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Biochemistry (Moscow)

, Volume 73, Issue 13, pp 1453–1466 | Cite as

Intermediate vimentin filaments and their role in intracellular organelle distribution

  • A. A. MininEmail author
  • M. V. Moldaver
Review

Abstract

Intermediate filaments (IF) represent one of three main cytoskeletal structures in most animal cells. The human IF protein family includes about 70 members divided into five main groups. The characteristic feature of IF is that in various cells and tissues they are formed by proteins of different groups. Structures of all IF proteins follow a unique scheme: a central α-helical part is flanked at the N and C ends by positively charged polypeptide chains devoid of a clear secondary structure. The central part is highly conserved for all proteins in all animals, whereas the N and C termini strongly differ both in size and amino acid composition. This review covers the broad spectrum of recent investigations of IF structure and diverse functions. Special attention is paid to the regulatory mechanisms of IF functions, mainly to phosphorylation by different protein kinases whose role is well studied. The review gives examples of hereditary diseases associated with mutations of some IF proteins, which point to an important physiological role of these cytoskeletal structures.

Key words

intermediate filaments vimentin keratins cytoskeleton 

Abbreviations

ABD

actin-binding domain

Bcl-2

oncogene 2 of B-cell lymphoma

BPAG1

bullous pemphigoid antigen 1

CaMKII

Ca-calmodulin-sensitive protein kinase

cdc2

cell division cycle protein kinase

EPR

electron paramagnetic resonance

ER

endoplasmic reticulum

GFAP

glial filament acidic protein

GSK3

glycogen synthase kinase

IF

intermediate filaments

IFAP

intermediate filament-associated proteins

LAMP-2

lysosome-bound membrane protein

MBD

microtubule-binding domain

NF-L, NF-M, NF-H

light, medium, and heavy neurofilament proteins

PAK

protein kinase activated by p21 protein

PKA

protein kinase A

PKC

protein kinase C

SAXS

small-angle X-ray scattering

SUN, KASH

integral proteins of nuclear membrane

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References

  1. 1.
    Fuchs, E., and Weber, K. (1994) Annu. Rev. Biochem., 63, 345–382.PubMedGoogle Scholar
  2. 2.
    Kreplak, L., and Fudge, D. (2007) Bioessays, 29, 26–35.PubMedGoogle Scholar
  3. 3.
    Toivola, D. M., Tao, G. Z., Habtezion, A., Liao, J., and Omary, M. B. (2005) Trends Cell Biol., 15, 608–617.PubMedGoogle Scholar
  4. 4.
    Herrmann, H., and Aebi, U. (2000) Curr. Opin. Cell Biol., 12, 79–90.PubMedGoogle Scholar
  5. 5.
    Coulombe, P. A., and Wong, P. (2004) Nat. Cell Biol., 6, 699–706.PubMedGoogle Scholar
  6. 6.
    Hesse, M., Magin, T. M., and Weber, K. (2001) J. Cell Sci., 114, 2569–2575.PubMedGoogle Scholar
  7. 7.
    Moll, R., Franke, W. W., Schiller, D. L., Geiger, B., and Krepler, R. (1982) Cell, 31, 11–24.PubMedGoogle Scholar
  8. 8.
