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Biochemistry (Moscow)

, Volume 75, Issue 13, pp 1606–1627 | Cite as

Cross-linked nucleic acids: isolation, structure, and biological role

  • V. A. EfimovEmail author
  • S. V. Fedyunin
Review

Abstract

This review includes literature data on main types of reagents inducing covalent cross-links of nucleic acids. Reactivity of cross-linking agents, preferable sites for their binding, and methods for determination of location of cross-links in duplex are discussed. Biological responses of cells to cross-linking in nucleic acids, i.e. replication and transcription blocking, onset of repair processes, and apoptotic cell death are considered, as well as application of cross-linking reagents as medicinal drugs for solving molecular-biological problems.

Key words

nucleic acids cross-link cross-linking agent 

Abbreviations

N

any nucleotide

NA

nucleic acid

PNA

peptide-nucleic acids

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References

  1. 1.
    Rajski, S., and Williams, R. (1998) Chem. Rev., 98, 2723–2796.PubMedGoogle Scholar
  2. 2.
    Stone, M., Cho, Y., Huang, H., Kin, H., Kozekov, I., Kozekova, A., Wang, H., Minro, I., Lloyd, R., Harris, T., and Rizzo, C. (2008) Accounts Chem. Res., 41, 793–804.Google Scholar
  3. 3.
    Scharer, O. (2005) ChemBioChem., 6, 27–32.PubMedGoogle Scholar
  4. 4.
    Su, T. (2006) Annu Rev. Genet., 40, 187–208.PubMedGoogle Scholar
  5. 5.
    Dronkert, M., and Kanaar, R. (2001) Mutat. Res., 486, 217–247.PubMedGoogle Scholar
  6. 6.
    Lehoczky, P., McHugh, J., and Chovanec, M. (2007) FEMS Microbiol. Rev., 31, 109–133.PubMedGoogle Scholar
  7. 7.
    Lieberman, B. (2008) Curr. Med. Chem., 15, 360–367.PubMedGoogle Scholar
  8. 8.
    Noll, D., Mason, T., and Miller, P. (2006) Chem. Rev., 106, 277–301.PubMedGoogle Scholar
  9. 9.
    Lushnikov, E. F., and Abrosimov, A. Yu. (2001) Cell Death (Apoptosis) [in Russian], Meditsina, Moscow, pp. 81–109.Google Scholar
  10. 10.
    Blank, M., and Shiloh, Y. (2007) Cell Cycle, 6, 686–695.PubMedGoogle Scholar
  11. 11.
    Strasser, A., O’Connor, L., and Dixit, V. (2000) Ann. Rev. Biochem., 69, 217–245.PubMedGoogle Scholar
  12. 12.
    Roos, W., and Kaina, B. (2006) Trends Mol. Med., 12, 440–450.PubMedGoogle Scholar
  13. 13.
    Gordeeva, A. V., Labas, Yu. A., and Zvyagilskaya, R. A. (2004) Biochemistry (Moscow), 69, 1055–1066.Google Scholar
  14. 14.
    Antsipovich, S. I., and Oretskaya, T. S. (1998) Uspekhi Khim., 67, 274–393.Google Scholar
  15. 15.
    Brookers, P. (1990) Mutat. Res., 233, 3–14.Google Scholar
  16. 16.
    Gilman, A., and Phillips, F. S. (1946) Science, 103, 409–411.Google Scholar
  17. 17.
    Ward, K. (1935) J. Am. Chem. Soc., 57, 914–916.Google Scholar
  18. 18.
    Rink, S., Solomon, M., Taylor, M., Rajur, S., McLaughlin, L., and Hopkins, P. (1993) J. Am. Chem. Soc., 115, 2551–2557.Google Scholar
  19. 19.
    White, I., Suzanger, M., Mattocks, A., Bailey, E., Farmer, P., and Connors, T. (1989) Carcinogenesis, 10, 2113–2118.PubMedGoogle Scholar
