Biochemistry (Moscow)

, Volume 73, Issue 7, pp 733–741 | Cite as

Evolution of cell interactions with extracellular matrix during carcinogenesis

  • A. Y. AlexandrovaEmail author


Interaction of cells with extracellular matrix (ECM) largely defines migration capacity of cells and ways of their dissemination in normal tissue processes and during tumor progression. We review current knowledge about structure of cell adhesions with ECM and their alterations during carcinogenesis. We analyze how changes in structure of cell—matrix adhesions and ECM itself lead to acquisition of neoplastic properties by cells. Modern concepts of tumor cell motility and changes in the relationships of cells with ECM during tumor development are presented. Contemporary approaches for influencing the cell—ECM adhesion structures for inhibition of invasion and metastasis are briefly discussed.

Key words

focal adhesions actin cytoskeleton extracellular matrix cell migration invasion 



extracellular matrix


epithelial-mesenchymal transition


focal adhesion kinase


focal contacts/focal adhesion


mesenchymal-amoeboid transition


matrix metalloproteases


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Gumbiner, B. M. (1996) Cell, 84, 345–357.PubMedCrossRefGoogle Scholar
  2. 2.
    Yamada, K. M., and Geiger, B. (1997) Curr. Opin. Cell Biol., 9, 76–85.PubMedCrossRefGoogle Scholar
  3. 3.
    Geiger, B., Bershadsky, A., Pankov, R., and Yamada, K. M. (2001) Nat. Rev. Mol. Cell Biol., 2, 793–805.PubMedCrossRefGoogle Scholar
  4. 4.
    Bosman, F. T., Havenith, M. G., Visser, R., and Cleutjens, J. P. (1992) Progr. Histochem. Cytochem., 24, 1–92.Google Scholar
  5. 5.
    Kleiman, H. K., Koblinski, J., Lee, S., and Engbring, J. (2001) Surg. Oncol. Clin. N. Am., 10, 329–338.Google Scholar
  6. 6.
    Lyubimov, A. V., Black, K. L., and Lyubimova, Yu. Yu. (2003) Vestnik RONTs, 3, 83–91.Google Scholar
  7. 7.
    Condeelis, J., Singer, R. H., and Segall, J. E. (2005) Annu. Rev. Cell Dev. Biol., 21, 695–718.PubMedCrossRefGoogle Scholar
  8. 8.
    Friedl, P., and Wolf, K. (2003) Nature Rev., 3, 362–374.CrossRefGoogle Scholar
  9. 9.
    Thiery, J. P. (2002) Nature Rev. Cancer, 2, 442–454.CrossRefGoogle Scholar
  10. 10.
    Lauffenburger, D. A., and Horwitz, A. F. (1996) Cell, 84, 359–369.PubMedCrossRefGoogle Scholar
  11. 11.
    Small, J. V., Kaverina, I., Krylyshkina, O., and Rottner, K. (1999) FEBS Lett., 452, 96–99.PubMedCrossRefGoogle Scholar
  12. 12.
    Hall, A. (1998) Science, 279, 509–514.PubMedCrossRefGoogle Scholar
  13. 13.
    Nobes, C. D., and Hall, A. (1999) J. Cell Biol., 144, 1235–1244.PubMedCrossRefGoogle Scholar
  14. 14.
    Etienne-Manneville, S., and Hall, A. (2002) Nature. (Lond.), 420, 629–635.CrossRefGoogle Scholar
  15. 15.
    Nobes, C. D., and Hall, A. (1995) Cell, 81, 53–62.PubMedCrossRefGoogle Scholar
  16. 16.
