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The structure and mechanism of the action of type-IB DNA topoisomerases

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Abstract

DNA topoisomerases responsible for the superspiralization of genomic DNA participate in almost all vitally important cell processes, including replication, transcription, and recombination, and are essential for normal cell functioning. The present review summarizes published data for type-IB topoisomerases. The results concerning the thermodynamic, structural, and kinetic aspects of the functioning of topoisomerases and the peculiarities of the mechanisms of their action have been analyzed for the first time.

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Abbreviations

AA:

amino acid

dsDNA, ssDNA, and scDNA:

double-stranded, single-stranded, and supercoiled DNA

RSA:

roentgen structural analysis

topo:

DNA topoisomerase type I

References

  1. Wang, J.C., Annu. Rev. Biochem., 1996, vol. 65, pp. 635–692.

    Article  CAS  PubMed  Google Scholar 

  2. Wang, J.C., Nat. Rev. Mol. Cell Biol., 2002, vol. 3, pp. 430–440.

    Article  CAS  PubMed  Google Scholar 

  3. Shuman, S., Proc. Natl. Acad. Sci. USA, 1989, vol. 86, pp. 3489–3493.

    Article  CAS  PubMed  Google Scholar 

  4. Zhu, J. and Schiestl, R.H., Mol. Cell Biol., 1996, vol. 16, pp. 1805–1812.

    CAS  PubMed  Google Scholar 

  5. Trowbridge, P.W., Roy, R., and Simmons, D.T., Mol. Cell Biol., 1999, vol. 19, pp. 1686–1694.

    CAS  PubMed  Google Scholar 

  6. Pommier, Y., Pourquier, P., Fan, Y., and Strumberg, D., Biochim. Biophys. Acta, 1998, vol. 1400, pp. 83–105.

    CAS  PubMed  Google Scholar 

  7. Merino, A., Madden, K.R., Lane, W.S., Champoux, J.J., and Reinberg, D., Nature, 1993, vol. 365, pp. 227–232.

    Article  CAS  PubMed  Google Scholar 

  8. Kato, S. and Kikuchi, A., Nagoya J. Med. Sci., 1998, vol. 61, pp. 11–26.

    CAS  PubMed  Google Scholar 

  9. Champoux, J.J., Annu. Rev. Biochem., 2001, vol. 70, pp. 369–413.

    Article  CAS  PubMed  Google Scholar 

  10. Berger, J.M., Biochim. Biophys. Acta, 1998, vol. 1400, pp. 3–18.

    CAS  PubMed  Google Scholar 

  11. Gupta, M., Fujimori, A., and Pommier, Y., Biochim. Biophys. Acta, 1995, vol. 1262, pp. 1–14.

    PubMed  Google Scholar 

  12. Sharma, A. and Mondragon, A., Curr. Opin. Struct. Biol., 1995, vol. 5, pp. 39–47.

    Article  CAS  PubMed  Google Scholar 

  13. Forterre, P., Gribaldo, S., Gadelle, D., and Serre, M.C., Biochimie, 2007, vol. 89, pp. 427–446.

    Article  CAS  PubMed  Google Scholar 

  14. Cretaio, E., Pattarello, L., Fontebasso, Y., Benedetti, P., and Losasso, C., Ital. J. Biochem., 2007, vol. 56, pp. 91–102.