  20. 20.
    Duan, J., Jiao, H., Kaizerman, J., Stanton, T., Evans, J., Lan, L., Lorente, G., Banica, M., Jung, D., Wang, J., Ma, H., Li, X., Yang, Z., Hoffman, R., Ammons, W., Hart, C., and Matteucci, M. (2008) J. Med. Chem., 51, 2412–2420.PubMedGoogle Scholar
  21. 21.
    Parker, L., Lacy, S., Farrugia, L., Evans, C., Robins, D., O’Hare, C., Hartley, J., Jaffar, M., and Stratford, I. (2004) J. Med. Chem., 47, 5683–5689.PubMedGoogle Scholar
  22. 22.
    Kapuriya, N., Kapuriya, K., Dong, H., Zhang, X., Chou, T., Chen, Y., Lee, T., Lee, W., Tsai, T., Naliapara, Y., and Su, T. (2009) Bioorg. Med. Chem., 17, 1264–1275.PubMedGoogle Scholar
  23. 23.
    Baguley, B. (1991) Anti-Cancer Drug Design, 6, 1–35.PubMedGoogle Scholar
  24. 24.
    Chen, C., Lin, Y., Zhang, X., Chou, T., Tsai, T., Kapuriya, N., Kakadiya, R., and Su, T. (2009) Europ. J. Med. Chem., 44, 3056–3059.Google Scholar
  25. 25.
    Hendry, J., Rose, F., Homer, R., and Roades, A. (1948) Br. J. Pharmacol., 6, 235–255.Google Scholar
  26. 26.
    Millard, J., and White, M. (1993) Biochemistry, 32, 2120–2124.PubMedGoogle Scholar
  27. 27.
    Millard, J., Hanly, T., Murphy, K., and Tretyakova, N. (2006) Chem. Res. Toxicol., 19, 16–19.PubMedGoogle Scholar
  28. 28.
    LePla, R., Landreau, C., Shipman, M., Hartley, J., and Jones, G. (2005) Bioorg. Med. Chem. Lett., 15, 2861–2864.PubMedGoogle Scholar
  29. 29.
    Finerty, M., Bingham, J., Hartley, J., and Shipman, M. (2009) Tetrahedron Lett., 50, 3648–3650.Google Scholar
  30. 30.
    Coley, H. (1997) Gen. Pharmac., 28, 177–182.Google Scholar
  31. 31.
    Jackson, C., Crabb, T., Gibson, M., Godfrey, R., Saunders, R., and Thurston, D. (1991) J. Pharm. Sci., 80, 245–251.PubMedGoogle Scholar
  32. 32.
    Jackson, C., Hartley, J., Jenkins, T., Godfrey, R., Saunders, R., and Thurston, D. (1991) Biochem. Pharmacol., 42, 2091–2097.PubMedGoogle Scholar
  33. 33.
    Coley, H., Brooks, N., Phillips, D., Hewer, A., Jenkins, T., Jarman, M., and Judson, I. (1995) Biochem. Pharmac., 49, 1203–1212.Google Scholar
  34. 34.
    Song, Y., Wang, P., Wu, J., Zhou, X., Zhang, X., Weng, L., Cao, X., and Liang, F. (2006) Bioorg. Med. Chem. Lett., 16, 1660–1664.PubMedGoogle Scholar
  35. 35.
    Weng, X., Ren, L., Weng, L., Huang, J., Zhu, S., Zhou, X., and Weng, L. (2007) Angew. Chem. Int. Ed., 46, 8020–8023.Google Scholar
  36. 36.
    Song, Z., Weng, X., Weng, L., Huang, J., Wang, X., Bai, M., Zhou, Y., Yang, G., and Zhou, X. (2008) Chemistry, 14, 5751–5754.PubMedGoogle Scholar
  37. 37.
    Ware, D., Wilson, W., Denny, W., and Rickard, C. (1991) J. Chem. Soc. Chem. Commun., 1171–1173.Google Scholar
  38. 38.
    Dunham, S., Chifotides, H., Mikulski, S., Burr, A., and Dunbar, K. (2005) Biochemistry, 44, 996–1003.PubMedGoogle Scholar
  39. 39.
    Malinge, J., Perez, C., and Leng, M. (1994) Nucleic Acids Res., 22, 3834–3839.PubMedGoogle Scholar
  40. 40.