    Steinert, P. M., Idler, W. W., and Zimmerman, S. B. (1976) J. Mol. Biol., 108, 547–567.PubMedGoogle Scholar
  9. 9.
    Lazarides, E. (1982) Annu. Rev. Biochem., 51, 219–250.PubMedGoogle Scholar
  10. 10.
    Osborn, M. (1983) J. Invest. Dermatol., 81, 104s–109s.PubMedGoogle Scholar
  11. 11.
    Portier, M. M., de Nechaud, B., and Gros, F. (1983) Dev. Neurosci., 6, 335–344.PubMedGoogle Scholar
  12. 12.
    Monteiro, M. J., and Cleveland, D. W. (1989) J. Cell Biol., 108, 579–593.PubMedGoogle Scholar
  13. 13.
    Steinert, P. M., Idler, W. W., Cabral, F., Gottesman, M. M., and Goldman, R. D. (1981) Proc. Natl. Acad. Sci. USA, 78, 3692–3696.PubMedGoogle Scholar
  14. 14.
    Lewis, S. A., and Cowan, N. J. (1985) J. Cell Biol., 100, 843–850.PubMedGoogle Scholar
  15. 15.
    Pachter, J. S., and Liem, R. K. (1985) J. Cell Biol., 101, 1316–1322.PubMedGoogle Scholar
  16. 16.
    Levy, E., Liem, R. K., D’Eustachio, P., and Cowan, N. J. (1987) Eur. J. Biochem., 166, 71–77.PubMedGoogle Scholar
  17. 17.
    Gerace, L., and Burke, B. (1988) Annu. Rev. Cell Biol., 4, 335–374.PubMedGoogle Scholar
  18. 18.
    Perng, M. D., Zhang, Q., and Quinlan, R. A. (2007) Exp. Cell Res., 313, 2180–2188.PubMedGoogle Scholar
  19. 19.
    Herrmann, H., and Aebi, U. (2000) Curr. Opin. Cell Biol., 12, 79–90.PubMedGoogle Scholar
  20. 20.
    Herrmann, H., and Aebi, U. (2004) Annu. Rev. Biochem., 73, 749–789.PubMedGoogle Scholar
  21. 21.
    Styers, M. L., Salazar, G., Love, R., Peden, A. A., Kowalczyk, A. P., and Faundez, V. (2004) Mol. Biol. Cell, 15, 5369–5382.PubMedGoogle Scholar
  22. 22.
    Tang, H. L., Lung, H. L., Wu, K. C., Le, A. H., Tang, H. M., and Fung, M. C. (2007) Biochem. J., 410, 141–146.Google Scholar
  23. 23.
    Gao, Y., and Sztul, E. (2001) J. Cell Biol., 152, 877–894.PubMedGoogle Scholar
  24. 24.
    Styers, M. L., Kowalczyk, A. P., and Faundez, V. (2005) Traffic, 6, 359–365.PubMedGoogle Scholar
  25. 25.
    Herrmann, H., Bar, H., Kreplak, L., Strelkov, S. V., and Aebi, U. (2007) Nat. Rev. Mol. Cell Biol., 8, 562–573.PubMedGoogle Scholar
  26. 26.
    Steinert, P. M., Marekov, L. N., and Parry, D. A. (1993) J. Biol. Chem., 268, 24916–24925.PubMedGoogle Scholar
  27. 27.
    Herrmann, H., Strelkov, S. V., Feja, B., Rogers, K. R., Brettel, M., Lustig, A., Haner, M., Parry, D. A., Steinert, P. M., Burkhard, P., and Aebi, U. (2000) J. Mol. Biol., 298, 817–832.PubMedGoogle Scholar
  28. 28.
    Wu, K. C., Bryan, J. T., Morasso, M. I., Jang, S. I., Lee, J. H., Yang, J. M., Marekov, L. N., Parry, D. A., and Steinert, P. M. (2000) Mol. Biol. Cell, 11, 3539–3558.PubMedGoogle Scholar
  29. 29.
    Brown, J. H., Cohen, C., and Parry, D. A. (1996) Proteins, 26, 134–145.PubMedGoogle Scholar
  30. 30.
    Michalczyk, K., and Ziman, M. (2005) Histol. Histopathol., 20, 665–671.PubMedGoogle Scholar
  31. 31.
    Parry, D. A., Steven, A. C., and Steinert, P. M. (1985) Biochem. Biophys. Res. Commun., 127, 1012–1018.PubMedGoogle Scholar
  32. 32.