    Rottner, K., Hall, A., and Small, J. V. (1999) Curr. Biol., 9, 640–648.PubMedCrossRefGoogle Scholar
  17. 17.
    Ridley, A. J. (2001) Trends Cell. Biol., 11, 471–477.PubMedCrossRefGoogle Scholar
  18. 18.
    Wolf, K., Mazo, I., Leung, H., Engelke, K., von Andrian, U. H., Deryugina, E. I., Strongin, A. Y., Brocker, E. B., and Friedl, P. (2003) J. Cell Biol., 160, 267–277.PubMedCrossRefGoogle Scholar
  19. 19.
    Yamazaki, D., Kurisu, S., and Takenawa, T. (2005) Cancer. Sci., 96, 379–386.PubMedCrossRefGoogle Scholar
  20. 20.
    Abercrombie, M., and Dunn, G. A. (1975) Exp. Cell. Res., 92, 57–62.PubMedCrossRefGoogle Scholar
  21. 21.
    Izzard, C. S., and Lochner, L. R. (1980) J. Cell. Sci., 42, 81–116.PubMedGoogle Scholar
  22. 22.
    Burridge, K., Fath, K., Kelly, T., Nucolls, G., and Turner, C. (1988) Ann. Rev. Cell Biol., 4, 487–525.PubMedGoogle Scholar
  23. 23.
    Volberg, T., Geiger, B., Citi, S., and Bershadsky, A. D. (1994) Cell Motil. Cytoskeleton, 29, 321–338.PubMedCrossRefGoogle Scholar
  24. 24.
    Helfman, D. M., Levy, E. T., Berthier, C., Shtutman, M., Riveline, D., Grosheva, I., Lachish-Zalait, A., Elbaum, M., and Bershadsky, A. D. (1999) Mol. Biol. Cell, 10, 3097–3112.PubMedGoogle Scholar
  25. 25.
    Zamir, E., Katz, B. Z., Aota, S., Yamada, K. M., Geiger, B., and Kam, Z. (1999) J. Cell Sci., 112, 1655–1669.PubMedGoogle Scholar
  26. 26.
    Neff, N. T., Lowrey, C., Decker, C., Tovar, A., Damsky, C., Buck, C., and Horwitz, A. F. (1982) J. Cell Biol., 95, 654–666.PubMedCrossRefGoogle Scholar
  27. 27.
    Machesky, L. M., and Hall, A. (1997) J. Cell Biol., 138, 913–926.PubMedCrossRefGoogle Scholar
  28. 28.
    Riveline, D., Zamir, E., Balaban, N. Q., Schwartz, U. S., Ishizaki, T., Narumiya, S., Kam, Z., Geiger, B., and Bershadsky, A. D. (2001) J. Cell Biol., 153, 1175–1185.PubMedCrossRefGoogle Scholar
  29. 29.
    Chrzanowska-Wodnicka, M., and Burridge, K. (1996) J. Cell Biol., 133, 1403–1415.PubMedCrossRefGoogle Scholar
  30. 30.
    Zamir, E., and Geiger, B. (2001) J. Cell Sci., 114, 3583–3590.PubMedGoogle Scholar
  31. 31.
    Schoenwaelder, S. M., and Burridge, K. (1999) Curr. Opin. Cell Biol., 11, 274–286.PubMedCrossRefGoogle Scholar
  32. 32.
    Clark, E. A., King, W. G., Brugge, J. S., Simons, M., and Hynes, R. O. (1998) J. Cell Biol., 142, 573–586.PubMedCrossRefGoogle Scholar
  33. 33.
    Alexandrova, A. Y., Arnold, K., Shtutman, M. S., Schaub, S., Meister, J. J., Geiger, B., Bershadsky, A. D., and Verkhovsky, A. B. (2001) Mol. Biol. Cell, 12, 263A.Google Scholar
  34. 34.
    Zaidel-Bar, R., Ballestrem, C., Kam, Z., and Geiger, B. (2003) J. Cell Sci., 116, 4605–4613.PubMedCrossRefGoogle Scholar
  35. 35.
    Bershadsky, A. D., Ballestrem, C., Carramusa, L., Zilberman, Y., Gilquin, B., Khochbin, S., Alexandrova, A. Y., Verkhovsky, A. B., Shemesh, T., and Kozlov, M. M. (2006) Eur. J. Cell Biol., 85, 165–173.PubMedCrossRefGoogle Scholar