    Huang, H., Zhu, L., Reid, B., Drobny, G., and Hopkins, P. (1995) Science, 270, 1842–1845.PubMedGoogle Scholar
  41. 41.
    Jung, Y., and Lippard, S. (2007) Chem. Rev., 107, 1387–1407.PubMedGoogle Scholar
  42. 42.
    Heringova, P., Woods, J., Mackay, F., Kasparkova, J., Sadler, P., and Brabec, V. (2006) J. Med. Chem., 49, 7792–7798.PubMedGoogle Scholar
  43. 43.
    Chopard, C., Lenoir, C., Rizzato, S., Vidal, M., Arpalahti, J., Gabison, L., Albinati, A., Garbay, C., and Kozelka, J. (2008) Inorg. Chem., 47, 9701–9705.PubMedGoogle Scholar
  44. 44.
    Qu, Y., Scarsdale, N., Tran, M., and Farrell, N. (2004) J. Inorg. Biochem., 98, 1585–1590.PubMedGoogle Scholar
  45. 45.
    Ciniino, G., Gamper, H., Isaacs, S., and Hearst, J. (1985) Ann. Rev. Biochem., 54, 1151–1193.Google Scholar
  46. 46.
    Hwang, G., Kim, J., and Choi, B. (1996) Biochem. Biophys. Res. Commun., 219, 191–197.PubMedGoogle Scholar
  47. 47.
    Via, L., Gonzalez-Gomez, J., Perez-Montoto, L., Santana, L., Uriarte, E., Marciani, S., Gia, M., and Gia, O. (2009) Bioorg. Med. Chem. Lett., 19, 2874–2876.PubMedGoogle Scholar
  48. 48.
    Hata, T., Sano, Y., Sugawara, R., Matsumae, A., Kanamori, K., Shima, T., and Hoshi, T. (1956) J. Antibiot. Ser. A, 9, 141–146.Google Scholar
  49. 49.
    Wakagi, S., Marumo, H., Tomoka, K., Shimizu, G., Kata, E., Kamada, H., Kudo, S., and Fugimoto, Y. (1958) Antibiot. Chemother., 8, 228–238.Google Scholar
  50. 50.
    Webb, J., Cosulich, D., Mowat, J., Patrick, J., Broscha, R., Meyer, W., Williams, R., Wolf, C., Fulmor, W., and Pidacks, C. (1962) J. Am. Chem. Soc., 84, 3185–3187.Google Scholar
  51. 51.
    Danishefsky, S., and Schkeryantz, J. (1995) Synlett., 475–490.Google Scholar
  52. 52.
    Tomasz, M., Lifman, R., Chowdary, D., Pawlak, J., Verdine, G., and Nakanishi, K. (1987) Science, 235, 1204–1208.PubMedGoogle Scholar
  53. 53.
    Rink, S., Lipman, R., Alley, S., Hopkins, P., and Tomasz, M. (1996) Chem. Res. Toxicol., 9, 382–389.PubMedGoogle Scholar
  54. 54.
    Norman, D., Live, D., Sastry, M., Lipman, R., Hingerty, B., Tomasz, M., Broyde, S., and Patel, D. (1990) Biochemistry, 29, 2861–2875.PubMedGoogle Scholar
  55. 55.
    Adikesavan, A., and Jaiswal, A. (2007) Mol. Cancer Ther., 6, 2719–2727.PubMedGoogle Scholar
  56. 56.
    He, Q., Maruenda, H., and Tomasz, M. (1994) J. Am. Chem. Soc., 116, 9349–9350.Google Scholar
  57. 57.
    Manuel, M. (2009) Chem. Res. Toxicol., 22, 1663–1668.Google Scholar
  58. 58.
    Paz, M., Kumar, S., Glover, M., Waring, M., and Tomasz, M. (2004) J. Med. Chem., 47, 3308–3319.PubMedGoogle Scholar
  59. 59.
    Na, Y., Li, V., Nakanishi, Y., Bastow, K., and Kohn, H. (2001) J. Med. Chem., 44, 3453–3462.PubMedGoogle Scholar
  60. 60.
    Boger, D., and Paianki, S. (1992) J. Am. Chem. Soc., 114, 9318–3927.Google Scholar
  61. 61.
    Hadjivassileva, T., Stapleton, P., Thurston, D., and Taylor, P. (2007) Int. J. Antimic. Agents, 29, 672–678.Google Scholar
  62. 62.
    Brockmann, H., and Bauer, K. (1950) Naturwissen Schaften, 37, 492–497.Google Scholar