    CAS  PubMed  Google Scholar 

  15. Leppard, J.B. and Champoux, J.J., Chromosoma, 2005, vol. 114, pp. 75–85.

    Article  CAS  PubMed  Google Scholar 

  16. Schoeffler, A.J. and Berger, J.M., Q. Rev. Biophys., 2008, vol. 41, pp. 41–101.

    CAS  PubMed  Google Scholar 

  17. Singh, P. and Bhardwaj, A., Mini Rev. Med. Chem., 2008, vol. 8, pp. 388–398.

    Article  CAS  PubMed  Google Scholar 

  18. Wethington, S.L., Wright, J.D., and Herzog, T.J., Expert Rev. Anticancer Ther., 2008, vol. 8, pp. 819–831.

    Article  CAS  PubMed  Google Scholar 

  19. Feun, L. and Savaraj, N., Expert. Rev. Anticancer Ther., 2008, vol. 8, pp. 707–716.

    Article  CAS  PubMed  Google Scholar 

  20. Beretta, G.L., Perego, P., and Zunino, F., Expert. Opin. Ther. Targets, 2008, vol. 12, pp. 1243–1256.

    Article  CAS  PubMed  Google Scholar 

  21. Teicher, B.A., Biochem. Pharmacol., 2008, vol. 75, pp. 1262–1271.

    Article  CAS  PubMed  Google Scholar 

  22. Giles, G.I. and Sharma, R.P., Med. Chem., 2005, vol. 1, pp. 383–394.

    Article  CAS  PubMed  Google Scholar 

  23. Tse-Dinh, Y.C., Infect. Disord. Drug Targets, 2007, vol. 7, pp. 3–9.

    Article  CAS  PubMed  Google Scholar 

  24. Das, B.B., Ganguly, A., and Majumder, H.K., Adv. Exp. Med. Biol., 2008, vol. 625, pp. 103–115.

    Article  PubMed  Google Scholar 

  25. Slesarev, A.I., Stetter, K.O., Lake, J.A., Gellert, M., Krah, R., and Kozyavkin, S.A., Nature, 1993, vol. 364, pp. 735–737.

    Article  CAS  PubMed  Google Scholar 

  26. Stewart, L., Redinbo, M.R., Qiu, X., Hol, W.G., and Champoux, J.J., Science, 1998, vol. 279, pp. 1534–1541.

    Article  CAS  PubMed  Google Scholar 

  27. Yang, Z. and Champoux, J.J., J. Biol. Chem., 2001, vol. 276, pp. 677–685.

    Article  CAS  PubMed  Google Scholar 

  28. Sekiguchi, J. and Shuman, S., J. Biol. Chem., 1994, vol. 269, pp. 29760–29764.

    CAS  PubMed  Google Scholar 

  29. Shuman, S. and Prescott, J., J. Biol. Chem., 1990, vol. 265, pp. 17826–17836.

    CAS  PubMed  Google Scholar 

  30. Sekiguchi, J. and Shuman, S., J. Biol. Chem., 1994, vol. 269, pp. 31731–31734.

    CAS  PubMed  Google Scholar 

  31. Tian, L., Sayer, J.M., Jerina, D.M., and Shuman, S., J. Biol. Chem., 2004, vol. 279, pp. 39718–39726.

    Article  CAS  PubMed  Google Scholar 

  32. Liao, S., Mao, C., Birktoft, J.J., Shuman, S., and Seeman, N.C., Biochemistry, 2004, vol. 43, pp. 1520–1531.

    Article  CAS  PubMed  Google Scholar 

  33. Sekiguchi, J. and Shuman, S., J. Biol. Chem., 1995, vol. 270, pp. 11636–11645.

    Article  CAS  PubMed  Google Scholar 

  34. Cheng, C. and Shuman, S., J. Biol. Chem., 1998, vol. 273, pp. 11589–11595.

    Article  CAS  PubMed  Google Scholar 

  35. Sekiguchi, J. and Shuman, S., EMBO J., 1996, vol. 15, pp. 3448–3457.

    CAS  PubMed  Google Scholar 

  36. Wittschieben, J. and Shuman, S., Nucleic Acid Res., 1997, vol. 25, pp. 3001–3008.

    Article  CAS  PubMed  Google Scholar 

  37. Gao, R., Zhang, Y., Choudhury, A.K., Dedkova, L.M., and Hecht, S.M., J. Am. Chem. Soc., 2005, vol. 127, pp. 3321–3331.

    Article  CAS  PubMed  Google Scholar 

  38. Hanai, R. and Wang, J.C., Proc. Natl. Acad. Sci. USA, 1994, vol. 91, pp. 11904–11908.

    Article  CAS  PubMed  Google Scholar 

  39. Hwang, Y., Minkah, N., Perry, K., Van Duyne, G.D., and Bushman, F.D., J. Biol. Chem., 2006, vol. 281, pp. 38052–38060.