    Geisler, N., and Weber, K. (1982) EMBO J., 1, 1649–1656.PubMedGoogle Scholar
  33. 33.
    Phillips, G. N., Jr. (1992) Proteins, 14, 425–429.PubMedGoogle Scholar
  34. 34.
    Meng, J. J., Khan, S., and Ip, W. (1994) J. Biol. Chem., 269, 18679–18685.PubMedGoogle Scholar
  35. 35.
    Strelkov, S. V., Herrmann, H., Geisler, N., Wedig, T., Zimbelmann, R., Aebi, U., and Burkhard, P. (2002) EMBO J., 21, 1255–1266.PubMedGoogle Scholar
  36. 36.
    Herrmann, H., and Aebi, U. (1999) Cell Mol. Life Sci., 55, 1416–1431.PubMedGoogle Scholar
  37. 37.
    Letai, A., Coulombe, P. A., and Fuchs, E. (1992) J. Cell Biol., 116, 1181–1195.PubMedGoogle Scholar
  38. 38.
    Budamagunta, M. S., Hess, J. F., Fitzgerald, P. G., and Voss, J. C. (2007) Cell Biochem. Biophys., 48, 45–53.PubMedGoogle Scholar
  39. 39.
    Traub, P., Scherbarth, A., Wiegers, W., and Shoeman, R. L. (1992) J. Cell Sci., 101, 363–381.PubMedGoogle Scholar
  40. 40.
    Herrmann, H., Hofmann, I., and Franke, W. W. (1992) J. Mol. Biol., 223, 637–650.PubMedGoogle Scholar
  41. 41.
    Shoeman, R. L., Hartig, R., Berthel, M., and Traub, P. (2002) Exp. Cell Res., 279, 344–353.PubMedGoogle Scholar
  42. 42.
    Geisler, N., Hatzfeld, M., and Weber, K. (1989) Eur. J. Biochem., 183, 441–447.PubMedGoogle Scholar
  43. 43.
    Herrmann, H., Haner, M., Brettel, M., Muller, S. A., Goldie, K. N., Fedtke, B., Lustig, A., Franke, W. W., and Aebi, U. (1996) J. Mol. Biol., 264, 933–953.PubMedGoogle Scholar
  44. 44.
    Heitlinger, E., Peter, M., Haner, M., Lustig, A., Aebi, U., and Nigg, E. A. (1991) J. Cell Biol., 113, 485–495.PubMedGoogle Scholar
  45. 45.
    Geisler, N., Schunemann, J., and Weber, K. (1992) Eur. J. Biochem., 206, 841–852.PubMedGoogle Scholar
  46. 46.
    Geisler, N. (1993) FEBS Lett., 323, 63–67.PubMedGoogle Scholar
  47. 47.
    Svergun, D. I., and Koch, M. H. (2002) Curr. Opin. Struct. Biol., 12, 654–660.PubMedGoogle Scholar
  48. 48.
    Koch, M. H., Vachette, P., and Svergun, D. I. (2003) Q. Rev. Biophys., 36, 147–227.PubMedGoogle Scholar
  49. 49.
    Sokolova, A. V., Kreplak, L., Wedig, T., Mucke, N., Svergun, D. I., Herrmann, H., Aebi, U., and Strelkov, S. V. (2006) Proc. Natl. Acad. Sci. USA, 103, 16206–16211.PubMedGoogle Scholar
  50. 50.
    Soellner, P., Quinlan, R. A., and Franke, W. W. (1985) Proc. Natl. Acad. Sci. USA, 82, 7929–7933.PubMedGoogle Scholar
  51. 51.
    Herrmann, H., Haner, M., Brettel, M., Ku, N. O., and Aebi, U. (1999) J. Mol. Biol., 286, 1403–1420.PubMedGoogle Scholar
  52. 52.
    Helfand, B. T., Chang, L., and Goldman, R. D. (2004) J. Cell Sci., 117, 133–141.PubMedGoogle Scholar
  53. 53.
    Prahlad, V., Yoon, M., Moir, R. D., Vale, R. D., and Goldman, R. D. (1998) J. Cell Biol., 143, 159–170.PubMedGoogle Scholar
  54. 54.
    Yoon, M., Moir, R. D., Prahlad, V., and Goldman, R. D. (1998) J. Cell Biol., 143, 147–157.PubMedGoogle Scholar
  55. 55.
    Gyoeva, F. K., and Gelfand, V. I. (1991) Nature, 353, 445–448.PubMedGoogle Scholar
  56. 56.