  63. 63.
    Wang, A., Ughetto, G., Quigley, G., and Rich, A. (1987) Biochemistry, 26, 1152–1163.PubMedGoogle Scholar
  64. 64.
    Gao, Y., Liaw, Y., Li, Y., van der Marel, G., van Boom, J., and Wang, A. (1991) Proc. Natl. Acad. Sci. USA, 88, 4845–4849.PubMedGoogle Scholar
  65. 65.
    Leng, F., Savkur, R., Fokt, I., Przewloka, T., Priebe, W., and Chaires, J. (1996) J. Am. Chem. Soc., 118, 4731–4738.Google Scholar
  66. 66.
    Taatjes, D., Gaudiano, G., Resing, K., and Koch, T. (1997) J. Med. Chem., 40, 1276–1286.PubMedGoogle Scholar
  67. 67.
    Kato, S., Burke, P., Fenick, D., Taatjes, D., Bierbaum, V., and Koch, T. (2000) Chem. Res. Toxicol., 13, 509–516.PubMedGoogle Scholar
  68. 68.
    Taatjea, D., Gaudiano, G., and Koch, T. (1997) Chem. Res. Toxicol., 10, 953–961.Google Scholar
  69. 69.
    Zhang, H., Gao, Y., van der Marel, G., van Boom, J., and Wang, A. (1993) J. Biol. Chem., 268, 10095–10101.PubMedGoogle Scholar
  70. 70.
    Fox, K., Webster, R., Phelps, R., Fokt, I., and Priebe, W. (2004) Eur. J. Biochem., 271, 3556–3566.PubMedGoogle Scholar
  71. 71.
    Portugal, J., Cashman, D., Trent, J., Ferrer-Miralies, N., Przewloka, T., Fokt, I., Priebe, W., and Chaires, J. (2005) J. Med. Chem., 48, 8209–8219.PubMedGoogle Scholar
  72. 72.
    Fenick, D., Taatjes, D., and Koch, T. (1997) J. Med. Chem., 40, 2452–2461.PubMedGoogle Scholar
  73. 73.
    Taatjes, D., Fenick, D., and Koch, T. (1998) J. Med. Chem., 41, 1306–1314.PubMedGoogle Scholar
  74. 74.
    Koch, T., Barthel, B., Kalet, B., Rudnicki, D., Post, G., and Burkhart, D. (2008) Top. Curr. Chem., 283, 141–170.Google Scholar
  75. 75.
    Caulfield, J., Wishnok, J., and Tannenbaum, S. (2003) Chem. Res. Toxicol., 16, 571–574.PubMedGoogle Scholar
  76. 76.
    Jackson, C., Hartley, J., Jenkins, T., Godfrey, R., Saunders, R., and Thurston, D. (1991) Biochem. Pharmacol., 42, 2091–2097.PubMedGoogle Scholar
  77. 77.
    Edfeldt, N., Harwood, E., Sigurdsson, S., Hopkins, P., and Reid, B. (2004) Nucleic Acids Res., 32, 2785–2794.PubMedGoogle Scholar
  78. 78.
    Edfeldt, N., Harwood, E., Sigurdsson, S., Hopkins, P., and Reid, B. (2004) Nucleic Acids Res., 32, 2795–2801.PubMedGoogle Scholar
  79. 79.
    Swenson, M., Paranawithana, S., Miller, P., and Kielkopf, C. (2007) Biochemistry, 46, 4545–4553.PubMedGoogle Scholar
  80. 80.
    Diakos, C., Messerle, B., del Socorro Murdoch, P., Parkinson, J., Sadler, P., Fenton, R., and Hambley, T. (2009) Inorg. Chem., 48, 3047–3056.PubMedGoogle Scholar
  81. 81.
    Candy Chen, H., and Chen, Y. (2009) Chem. Res. Toxicol., 22, 1334–1341.Google Scholar
  82. 82.
    Kozlov, I. A., Ivanovskaya, M. G., Kubareva, E. A., and Volkov, E. M. (1996) Mol. Biol. (Moscow), 30, 503.Google Scholar
  83. 83.
    Noll, D., Noronha, A., Wilds, C., and Miller, P. (2004) Front. Biosci., 6, 421–437.Google Scholar
  84. 84.
    Angelov, T., Guainazzi, A., and Scharer, O. (2009) Org. Lett., 11, 661–664.PubMedGoogle Scholar
  85. 85.