    Article  CAS  PubMed  Google Scholar 

  40. Tian, L., Claeboe, C.D., Hecht, S.M., and Shuman, S., Structure, 2005, vol. 13, pp. 513–520.

    Article  CAS  PubMed  Google Scholar 

  41. Stivers, J.T., Shuman, S., and Mildvan, A.S., Biochemistry, 1994, vol. 33, pp. 327–339.

    Article  CAS  PubMed  Google Scholar 

  42. Stivers, J.T., Shuman, S., and Mildvan, A.S., Biochemistry, 1994, vol. 33, pp. 15449–15458.

    Article  CAS  PubMed  Google Scholar 

  43. Morham, S.G. and Shuman, S., Genes Dev., 1990, vol. 4, pp. 515–524.

    Article  CAS  PubMed  Google Scholar 

  44. Klemperer, N. and Traktman, P., J. Biol. Chem., 1993, vol. 268, pp. 15887–15899.

    CAS  PubMed  Google Scholar 

  45. Stivers, J.T., Harris, T.K., and Mildvan, A.S., Biochemistry, 1997, vol. 36, pp. 5212–5222.

    Article  CAS  PubMed  Google Scholar 

  46. Wang, H.K., Morris-Natschke, S.L., and Lee, K.H., Med. Res. Rev., 1997, vol. 17, pp. 367–425.

    Article  CAS  PubMed  Google Scholar 

  47. Been, M.D. and Champoux, J.J., J. Mol. Biol., 1984, vol. 180, pp. 515–531.

    Article  CAS  PubMed  Google Scholar 

  48. Trask, D.K. and Muller, M.T., Nucleic Acid Res., 1983, vol. 11, pp. 2779–2800.

    Article  CAS  PubMed  Google Scholar 

  49. Andersen, A.H., Svejstrup, J.Q., and Westergaard, O., Adv. Pharmacol., 1994, vol. 29A, pp. 83–101.

    Article  CAS  PubMed  Google Scholar 

  50. Tanizawa, A., Kohn, K.W., and Pommier, Y., Nucleic Acid Res., 1993, vol. 21, pp. 5157–5166.

    Article  CAS  PubMed  Google Scholar 

  51. Shen, C.C. and Shen, C.K., J. Mol. Biol., 1990, vol. 212, pp. 67–78.

    Article  CAS  PubMed  Google Scholar 

  52. Camilloni, G., Caserta, M., Amadei, A., and Di Mauro, E., Biochim. Biophys. Acta, 1991, vol. 1129, pp. 73–82.

    CAS  PubMed  Google Scholar 

  53. Muller, M.T., Biochim. Biophys. Acta, 1985, vol. 824, pp. 263–267.

    CAS  PubMed  Google Scholar 

  54. Camilloni, G., Di Martino, E., Caserta, M., and Di Mauro, E., Nucleic Acid Res., 1988, vol. 16, pp. 7071–7085.

    Article  CAS  PubMed  Google Scholar 

  55. Camilloni, G., Di Martino, E., Di Mauro, E., and Caserta, M., Proc. Natl. Acad. Sci. USA, 1989, vol. 86, pp. 3080–3084.

    Article  CAS  PubMed  Google Scholar 

  56. Caserta, M., Amadei, A., Camilloni, G., and Di Mauro, E., Biochemistry, 1990, vol. 29, pp. 8152–8157.

    Article  CAS  PubMed  Google Scholar 

  57. Madden, K.R., Stewart, L., and Champoux, J.J., EMBO J., 1995, vol. 14, pp. 5399–5409.

    CAS  PubMed  Google Scholar 

  58. Depew, D.E. and Wang, J.C., Proc. Natl. Acad. Sci. USA, 1975, vol. 72, pp. 4275–4279.

    Article  CAS  PubMed  Google Scholar 

  59. Pulleyblank, D.E., Shure, M., Tang, D., Vinograd, J., and Vosberg, H.P., Proc. Natl. Acad. Sci. USA, 1975, vol. 72, pp. 4280–4284.

    Article  CAS  PubMed  Google Scholar 

  60. Krogh, S., Mortensen, U.H., Westergaard, O., and Bonven, B.J., Nucleic Acid Res., 1991, vol. 19, pp. 1235–1241.

    Article  CAS  PubMed  Google Scholar 

  61. Zechiedrich, E.L. and Osheroff, N., EMBO J., 1990, vol. 9, pp. 4555–4562.

    CAS  PubMed  Google Scholar 

  62. Edwards, K.A., Halligan, B.D., Davis, J.L., Nivera, N.L., and Liu, L.F., Nucleic Acid Res., 1982, vol. 10, pp. 2565–2576.