    Helfand, B. T., Mikami, A., Vallee, R. B., and Goldman, R. D. (2002) J. Cell Biol., 157, 795–806.PubMedGoogle Scholar
  57. 57.
    Yoon, K. H., Yoon, M., Moir, R. D., Khuon, S., Flitney, F. W., and Goldman, R. D. (2001) J. Cell Biol., 153, 503–516.PubMedGoogle Scholar
  58. 58.
    Brown, A. (2000) Nat. Rev. Mol. Cell Biol., 1, 153–156.PubMedGoogle Scholar
  59. 59.
    Roy, S., Coffee, P., Smith, G., Liem, R. K., Brady, S. T., and Black, M. M. (2000) J. Neurosci., 20, 6849–6861.PubMedGoogle Scholar
  60. 60.
    Styers, M. L., Kowalczyk, A. P., and Faundez, V. (2005) Traffic, 6, 359–365.PubMedGoogle Scholar
  61. 61.
    Toivola, D. M., Tao, G. Z., Habtezion, A., Liao, J., and Omary, M. B. (2005) Trends Cell Biol., 15, 608–617.PubMedGoogle Scholar
  62. 62.
    Goldman, R. D., Chou, Y. H., Prahlad, V., and Yoon, M. (1999) FASEB J., 13,Suppl. 2, S261–265.PubMedGoogle Scholar
  63. 63.
    Svitkina, T. M., Verkhovsky, A. B., and Borisy, G. G. (1996) J. Cell Biol., 135, 991–1007.PubMedGoogle Scholar
  64. 64.
    Ruhrberg, C., and Watt, F. M. (1997) Curr. Opin. Genet. Dev., 7, 392–397.PubMedGoogle Scholar
  65. 65.
    Wiche, G. (1998) J. Cell Sci., 111, 2477–2486.PubMedGoogle Scholar
  66. 66.
    Hijikata, T., Murakami, T., Imamura, M., Fujimaki, N., and Ishikawa, H. (1999) J. Cell Sci., 112, 867–876.PubMedGoogle Scholar
  67. 67.
    Andra, K., Lassmann, H., Bittner, R., Shorny, S., Fassler, R., Propst, F., and Wiche, G. (1997) Genes Dev., 11, 3143–3156.PubMedGoogle Scholar
  68. 68.
    Andra, K., Nikolic, B., Stocher, M., Drenckhahn, D., and Wiche, G. (1998) Genes Dev., 12, 3442–3451.PubMedGoogle Scholar
  69. 69.
    Yang, Y., Bauer, C., Strasser, G., Wollman, R., Julien, J. P., and Fuchs, E. (1999) Cell, 98, 229–238.PubMedGoogle Scholar
  70. 70.
    Elliott, C. E., Becker, B., Oehler, S., Castanon, M. J., Hauptmann, R., and Wiche, G. (1997) Genomics, 42, 115–125.PubMedGoogle Scholar
  71. 71.
    Paulin, D., and Li, Z. (2004) Exp. Cell Res., 301, 1–7.PubMedGoogle Scholar
  72. 72.
    Milner, D. J., Mavroidis, M., Weisleder, N., and Capetanaki, Y. (2000) J. Cell Biol., 150, 1283–1298.PubMedGoogle Scholar
  73. 73.
    Nekrasova, O., Kulik, A., and Minin, A. (2007) Biochemistry (Membrane and Cell Biology), 1, 108–113.Google Scholar
  74. 74.
    Wagner, O. I., Lifshitz, J., Janmey, P. A., Linden, M., McIntosh, T. K., and Leterrier, J. F. (2003) J. Neurosci., 23, 9046–9058.PubMedGoogle Scholar
  75. 75.
    Brownlees, J., Ackerley, S., Grierson, A. J., Jacobsen, N. J., Shea, K., Anderton, B. H., Leigh, P. N., Shaw, C. E., and Miller, C. C. (2002) Hum. Mol. Genet., 11, 2837–2844.PubMedGoogle Scholar
  76. 76.
    Bonifas, J. M., Rothman, A. L., and Epstein, E. H., Jr. (1991) Science, 254, 1202–1205.PubMedGoogle Scholar
  77. 77.
    Gao, Y., and Sztul, E. (2001) J. Cell Biol., 152, 877–893.PubMedGoogle Scholar
  78. 78.
    Gao, Y. S., Vrielink, A., MacKenzie, R., and Sztul, E. (2002) Eur. J. Cell Biol., 81, 391–401.PubMedGoogle Scholar
  79. 79.