    Dooley, P., Tsarouhtsis, D., Korbel, G., Nechev, L., Shearer, J., Zegar, I., Harris, C., Stone, M., and Harris, T. (2001) J. Am. Chem. Soc., 123, 1730–1739.PubMedGoogle Scholar
  86. 86.
    Wilds, J., Booth, J., and Noronha, A. (2006) Tetrahedron Lett., 47, 9125–9128.Google Scholar
  87. 87.
    Colb, H., Finn, M., and Sharpless, K. (2001) Angew. Chem., 113, 2056–2075.Google Scholar
  88. 88.
    Humenik, M., Huang, Y. W., Wang, Y. R., and Sprinzl, M. (2007) ChemBioChem., 8, 1103–1106.PubMedGoogle Scholar
  89. 89.
    Rozkiewicz, D., Gierlich, J., Burley, G., Gutsmiedl, K., Garell, T., Ravoo, B., and Reinhoudt, D. (2007) ChemBioChem., 8, 1997–2002.PubMedGoogle Scholar
  90. 90.
    Seela, F., and Sirivolu, V. (2007) Helv. Chim. Acta, 90, 535–552.Google Scholar
  91. 91.
    Zocalka, P., El-Sagheer, A., and Brown, T. (2008) ChemBioChem., 9, 1280–1285.Google Scholar
  92. 92.
    Efimov, V. A., Aralov, A. V., Fedyunin, S. V., Klykov, V. N., and Chakhmakhcheva, O. G. (2009) Bioorg. Chem. (Moscow), 35, 270–273.Google Scholar
  93. 93.
    Gates, K. (2009) Chem. Res. Toxicol., 22, 1747–1760.PubMedGoogle Scholar
  94. 94.
    Shrivastav, M., de Haro, L., and Nickoloff, J. (2008) Cell Res., 18, 134–147.PubMedGoogle Scholar
  95. 95.
    Peng, X., Ghosh, A., van Houten, B., and Greenberg, M. (2010) Biochemistry, 49, 11–19.PubMedGoogle Scholar
  96. 96.
    Skladanowski, A., Bozko, P., and Sabisz, M. (2009) Chem. Rev., 109, 2951–2973.PubMedGoogle Scholar
  97. 97.
    Millau, J., Bastien, N., and Drouin, R. (2009) Mutat. Res., 681, 118–133.PubMedGoogle Scholar
  98. 98.
    Likhacheva, A. S., Rogachev, V. A., Nikolin, V. P., Popova, N. A., Shilov, A. G., Sebeleva, T. E., Strunkin, D. N., Chernykh, E. R., Gelfgat, E. L., Bogachev, S. S., and Shurdov, M. A. (2008) Vestnik VOGiS, 12, 426–473.Google Scholar
  99. 99.
    Konora, J. (1988) Biochem. Pharmacol., 37, 2303–2309.Google Scholar
  100. 100.
    Bernstein, C., Bernstein, H., Payne, C., and Gareval, H. (2002) Mutat. Res., 511, 145–178.PubMedGoogle Scholar
  101. 101.
    Kaina, B., Christmann, M., Naumann, S., and Roos, W. (2007) DNA Repair, 6, 1079–1099.PubMedGoogle Scholar
  102. 102.
    Reardon, J., and Sancar, A. (2005) Progr. Nucleic Acid Res. Mol. Biol., 79, 183–235.Google Scholar
  103. 103.
    Verhage, R., Zeeman, A., Degroot, N., Gleig, F., Bang, D., van de Putte, P., and Brouwer, J. (1994) Mol Cell Biol., 14, 6135–6142.PubMedGoogle Scholar
  104. 104.
    Shrivastav, M., de Haro, L., and Nickoloff, J. (2008) Cell Res., 18, 134–147.PubMedGoogle Scholar
  105. 105.
    Ohnishi, T., Mori, E., and Takahashi, A. (2009) Mutat. Res., 669, 8–12.PubMedGoogle Scholar
  106. 106.
    Burma, S., Chen, B., and Chen, D. (2006) DNA Repair, 5, 1042–1048.PubMedGoogle Scholar
  107. 107.
    Truglio, J., Croteau, D., van Houten, B., and Kisker, C. (2006) Chem. Rev., 106, 233–252.PubMedGoogle Scholar
  108. 108.
    Berardini, M., Foster, P., and Loechler, E. (1999) J. Bacteriol., 181, 2878–2882.PubMedGoogle Scholar
  109. 109.