  36. 36.
    Beningo, K. A., Dembo, M., Kaverina, I. N., Smal, J. V., and Wang, Y. (2001) J. Cell Biol., 153, 881–888.PubMedCrossRefGoogle Scholar
  37. 37.
    Totsukawa, G., Wu, Y., Sasaki, Y., Hartshorne, D. J., Yamakita, Y., Yamashiro, S., and Matsumura, F. (2004) J. Cell. Biol., 164, 427–439.PubMedCrossRefGoogle Scholar
  38. 38.
    Friedl, P., Zanker, K. S., and Bröcker, E.-B. (1998) Microsc. Res. Tech., 43, 369–378.PubMedCrossRefGoogle Scholar
  39. 39.
    Balaban, N. Q., Schwarz, U. S., Riveline, D., Goichberg, P., Tzur, G., Sabanay, I., Mahalu, D., Safran, S., Bershadsky, A., Addadi, L., and Geiger, B. (2001) Nat. Cell. Biol., 3, 466–472.PubMedCrossRefGoogle Scholar
  40. 40.
    Katz, N., Zamir, E., Bershadsky, A., Kam, Z., Yamada, K. M., and Geiger, B. (2000) Moll. Biol. Cell, 11, 1047–1060.Google Scholar
  41. 41.
    Zamir, E., Katz, M., Posen, Y., Erez, N., Yamada, K. M., Katz, B. Z., Lin, S., Lin, D. C., Bershadsky, A., Kam, Z., and Geiger, B. (2000) Nat. Cell Biol., 2, 191–196.PubMedCrossRefGoogle Scholar
  42. 42.
    Pankov, R., Cukierman, E., Katz, B. Z., Matsumoto, K., Lin, D. C., Lin, S., Hahn, C., and Yamada, K. M. (2000) J. Cell Biol., 148, 1075–1090.PubMedCrossRefGoogle Scholar
  43. 43.
    Takino, T., Watanabe, Y., Matsui, M., Miyamori, H., Kodo, T., Seiki, M., and Sato, H. (2006) Exp. Cell Res., 312, 1381–1389.PubMedCrossRefGoogle Scholar
  44. 44.
    Tarone, G., Cirillo, D., Giancotti, F. G., Comoglio, P. M., and Marchisio, P. C. (1985) Exp. Cell Res., 159, 141–157.PubMedCrossRefGoogle Scholar
  45. 45.
    Linder, S., and Aepfelbacher, M. (2003) Trends Cell Biol., 13, 376–385.PubMedCrossRefGoogle Scholar
  46. 46.
    Bowden, E. T., Onikoyi, E., Slack, R., Myoui, A., Yoneda, T., Yamada, K. M., and Mueller, S. C. (2006) Exp. Cell. Res., 312, 1240–1253.PubMedCrossRefGoogle Scholar
  47. 47.
    Linder, S., Nelson, D., Weiss, M., and Aepfelbacher, M. (1999) Proc. Natl. Acad. Sci. USA, 96, 9648–9653.PubMedCrossRefGoogle Scholar
  48. 48.
    Lakkakorpi, P. T., Nakamura, I., Nagy, R. M., Parsons, J. T., Rodan, G. A., and Duong, L. T. (1999) J. Biol. Chem., 274, 4900–4907.PubMedCrossRefGoogle Scholar
  49. 49.
    Duong, L. T., Lakkakorpi, P. T., Nakamura, I., Machwate, M., Nagy, R. M., and Rodan, G. A. (1998) J. Clin. Invest., 102, 881–892.PubMedCrossRefGoogle Scholar
  50. 50.
    Wesolowski, G., Duong, L. T., Lakkakorpi, P. T., Nagy, R. M., Tezuka, K., Tanaka, H., Rodan, G. A., and Rodan, S. B. (1995) Exp. Cell Res., 219, 679–686.PubMedCrossRefGoogle Scholar
  51. 51.
    Gimona, M. (2008) Semin. Cancer Biol., 18, 23–34.PubMedCrossRefGoogle Scholar
  52. 52.
    Ayala, I., Baldassarre, M., Caldieri, G., and Buccione, R. (2006) Eur. J. Cell Biol., 85, 159–164.PubMedCrossRefGoogle Scholar
  53. 53.
    Linder, S. (2007) Trends Cell Biol., 17, 107–117.PubMedCrossRefGoogle Scholar
  54. 54.