    Suzuki, T., Nakamoto, T., Ogawa, S., Seo, S., Matsumura, T., Tachibana, K., Morimoto, C., and Hirai, H. (2002) J. Biol. Chem., 277, 14933–14941.PubMedGoogle Scholar
  80. 80.
    Styers, M. L., Salazar, G., Love, R., Peden, A. A., Kowalczyk, A. P., and Faundez, V. (2004) Mol. Biol. Cell, 15, 5369–5382.PubMedGoogle Scholar
  81. 81.
    Shintani, T., and Klionsky, D. J. (2004) Science, 306, 990–995.PubMedGoogle Scholar
  82. 82.
    Blankson, H., Holten, T., Oksendal, A. N., and Jynge, P. (1995) Acta Radiol. Suppl., 399, 135–141.PubMedGoogle Scholar
  83. 83.
    Starr, D. A. (2007) Mol. Biosyst., 3, 583–589.PubMedGoogle Scholar
  84. 84.
    Sarria, A. J., Lieber, J. G., Nordeen, S. K., and Evans, R. M. (1994) J. Cell Sci., 107, 1593–1607.PubMedGoogle Scholar
  85. 85.
    Shah, S. B., Davis, J., Weisleder, N., Kostavassili, I., McCulloch, A. D., Ralston, E., Capetanaki, Y., and Lieber, R. L. (2004) Biophys. J., 86, 2993–3008.PubMedGoogle Scholar
  86. 86.
    Fuchs, E., Esteves, R. A., and Coulombe, P. A. (1992) Proc. Natl. Acad. Sci. USA, 89, 6906–6910.PubMedGoogle Scholar
  87. 87.
    Ralston, E., Lu, Z., Biscocho, N., Soumaka, E., Mavroidis, M., Prats, C., Lomo, T., Capetanaki, Y., and Ploug, T. (2006) J. Cell Physiol., 209, 874–882.PubMedGoogle Scholar
  88. 88.
    Wilhelmsen, K., Litjens, S. H., Kuikman, I., Tshimbalanga, N., Janssen, H., van den Bout, I., Raymond, K., and Sonnenberg, A. (2005) J. Cell Biol., 171, 799–810.PubMedGoogle Scholar
  89. 89.
    Schweitzer, S. C., and Evans, R. M. (1998) Subcell. Biochem., 31, 437–462.PubMedGoogle Scholar
  90. 90.
    Wang, C., JeBailey, L., and Ridgway, N. D. (2002) Biochem. J., 361, 461–472.PubMedGoogle Scholar
  91. 91.
    Ogawara, M., Inagaki, N., Tsujimura, K., Takai, Y., Sekimata, M., Ha, M. H., Imajoh-Ohmi, S., Hirai, S., Ohno, S., Sugiura, H., et al. (1995) J. Cell Biol., 131, 1055–1066.PubMedGoogle Scholar
  92. 92.
    Li, Q. F., Spinelli, A. M., Wang, R., Anfinogenova, Y., Singer, H. A., and Tang, D. D. (2006) J. Biol. Chem., 281, 34716–34724.PubMedGoogle Scholar
  93. 93.
    Eriksson, J. E., He, T., Trejo-Skalli, A. V., Harmala-Brasken, A. S., Hellman, J., Chou, Y. H., and Goldman, R. D. (2004) J. Cell Sci., 117, 919–932.PubMedGoogle Scholar
  94. 94.
    Eriksson, J. E., Opal, P., and Goldman, R. D. (1992) Curr. Opin. Cell Biol., 4, 99–104.PubMedGoogle Scholar
  95. 95.
    Ku, N. O., Liao, J., Chou, C. F., and Omary, M. B. (1996) Cancer Metastasis Rev., 15, 429–444.PubMedGoogle Scholar
  96. 96.
    Foisner, R., Traub, P., and Wiche, G. (1991) Proc. Natl. Acad. Sci. USA, 88, 3812–3816.PubMedGoogle Scholar
  97. 97.
    Liao, J., and Omary, M. B. (1996) J. Cell Biol., 133, 345–357.PubMedGoogle Scholar
  98. 98.
    Caulin, C., Ware, C. F., Magin, T. M., and Oshima, R. G. (2000) J. Cell Biol., 149, 17–22.PubMedGoogle Scholar
  99. 99.
    Feng, L., Zhou, X., Liao, J., and Omary, M. B. (1999) J. Cell Sci., 112, 2081–2090.PubMedGoogle Scholar
  100. 100.