    Kroghand, B., and Symington, L. (2004) Annu. Rev. Genet., 38, 233–271.Google Scholar
  110. 110.
    Essers, J., Theil, A., Baldeyron, C., van Cappellen, W., Houtsmuller, A., Kanaar, and Vermeulen, R. (2005) Mol. Cell. Biol., 9350–9359.Google Scholar
  111. 111.
    Henriques, J., and Moustacchi, E. (1980) Genetics, 95, 273–288.PubMedGoogle Scholar
  112. 112.
    Brendel, M., Bonatto, D., Strauss, M., Revers, L., Pungartnik, C., Saffi, J., and Henriques, J. (2003) Mutat. Res., 544, 179–193.PubMedGoogle Scholar
  113. 113.
    Clingen, P., Wu, J., Miller, J., Mistry, N., Chin, F., Wynne, P., Prise, K., and Hartley, J. (2008) Biochem. Pharmacol., 76, 19–27.PubMedGoogle Scholar
  114. 114.
    Rigu, G., and Robert, B. (2007) Curr. Med. Chem., 14, 503–517.Google Scholar
  115. 115.
    Bergstralh, D., and Sekelsky, J. (2008) Trends Genet., 24, 70–76.PubMedGoogle Scholar
  116. 116.
    Minko, I., Harbut, M., Kozekov, I., Kozekova, A., Jakobs, P., Olson, S., Moses, R., Harris, T., Rizzo, C., and Lloyd, R. (2008) J. Biol. Chem., 283, 17075–17082.PubMedGoogle Scholar
  117. 117.
    Woodgate, R. (1999) Genes Dev., 13, 2191–2195.PubMedGoogle Scholar
  118. 118.
    Zietlow, L., Smith, L., Bessho, M., and Bessho, T. (2009) Biochemistry, 48, 11817–11824.PubMedGoogle Scholar
  119. 119.
    De Winter, J., and Joenje, H. (2009) Mutat. Res., 668, 11–19.PubMedGoogle Scholar
  120. 120.
    Alpi, A., Langevin, F., Mosedale, G., Machida, Y., Dutta, A., and Patel, K. (2007) Mol. Cell Biol., 27, 8421–8430.PubMedGoogle Scholar
  121. 121.
    Kim, J., Kee, Y., Gurtan, A., and Andrea, A. (2008) Blood, 111, 5215–5222.PubMedGoogle Scholar
  122. 122.
    Smeaton, M., Hlavin, E., Mason, T., Noronha, A., Wilds, C., and Miller, P. (2008) Biochemistry, 47, 9920–9930.PubMedGoogle Scholar
  123. 123.
    Smeaton, M., Hlavin, E., Noronha, A., and Murphy, S. (2009) Chem. Res. Toxicol., 22, 1285–1297.PubMedGoogle Scholar
  124. 124.
    Ljungman, M. (2009) Chem. Rev., 109, 2929–2950.PubMedGoogle Scholar
  125. 125.
    Powell, S., and Bindra, R. (2009) DNA Repair, 8, 1153–1165.PubMedGoogle Scholar
  126. 126.
    Zhu, Y., Hu, J., Hu, Y., and Liu, W. (2009) Cancer Treatment Rev., 35, 590–596.Google Scholar
  127. 127.
    Mashkovsky, M. D. (1998) Officinal Drugs (Manual for Physicians) [in Russian], Pt. 2, Meditsina, Moscow, pp. 288–290.Google Scholar
  128. 128.
    Brosh, R., and Bohr, V. (2007) Nucleic Acids Res., 35, 7527–7544.PubMedGoogle Scholar
  129. 129.
    Feuerhahn, S., and Egly, J. (2008) Trends Genet., 24, 467–474.PubMedGoogle Scholar
  130. 130.
    Nagy, Z., and Soutoglou, E. (2009) Trends Cell Biol., 19, 617–629.PubMedGoogle Scholar
  131. 131.
    Ben-Yehoyada, M., Wang, L., Kozekov, I., Rizzo, C., Gottesman, M., and Gautier, J. (2009) Molecular Cell, 35, 704–715.PubMedGoogle Scholar
  132. 132.
    Lippincott-Schwartz, J., Snapp, E., and Kenworthy, A. (2001) Nat. Rev. Mol. Cell Biol., 2, 444–456.PubMedGoogle Scholar
  133. 133.