    Yamaguchi, H., Pixey, F., and Condeelis, J. (2006) Eur. J. Cell Biol., 85, 213–218.PubMedCrossRefGoogle Scholar
  55. 55.
    Vasiliev, J. M., and Gelfand, I. M. (1980) in Neoplastic and. Normal Cells in Culture, Cambridge University Press, Cambridge.Google Scholar
  56. 56.
    Vasiliev, J. M. (2004) Int. J. Dev. Biol., 48, 425–439.PubMedCrossRefGoogle Scholar
  57. 57.
    Farina, K. L., Wyckoff, J. B., Rivera, J., Lee, H., Segall, J. E., Condeelis, J. S., and Jones, J. G. (1998) Cancer Res., 58, 2528–2532.PubMedGoogle Scholar
  58. 58.
    Sahai, E., Olson, M. F., and Marshall, C. J. (2001) EMBO. J., 20, 755–766.PubMedCrossRefGoogle Scholar
  59. 59.
    Harris, A. K., Wild, P., and Stopak, D. (1980) Science, 208, 177–179.PubMedCrossRefGoogle Scholar
  60. 60.
    Hynes, R. O. (1992) Cell, 69, 11–25.PubMedCrossRefGoogle Scholar
  61. 61.
    Schwartz, M. A., Schaller, M. D., and Ginsberg, M. H. (1995) Annu. Rev. Cell Dev. Biol., 11, 549–599.PubMedCrossRefGoogle Scholar
  62. 62.
    Giancotti, F. G., and Ruoslahti, E. (1999) Science, 285, 1028–1032.PubMedCrossRefGoogle Scholar
  63. 63.
    Hynes, R. O. (2002) Cell, 110, 673–687.PubMedCrossRefGoogle Scholar
  64. 64.
    Guo, W., and Giancotti, F. G. (2004) Nat. Rev. Mol. Cell. Biol., 5, 816–826.PubMedCrossRefGoogle Scholar
  65. 65.
    Schwartz, M. A. (1997) J. Cell Biol., 139, 575–578.PubMedCrossRefGoogle Scholar
  66. 66.
    Howe, A., Aplin, A. E., Alahari, S. K., and Juliano, R. L. (1998) Curr. Opin. Cell Biol., 10, 220–231.PubMedCrossRefGoogle Scholar
  67. 67.
    Frisch, S. M., and Ruoslahti, E. (1997) Curr. Opin. Cell. Biol., 9, 701–706.PubMedCrossRefGoogle Scholar
  68. 68.
    Bissell, M. J., and Radisky, D. (2001) Nature Rev. Cancer, 1, 46–54.CrossRefGoogle Scholar
  69. 69.
    Wiseman, B. S., and Werb, Z. (2002) Science, 296, 1046–1049.PubMedCrossRefGoogle Scholar
  70. 70.
    Maschler, S., Wirl, G., Spring, H., Bredow, D. V., Sordat, I., Beug, H., and Reichmann, E. (2005) Oncogene, 17, 2032–2041.CrossRefGoogle Scholar
  71. 71.
    Mercurio, A. M., and Rabinovitz, I. (2001) Semin. Cancer. Biol., 11, 129–141.PubMedCrossRefGoogle Scholar
  72. 72.
    Ramos, D. M., But, M., Regezi, J., Schmidt, B. L., Atakilit, A., Dang, D., Ellis, D., Jordan, R., and Li, X. (2002) Matrix Biol., 21, 297–307.PubMedCrossRefGoogle Scholar
  73. 73.
    Albelda, S. M., Mette, S. A., Elder, D. E., Stewart, R., Damjanovich, L., Herlyn, M., and Buck, C. A. (1990) Cancer Res., 50, 6757–6764.PubMedGoogle Scholar
  74. 74.
    Gladson, C. L., and Cheresh, D. A. (1991) J. Clin. Invest., 88, 1924–1932.PubMedCrossRefGoogle Scholar
  75. 75.
    Miranti, C. K., and Brugge, J. S. (2002) Nature Cell Biol., 4, E83–E90.PubMedCrossRefGoogle Scholar
  76. 76.
    Giancotti, F. G., and Tarone, G. (2003) Annu. Rev. Cell. Dev. Biol., 19, 173–206.PubMedCrossRefGoogle Scholar
  77. 77.