    Giasson, B. I., and Mushynski, W. E. (1996) J. Biol. Chem., 271, 30404–30409.PubMedGoogle Scholar
  101. 101.
    Goto, H., Kosako, H., Tanabe, K., Yanagida, M., Sakurai, M., Amano, M., Kaibuchi, K., and Inagaki, M. (1998) J. Biol. Chem., 273, 11728–11736.PubMedGoogle Scholar
  102. 102.
    Sin, W. C., Chen, X. Q., Leung, T., and Lim, L. (1998) Mol. Cell Biol., 18, 6325–6339.PubMedGoogle Scholar
  103. 103.
    Inagaki, M., Nishi, Y., Nishizawa, K., Matsuyama, M., and Sato, C. (1987) Nature, 328, 649–652.PubMedGoogle Scholar
  104. 104.
    Chou, Y. H., Bischoff, J. R., Beach, D., and Goldman, R. D. (1990) Cell, 62, 1063–1071.PubMedGoogle Scholar
  105. 105.
    Chou, Y. H., Rosevear, E., and Goldman, R. D. (1989) Proc. Natl. Acad. Sci. USA, 86, 1885–1889.PubMedGoogle Scholar
  106. 106.
    Tsujimura, K., Tanaka, J., Ando, S., Matsuoka, Y., Kusubata, M., Sugiura, H., Yamauchi, T., and Inagaki, M. (1994) J. Biochem., 116, 426–434.PubMedGoogle Scholar
  107. 107.
    Takai, Y., Ogawara, M., Tomono, Y., Moritoh, C., Imajoh-Ohmi, S., Tsutsumi, O., Taketani, Y., and Inagaki, M. (1996) J. Cell Biol., 133, 141–149.PubMedGoogle Scholar
  108. 108.
    Ando, S., Tanabe, K., Gonda, Y., Sato, C., and Inagaki, M. (1989) Biochemistry, 28, 2974–2979.PubMedGoogle Scholar
  109. 109.
    Ando, S., Tokui, T., Yamauchi, T., Sugiura, H., Tanabe, K., and Inagaki, M. (1991) Biochem. Biophys. Res. Commun., 175, 955–962.PubMedGoogle Scholar
  110. 110.
    Kusubata, M., Tokui, T., Matsuoka, Y., Okumura, E., Tachibana, K., Hisanaga, S., Kishimoto, T., Yasuda, H., Kamijo, M., Ohba, Y., et al. (1992) J. Biol. Chem., 267, 20937–20942.PubMedGoogle Scholar
  111. 111.
    Chou, Y. H., Ngai, K. L., and Goldman, R. (1991) J. Biol. Chem., 266, 7325–7328.PubMedGoogle Scholar
  112. 112.
    Goto, H., Tanabe, K., Manser, E., Lim, L., Yasui, Y., and Inagaki, M. (2002) Genes Cells, 7, 91–97.PubMedGoogle Scholar
  113. 113.
    Nakamura, Y., Takeda, M., Aimoto, S., Hojo, H., Takao, T., Shimonishi, Y., Hariguchi, S., and Nishimura, T. (1992) J. Biol. Chem., 267, 23269–23274.PubMedGoogle Scholar
  114. 114.
    Inagaki, M., Gonda, Y., Nishizawa, K., Kitamura, S., Sato, C., Ando, S., Tanabe, K., Kikuchi, K., Tsuiki, S., and Nishi, Y. (1990) J. Biol. Chem., 265, 4722–4729.PubMedGoogle Scholar
  115. 115.
    Sekimata, M., Tsujimura, K., Tanaka, J., Takeuchi, Y., Inagaki, N., and Inagaki, M. (1996) J. Cell Biol., 132, 635–641.PubMedGoogle Scholar
  116. 116.
    Geisler, N., and Weber, K. (1988) EMBO J., 7, 15–20.PubMedGoogle Scholar
  117. 117.
    Kitamura, S., Ando, S., Shibata, M., Tanabe, K., Sato, C., and Inagaki, M. (1989) J. Biol. Chem., 264, 5674–5678.PubMedGoogle Scholar
  118. 118.
    Kusubata, M., Matsuoka, Y., Tsujimura, K., Ito, H., Ando, S., Kamijo, M., Yasuda, H., Ohba, Y., Okumura, E., Kishimoto, T., et al. (1993) Biochem. Biophys. Res. Commun., 190, 927–934.PubMedGoogle Scholar
  119. 119.
    Sihag, R. K., and Nixon, R. A. (1991) J. Biol. Chem., 266, 18861–18867.PubMedGoogle Scholar
  120. 120.
