J. Biol. Chem., 274, 36734–36740.
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.
Behrens, J., von Kries, J. P., Kuhl, M., Bruhn, L., Wedlich, D., Grosschedl, R., and Birchmeier, W. (1996) Nature, 382, 638–642.
Huber, O., Korn, R., McLaughlin, J., Ohsugi, M., Herrmann, B. G., and Kemler, R. (1996) Mech. Dev., 59, 3–10.
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.
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.
Tetsu, O., and McCormick, F. (1999) Nature, 398, 422–426.
Shimokawa, T., Furukawa, Y., Sakai, M., Li, M., Miwa, N., Lin, Y. M., and Nakamura, Y. (2003) Cancer Res., 63, 6116–6120.
Gavert, N., and Ben-Ze’ev, A. (2007) J. Cell. Biochem., 102, 820–828.
Brembeck, F. H., Rosario, M., and Birchmeier, W. (2006) Curr. Opin. Genet. Dev., 16, 51–59.
Brembeck, F. H., Schwarz-Romond, T., Bakkers, J., Wilhelm, S., Hammerschmidt, M., and Birchmeier, W. (2004) Genes Dev., 18, 2225–2230.
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.
Kishida, S., Yamamoto, H., Ikeda, S., Kishida, M., Sakamoto, I., Koyama, S., and Kikuchi, A. (1998) J. Biol. Chem., 273, 10823–10826.
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.
Pinson, K. I., Brennan, J., Monkley, S., Avery, B. J., and Skarnes, W. C. (2000) Nature, 407, 535–538.
Tolwinski, N. S., Wehrli, M., Rives, A., Erdeniz, N., DiNardo, S., and Wieschaus, E. (2003) Dev. Cell, 4, 407–418.
Kramps, T., Peter, O., Brunner, E., Nellen, D., Froesch, B., Chatterjee, S., Murone, M., Zullig, S., and Basler, K. (2002) Cell, 109, 47–60.
Townsley, F. M., Cliffe, A., and Bienz, M. (2004) Nat. Cell. Biol., 6, 626–633.
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.
Herzig, M., Savarese, F., Novatchkova, M., Semb, H., and Christofori, G. (2007) Oncogene, 26, 2290–2298.
Morin, P. J., Sparks, A. B., Korinek, V., Barker, N., Clevers, H., Vogelstein, B., and Kinzler, K. W. (1997) Science, 275, 1787–1790.
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.
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.
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.
Kawasaki, Y., Sato, R., and Akiyama, T. (2003) Nat. Cell. Biol., 5, 211–215.
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.
Frame, S., and Cohen, P. (2001) Biochem. J., 359, 1–16.
Ciruna, B., and Sleeman, J. (2006) Dev. Cell, 1, 37–49.
Thiery, J. P., and Sleeman, J. (2006) Nat. Rev. Mol. Cell. Biol., 7, 131–142.
Chamorro, M. N., Schwartz, D. R., Vonica, A., Brivanlou, A. H., Cho, K. R., and Varmus, H. E. (2005) EMBO J., 24, 73–84.
Katoh, M., and Katoh, M. (2006) Int. J. Oncol., 29, 163–168.
El Sayegh, T. Y., Kapus, A., and McCulloch, C. A. (2007) FEBS Lett., 581, 167–174.
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.
Derycke, L. D. M., and Bracke, M. E. (2004) Int. J. Dev., 48, 463–476.
Nieman, M. T., Prudoff, R. S., Johnson, K. R., and Wheelock, M. J. (1999) J. Cell Biol., 147, 631–644.
Hazan, R. B., Phillips, G. R., Qiao, R. F., Norton, L., and Aaronson, S. A. (2000) J. Cell Biol., 148, 779–790.
Gaggioli, C., Hooper, S., Hidalgo-Carcedo, C., Grosse, R., Marshall, J. F., Harrington, K., and Sahai, E. (2007) Nat. Cell. Biol., 9, 1392–1400.
Suyama, K., Shapiro, I., Guttman, M., and Hazan, R. B. (2002) Cancer Cell, 2, 301–314.
Theisen, C. S., Wahl, J. K., III, Johnson, K. R., and Wheelock, M. J. (2007) Mol. Biol. Cell, 18, 1220–1232.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © N. A. Gloushankova, 2008, published in Biokhimiya, 2008, Vol. 73, No. 7, pp. 925–934.
Rights 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
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S000629790807002X