    Brooks, P. C., Strumblad, S., Sanders, L. C., von Schalscha, T. L., Aimes, R. T., Stetler-Stevenson, W. G., Quigley, J. P., and Cheresh, D. A. (1996) Cell, 85, 683–693.PubMedCrossRefGoogle Scholar
  78. 78.
    Rolli, M., Fransvea, E., Pilch, J., Saven, A., and Felding-Habermann, B. (2003) Proc. Natl. Acad. Sci. USA, 100, 9482–9487.PubMedCrossRefGoogle Scholar
  79. 79.
    Hu, B., Jarzynka, M. J., Guo, P., Imanishi, Y., Schlaepfer, D. D., and Cheng, S. Y. (2006) Cancer Res., 66, 775–783.PubMedCrossRefGoogle Scholar
  80. 80.
    Tan, C., Cruet-Hennequart, S., Troussard, A., Fazli, L., Costello, P., Sutton, K., Wheeler, J., Gleave, M., Sanghera, J., and Dedhar, S. (2004) Cancer Cell, 5, 79–90.PubMedCrossRefGoogle Scholar
  81. 81.
    De, S., Razorenova, O., McCabe, N. P., O’Toole, T., Qin, J., and Byzova, T. V. (2005) Proc. Natl. Acad. Sci. USA, 102, 7589–7594.PubMedCrossRefGoogle Scholar
  82. 82.
    Owens, L. V., Xu, L., Craven, R. J., Dent, G. A., Weiner, T. M., Kornberg, L., Liu, E. T., and Cance, W. G. (1995) Cancer Res., 55, 2752–2755.PubMedGoogle Scholar
  83. 83.
    Kahana, O., Micksche, M., Witz, I. P., and Yron, L. (2002) Oncogene, 21, 3969–3977.PubMedCrossRefGoogle Scholar
  84. 84.
    Hsia, D. A., Mitra, S. K., Hauck, C. R., Streblow, D. N., Nelson, J. A., Ilic, D., Huang, S., Li, E., Nemerow, G. R., Leng, J., Spencer, K. S. R., Cheresh, D. A., and Schlaepfer, D. D. (2003) J. Cell Biol., 160, 753–767.PubMedCrossRefGoogle Scholar
  85. 85.
    Schlaepfer, D. D., Mitra, S. K., and Ilic, D. (2004) Biochim. Biophys. Acta, 1692, 77–102.PubMedGoogle Scholar
  86. 86.
    Kornberg, L. J. (1998) Head Neck, 20, 745–752.PubMedCrossRefGoogle Scholar
  87. 87.
    Cance, W. G., Harris, J. E., Iacocca, M. V., Roche, E., Yang, X., Chang, J., Simkins, S., and Xu, L. (2000) Clin. Cancer Res., 6, 2417–2423.PubMedGoogle Scholar
  88. 88.
    Gabarra-Niecko, V., Schaller, M. D., and Dunty, J. M. (2003) Cancer Metastasis Rev., 4, 359–374.CrossRefGoogle Scholar
  89. 89.
    Ilic, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., Yamamoto, T., and Aizawa, S. (1995) Nature, 377, 539–544.PubMedCrossRefGoogle Scholar
  90. 90.
    Zeng, L., Si, X., Yu, W. P., Le, H. T., Ng, K. P., Teng, R. M., Ryan, K., Wang, D. Z., Ponniah, S., and Pallen, C. J. (2003) J. Cell Biol., 160, 137–146.PubMedCrossRefGoogle Scholar
  91. 91.
    Webb, D. J., Donais, K., Whitmore, L. A., Thomas, S. M., Turner, C. E., Parsons, J. T., and Horwitz, A. F. (2004) Nat. Cell. Biol., 2, 154–161.CrossRefGoogle Scholar
  92. 92.
    Burridge, K., and Wennerberg, K. (2004) Cell, 2, 167–179.CrossRefGoogle Scholar
  93. 93.
    Tilghman, R. W., and Parsons, J. T. (2008) Semin. Cancer. Biol., 18, 45–52.PubMedCrossRefGoogle Scholar
  94. 94.
    Petit, V., Boyer, B., Lentz, D., Turner, C. E., Thiery, J. P., and Valles, A. M. (2000) J. Cell. Biol., 148, 957–970.PubMedCrossRefGoogle Scholar
  95. 95.