    Shav-Tal, Y., Singer, R., and Darzacq, X. (2004) Nat. Rev. Mol. Cell Biol., 5, 855–861.PubMedGoogle Scholar
  134. 134.
    Piston, D., and Kremers, G. (2007) Trends Biochem. Sci., 32, 407–414.PubMedGoogle Scholar
  135. 135.
    Huang, B., Bates, M., and Zhuang, X. (2009) Annu. Rev. Biochem., 78, 993–1016.PubMedGoogle Scholar
  136. 136.
    Silva, L. (2005) Curr. Protein Pept. Sci., 6, 387–395.PubMedGoogle Scholar
  137. 137.
    Moreno-Herrero, F., de Jager, M., Dekker, N., Kanaar, R., Wyman, C., and Dekker, C. (2005) Nature, 437, 440–443.PubMedGoogle Scholar
  138. 138.
    Recuero-Checa, M., Dore, A., Arias-Palomo, E., Rivera-Calzada, A., Scheres, S., Maman, J., Pearl, L., and Llorca, O. (2009) DNA Repair, 8, 1380–1389.PubMedGoogle Scholar
  139. 139.
    Oleinick, N., Morris, R., and Belichenko, I. (2002) Photochem. Photobiol. Sci., 1, 1–21.PubMedGoogle Scholar
  140. 140.
    Salvesen, G., and Dixit, V. (1999) Proc. Natl. Acad. Sci. USA, 96, 10964–10967.PubMedGoogle Scholar
  141. 141.
    Brozovic, A., Fritz, G., Christmann, M., Zisowsky, J., Jaehde, U., Osmak, M., and Kaina, B. (2004) Int. J. Cancer, 112, 974–985.PubMedGoogle Scholar
  142. 142.
    Lane, D. (1992) Nature, 358, 15–16.PubMedGoogle Scholar
  143. 143.
    Staehelin, M. (1958) Biochim. Biophys. Acta, 29, 410–417.PubMedGoogle Scholar
  144. 144.
    Staehelin, M. (1959) Biochim. Biophys. Acta, 31, 448–454.PubMedGoogle Scholar
  145. 145.
    Axelrod, V., Feldman, Y., Chuguev, I., and Bayev, A. (1969) Biochim. Biophys. Acta, 186, 33–45.PubMedGoogle Scholar
  146. 146.
    Juzumiene, D., Shapkina, T., Kirillov, S., and Wollenzien, P. (2001) Methods, 25, 333–343.PubMedGoogle Scholar
  147. 147.
    Nanda, K., and Wollenzien, P. (2004) Biochemistry, 43, 8923–8934.PubMedGoogle Scholar
  148. 148.
    Stewart, D., Thomas, S., Mayfield, C., and Miller, D. (2001) Nucleic Acids Res., 29, 4052–4061.PubMedGoogle Scholar
  149. 149.
    Higuchi, M., Sakamoto, T., Kobori, A., and Murakami, A. (2006) Nucleic Acids Symp. Ser., 50, 301–302.Google Scholar
  150. 150.
    Kean, J., Murakami, A., Blake, K., Cushman, C., and Miller, P. (1988) Biochemistry, 27, 9113–9121.PubMedGoogle Scholar
  151. 151.
    Thaden, J., and Miller, P. (1993) Bioconj. Chem., 4, 386–394.Google Scholar
  152. 152.
    Kim, Y., and Hong, I. (2008) Bioorg. Med. Chem. Lett., 18, 5054–5057.PubMedGoogle Scholar
  153. 153.
    Gantchev, T., Girouard, S., Dodd, D., Wojciechowski, F., Hudson, R., and Hunting, D. (2009) Biochemistry, 48, 7032–7044.PubMedGoogle Scholar
  154. 154.
    Bombard, S., Kozelka, J., Favre, A., and Chottard, J. (1998) Eur. J. Biochem., 252, 25–35.PubMedGoogle Scholar
  155. 155.
    Kazakov, S., and Altman, S. (1992) Proc. Natl. Acad. Sci. USA, 89, 7939–7943.PubMedGoogle Scholar

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© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  1. 1.Shemyakin and Ovchinnikov Institute of Bioorganic ChemistryRussian Academy of SciencesMoscowRussia

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