    Gonda, Y., Nishizawa, K., Ando, S., Kitamura, S., Minoura, Y., Nishi, Y., and Inagaki, M. (1990) Biochem. Biophys. Res. Commun., 167, 1316–1325.PubMedGoogle Scholar
  121. 121.
    Vallano, M. L., Buckholz, T. M., and DeLorenzo, R. J. (1985) Biochem. Biophys. Res. Commun., 130, 957–963.PubMedGoogle Scholar
  122. 122.
    Link, W. T., Dosemeci, A., Floyd, C. C., and Pant, H. C. (1993) Neurosci. Lett., 151, 89–93.PubMedGoogle Scholar
  123. 123.
    Guan, R. J., Khatra, B. S., and Cohlberg, J. A. (1991) J. Biol. Chem., 266, 8262–8267.PubMedGoogle Scholar
  124. 124.
    Hocevar, B. A., Burns, D. J., and Fields, A. P. (1993) J. Biol. Chem., 268, 7545–7552.PubMedGoogle Scholar
  125. 125.
    Lamb, N. J., Fernandez, A., Feramisco, J. R., and Welch, W. J. (1989) J. Cell Biol., 108, 2409–2422.PubMedGoogle Scholar
  126. 126.
    Eriksson, J. E., Brautigan, D. L., Vallee, R., Olmsted, J., Fujiki, H., and Goldman, R. D. (1992) Proc. Natl. Acad. Sci. USA, 89, 11093–11097.PubMedGoogle Scholar
  127. 127.
    Izawa, I., and Inagaki, M. (2006) Cancer Sci., 97, 167–174.PubMedGoogle Scholar
  128. 128.
    Kosako, H., Goto, H., Yanagida, M., Matsuzawa, K., Fujita, M., Tomono, Y., Okigaki, T., Odai, H., Kaibuchi, K., and Inagaki, M. (1999) Oncogene, 18, 2783–2788.PubMedGoogle Scholar
  129. 129.
    Goto, H., Yasui, Y., Kawajiri, A., Nigg, E. A., Terada, Y., Tatsuka, M., Nagata, K., and Inagaki, M. (2003) J. Biol. Chem., 278, 8526–8530.PubMedGoogle Scholar
  130. 130.
    Altmannsberger, M., Osborn, M., Holscher, A., Schauer, A., and Weber, K. (1981) Virchows Arch. B Cell Pathol. Incl. Mol. Pathol., 37, 277–284.PubMedGoogle Scholar
  131. 131.
    Holwell, T. A., Schweitzer, S. C., and Evans, R. M. (1997) J. Cell Sci., 110, 1947–1956.PubMedGoogle Scholar
  132. 132.
    Pekny, M., Leveen, P., Pekna, M., Eliasson, C., Berthold, C. H., Westermark, B., and Betsholtz, C. (1995) EMBO J., 14, 1590–1598.PubMedGoogle Scholar
  133. 133.
    Colucci-Guyon, E., Portier, M. M., Dunia, I., Paulin, D., Pournin, S., and Babinet, C. (1994) Cell, 79, 679–694.PubMedGoogle Scholar
  134. 134.
    Schiffers, P. M., Henrion, D., Boulanger, C. M., Colucci-Guyon, E., Langa-Vuves, F., van Essen, H., Fazzi, G. E., Levy, B. I., and De Mey, J. G. (2000) Arterioscler. Thromb. Vasc. Biol., 20, 611–616.PubMedGoogle Scholar
  135. 135.
    Terzi, F., Henrion, D., Colucci-Guyon, E., Federici, P., Babinet, C., Levy, B. I., Briand, P., and Friedlander, G. (1997) J. Clin. Invest., 100, 1520–1528.PubMedGoogle Scholar
  136. 136.
    Alberts, B., Brey, D., Lewis, J., Raff, M., Roberts, K., and Watson, J. D. (1993) Molecular Biology of Cell, Vol. 2 [Russian translation], 2nd Edn., Mir, Moscow.Google Scholar

Copyright information

© MAIK Nauka 2008

Authors and Affiliations

  1. 1.Institute of Protein ResearchRussian Academy of SciencesPushchino, Moscow RegionRussia
  2. 2.Engelhardt Institute of Molecular BiologyRussian Academy of SciencesMoscowRussia

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