    Tsubouchi, A., Sakakura, J., Yagi, R., Mazaki, Y., Schaefer, E., Yano, H., and Sabe, H. (2002) J. Cell. Biol., 159, 673–683.PubMedCrossRefGoogle Scholar
  96. 96.
    Azuma, K., Tanaka, M., Uekita, T., Inoue, S., Yokota, J., Ouchi, Y., and Sakai, R. (2005) Oncogene, 24, 4754–4764.PubMedCrossRefGoogle Scholar
  97. 97.
    Katz, M., Amit, I., Citri, A., Shay, T., Carvalho, S., Lavi, S., Milanezi, F., Lyass, L., Amariglio, N., Jacob-Hirsch, J., Ben-Chetrit, N., Tarcic, G., Lindzen, M., Avraham, R., Liao, Y.-C., Trusk, P., Lyass, A., Rechavi, G., Spector, N. L., Lo, S. H., Schmitt, F., Bacus, S. S., and Yarden, Y. (2007) Nat. Cell Biol., 9, 961–969.PubMedCrossRefGoogle Scholar
  98. 98.
    Potter, D. A., Tirnauer, J. S., Janssen, R., Croall, D. E., Hughes, C. N., Fiacco, K. A., Mier, J. W., Maki, M., and Herman, I. M. (1998) J. Cell Biol., 141, 647–662.PubMedCrossRefGoogle Scholar
  99. 99.
    Pfaff, M., Du, X., and Ginsberg, M. H. (1999) FEBS Lett., 460, 17–22.PubMedCrossRefGoogle Scholar
  100. 100.
    Carragher, N. O., and Frame, M. C. (2004) Trends Cell. Biol., 14, 241–249.PubMedCrossRefGoogle Scholar
  101. 101.
    Gimona, M., and Buccione, R. (2006) Int. J. Biochem. Cell. Biol., 38, 1875–1892.PubMedCrossRefGoogle Scholar
  102. 102.
    Seals, D. F., Azucena, E. F., Jr., Pass, I., Tesfay, L., Gordon, R., Woodrow, M., Resau, J. H., and Courtneidge, S. A. (2005) Cancer Cell, 7, 155–165.PubMedCrossRefGoogle Scholar
  103. 103.
    Moreau, V., Tatin, F., Varon, C., Anies, G., Savona-Barron, C., and Genot, E. (2006) Eur. J. Cell Biol., 85, 319–325.PubMedCrossRefGoogle Scholar
  104. 104.
    Kaverina, I., Stradal, T. E., and Gimona, M. (2003) J. Cell. Sci., 116, 4915–4924.PubMedCrossRefGoogle Scholar
  105. 105.
    Burgstaller, G., and Gimona, M. (2004) J. Cell Sci., 117, 223–231.PubMedCrossRefGoogle Scholar
  106. 106.
    Sternlicht, M. D., and Werb, Z. (2001) Annu. Rev. Cell Dev. Biol., 17, 463–516.PubMedCrossRefGoogle Scholar
  107. 107.
    Coussens, L. M., Fingleton, B., and Matrisian, L. M. (2002) Science, 295, 2387–2392.PubMedCrossRefGoogle Scholar
  108. 108.
    Wolf, K., Yi, I., Wu, Y., Liu, Y., Geiger, J., Tam, E., Overall, C., Stack, M. S., and Friedl, P. (2007) Nat. Cell Biol., 9, 893–904.PubMedCrossRefGoogle Scholar
  109. 109.
    Ioachim, E., Charchanti, A., Briasoulis, E., Karavasilis, V., Tsanou, H., Arvanitis, D. L., Pavlidis, N., and Agnantis, N. J. (2002) Eur. J. Cancer, 38, 2362–2370.Google Scholar
  110. 110.
    Sherman-Baust, C. A., Weeraratna, A. T., Rangel, L. B., Pizer, E. S., Cho, K. R., Schwartz, D. R., Shock, T., and Morin, P. J. (2003) Cancer Cell, 3, 377–386.PubMedCrossRefGoogle Scholar
  111. 111.
    Sahai, E., and Marshall, C. J. (2002) Nat. Rev. Cancer, 2, 133–142.PubMedCrossRefGoogle Scholar
  112. 112.
    Clark, E. A., Golub, T. R., Lander, E. S., and Hynes, R. O. (2000) Nature, 406, 532–535.PubMedCrossRefGoogle Scholar