    Article  CAS  PubMed  Google Scholar 

  63. Been, M.D., Burgess, R.R., and Champoux, J.J., Nucleic Acid Res., 1984, vol. 12, pp. 3097–3114.

    Article  CAS  PubMed  Google Scholar 

  64. Bonven, B.J., Gocke, E., and Westergaard, O., Cell, 1985, vol. 41, pp. 541–551.

    Article  CAS  PubMed  Google Scholar 

  65. Christiansen, K., Bonven, B.J., and Westergaard, O., J. Mol. Biol., 1987, vol. 193, pp. 517–525.

    Article  CAS  PubMed  Google Scholar 

  66. Ness, P.J., Koller, T., and Thoma, F., J. Mol. Biol., 1988, vol. 200, pp. 127–139.

    Article  CAS  PubMed  Google Scholar 

  67. Thomsen, B., Mollerup, S., Bonven, B.J., Frank, R., Blocker, H., Nielsen, O.F., and Westergaard, O., EMBO J., 1987, vol. 6, pp. 1817–1823.

    CAS  PubMed  Google Scholar 

  68. Busk, H., Thomsen, B., Bonven, B.J., Kjeldsen, E., Nielsen, O.F., and Westergaard, O., Nature, 1987, vol. 327, pp. 638–640.

    Article  CAS  PubMed  Google Scholar 

  69. Stevnsner, T., Mortensen, U.H., Westergaard, O., and Bonven, B.J., J. Biol. Chem., 1989, vol. 264, pp. 10110–10113.

    CAS  PubMed  Google Scholar 

  70. Christiansen, K. and Westergaard, O., J. Biol. Chem., 1994, vol. 269, pp. 721–729.

    CAS  PubMed  Google Scholar 

  71. Svejstrup, J.Q., Christiansen, K., Andersen, A.H., Lund, K., and Westergaard, O., J. Biol. Chem., 1990, vol. 265, pp. 12529–12535.

    CAS  PubMed  Google Scholar 

  72. Andersen, A.H., Gocke, E., Bonven, B.J., Nielsen, O.F., and Westergaard, O., Nucleic Acid Res., 1985, vol. 13, pp. 1543–1557.

    Article  CAS  PubMed  Google Scholar 

  73. Jaxel, C., Capranico, G., Kerrigan, D., Kohn, K.W., and Pommier, Y., J. Biol. Chem., 1991, vol. 266, pp. 20418–20423.

    CAS  PubMed  Google Scholar 

  74. Christiansen, K., Svejstrup, A.B., Andersen, A.H., and Westergaard, O., J. Biol. Chem., 1993, vol. 268, pp. 9690–9701.

    CAS  PubMed  Google Scholar 

  75. Leteurtre, F., Kohlhagen, G., Fesen, M.R., Tanizawa, A., Kohn, K.W., and Pommier, Y., J. Biol. Chem., 1994, vol. 269, pp. 7893–7900.

    CAS  PubMed  Google Scholar 

  76. Oshchepkov, D.Yu., Bugreev, D.V., Vityaev, E.E., and Nevinsky, G.A., in Proceedings of the Third International Conference on BGRS. Novosibirsk, Russia, 2002, vol. 1, pp. 161–164.

    Google Scholar 

  77. Oshchepkov, D.Yu., Turnaev, I.I., and Vityaev, E.E., in Proceedings of the Third International Conference on BGRS. Novosibirsk, Russia, 2002, vol. 1, pp. 43–46.

    Google Scholar 

  78. Bugreev, D.V., Buneva, V.N., and Nevinskii, G.A., Mol. Biol., 2003, vol. 37, pp. 325–339.

    Article  CAS  Google Scholar 

  79. D’Arpa, P., Machlin, P.S., and Ratrie, H., 3rd Rothfield N.F., Cleveland D.W., Earnshaw W.C, Proc. Natl. Acad. Sci. USA, 1988, vol. 85, pp. 2543–2547.

    Article  PubMed  Google Scholar 

  80. Stewart, L., Ireton, G.C., and Champoux, J.J., J. Biol. Chem., 1996, vol. 271, pp. 7602–7608.

    Article  CAS  PubMed  Google Scholar 

  81. Alsner, J., Svejstrup, J.Q., Kjeldsen, E., Sorensen, B.S., and Westergaard, O., J. Biol. Chem., 1992, vol. 267, pp. 12408–12411.