  113. 113.
    Itoh, K., Yoshioka, K., Akedo, H., Uehata, M., Ishizaki, T., and Narumiya, S. (1999) Nature Med., 5, 221–225.PubMedCrossRefGoogle Scholar
  114. 114.
    Kaneko, K., Satoh, K., Masamune, A., Satoh, A., and Shimosegawa, T. (2002) Pancreas, 24, 34–41.PubMedCrossRefGoogle Scholar
  115. 115.
    Matsui, T., Maeda, M., Doi, Y., Yonemura, S., Amano, M., Kaibuchi, K., Tsukita, S., and Tsukita, S. (1998) J. Cell Biol., 140, 647–657.PubMedCrossRefGoogle Scholar
  116. 116.
    Akisawa, N., Nishimori, I., Iwamura, T., Onishi, S., and Hollingsworth, M. A. (1999) Biochem. Biophys. Res. Commun., 258, 395–400.PubMedCrossRefGoogle Scholar
  117. 117.
    Engers, R., Springer, E., Michiels, F., Collard, J. G., and Gabbert, H. E. (2001) J. Biol. Chem., 276, 41889–41897.PubMedCrossRefGoogle Scholar
  118. 118.
    Zhuge, Y., and Xu, J. (2001) J. Biol. Chem., 276, 16248–16256.PubMedGoogle Scholar
  119. 119.
    Sahai, E., and Marshall, C. J. (2003) Nat. Cell Biol., 5, 711–719.PubMedCrossRefGoogle Scholar
  120. 120.
    Worthylake, R. A., Lemoine, S., Watson, J. M., and Burridge, K. (2001) J. Cell Biol., 154, 147–160.PubMedCrossRefGoogle Scholar
  121. 121.
    McLean, G. W., Carragher, N. O., Avizienyte, E., Evans, J., Brunton, V. G., and Frame, M. C. (2005) Nat. Cancer Rev., 5, 505–515.CrossRefGoogle Scholar
  122. 122.
    Shi, Q., Hjelmeland, A. B., Keir, S. T., Song, L., Wickman, S., Jackson, D., Ohmori, O., Bigner, D. D., Friedman, H. S., and Rich, J. N. (2007) Mol. Carcinog., 6, 488–496.CrossRefGoogle Scholar
  123. 123.
    Slack-Davis, J. K., Martin, K. H., Tilghman, R. W., Iwanicki, M., Ung, E. J., Autry, C., Luzzio, M. J., Cooper, B., Kath, J. C., Roberts, W. G., and Parsons, J. T. (2007) J. Biol. Chem., 20, 14845–14852.CrossRefGoogle Scholar
  124. 124.
    Roberts, W. G., Ung, E., Whalen, P., Cooper, B., Hulford, C., Autry, C., Richter, D., Emerson, E., Lin, J., Kath, J., Coleman, K., Yao, L., Martinez-Alsina, L., Lorenzen, M., Berliner, M., Luzzio, M., Patel, N., Schmitt, E., and LaGreca, S. (2007) Proc. Annu. Meet. Am. Assoc. Cancer Res., 48, 1282.Google Scholar
  125. 125.
    Kawahara, E., Ohmori, O., Nonomura, K., Murakami, Y., Tomioka, D., Niwa, S., Meyer, T., Mestan, J., Honda, T., and Hatakeyama, S. (2006) J. Clin. Oncol., 24, 13163.Google Scholar
  126. 126.
    Siu, L. L., Burris, H. A., Mileshkin, L., Camidge, D. R., Rischin, D., Chen, E. X., Jones, S., Yin D., and Fingert, H. (2007) J. Clin. Oncol., 25, 3527.CrossRefGoogle Scholar
  127. 127.
    Moschos, S. J., Drogowski, L. M., Reppert, S. I., and Kirkwood, J. M. (2007) Oncology (Williston Park), 9, 13–20.Google Scholar

Copyright information

© MAIK Nauka 2008

Authors and Affiliations

  1. 1.Institute of Carcinogenesis, Blokhin Russian Cancer Research CenterRussian Academy of Medical SciencesMoscowRussia

Personalised recommendations