    CAS  PubMed  Google Scholar 

  82. Bharti, A.K., Olson, M.O., Kufe, D.W., and Rubin, E.H., J. Biol. Chem., 1996, vol. 271, pp. 1993–1997.

    Article  CAS  PubMed  Google Scholar 

  83. Lisby, M., Olesen, J.R., Skouboe, C., Krogh, B.O., Straub, T., Boege, F., Velmurugan, S., Martensen, P.M., Andersen, A.H., Jayaram, M., Westergaard, O., and Knudsen, B.R., J. Biol. Chem., 2001, vol. 276, pp. 20220–20227.

    Article  CAS  PubMed  Google Scholar 

  84. Mo, Y.Y., Wang, C., and Beck, W.T., J. Biol. Chem., 2000, vol. 275, pp. 41107–41113.

    Article  CAS  PubMed  Google Scholar 

  85. Zhang, H., Barcelo, J.M., Lee, B., Kohlhagen, G., Zimonjic, D.B., Popescu, N.C., and Pommier, Y., Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 10608–10613.

    Article  CAS  PubMed  Google Scholar 

  86. Madden, K.R. and Champoux, J.J., Cancer Res., 1992, vol. 52, pp. 525–532.

    CAS  PubMed  Google Scholar 

  87. Gao, R., Zhang, Y., Dedkova, L., Choudhury, A.K., Rahier, N.J., and Hecht, S.M., Biochemistry, 2006, vol. 45, pp. 8402–8410.

    Article  CAS  PubMed  Google Scholar 

  88. Stewart, L., Ireton, G.C., and Champoux, J.J., J. Mol. Biol., 1997, vol. 269, pp. 355–372.

    Article  CAS  PubMed  Google Scholar 

  89. Redinbo, M.R., Stewart, L., Kuhn, P., Champoux, J.J., and Hol, W.G., Science, 1998, vol. 279, pp. 1504–1513.

    Article  CAS  PubMed  Google Scholar 

  90. Lue, N., Sharma, A., Mondragon, A., and Wang, J.C., Structure, 1995, vol. 3, pp. 1315–1322.

    Article  CAS  PubMed  Google Scholar 

  91. Klemm, J.D., Rould, M.A., Aurora, R., Herr, W., and Pabo, C.O., Cell, 1994, vol. 77, pp. 21–32.

    Article  CAS  PubMed  Google Scholar 

  92. Hickman, A.B., Waninger, S., Scocca, J.J., and Dyda, F., Cell, 1997, vol. 89, pp. 227–237.

    Article  CAS  PubMed  Google Scholar 

  93. Nevinskii, G.A., Mol. Biol., 1995, vol. 29, pp. 16–37.

    CAS  Google Scholar 

  94. Bugreev, D.V. and Nevinskii, G.A., Biokhimiya, 1999, vol. 64, pp. 291–305.

    Google Scholar 

  95. Bugreev, D.V., Vasyutina, E.L., Kolocheva, T.I., Buneva, V.N., Andoh, T., and Nevinsky, G.A., Biochimie, 1998, vol. 80, pp. 303–308.

    Article  CAS  PubMed  Google Scholar 

  96. Bugreev, D.V., Buneva, V.N., Sinitsyna, O.I., and Nevinsky, G.A., Bioorg. Khim., 2003, vol. 29, pp. 163–174 [Russ. J. Bioorg. Chem. (Engl. Transl.), 2003, vol. 29, pp. 143–153].

    CAS  PubMed  Google Scholar 

  97. Bugreev, D.V., Sinitsyna, O.I., Buneva, V.N., and Nevinsky, G.A., Bioorg. Khim., 2003, vol. 29, pp. 277–289 [Russ. J. Bioorg. Chem. (Engl. Transl.), 2003, vol. 29, pp. 249–261].

    CAS  PubMed  Google Scholar 

  98. Nevinsky, G.A., Bugreev, D.V., Buneva, V.N., Yasui, Y., Nishizawa, M., and Andoh, T., FEBS Lett., 1995, vol. 368, pp. 97–100.

    Article  CAS  PubMed  Google Scholar 

  99. Bugreev, D.V., Vasyutina, E.L., Buneva, V.N., Yasui, Y., Nishizawa, M., Andoh, T., and Nevinsky, G.A., FEBS Lett., 1997, vol. 407, pp. 18–20.

    Article  CAS  PubMed  Google Scholar 

  100. Redinbo, M.R., Champoux, J.J., and Hol, W.G., Biochemistry, 2000, vol. 39, pp. 6832–6840.

    Article  CAS  PubMed  Google Scholar 

  101. Stewart, L., Ireton, G.C., and Champoux, J.J., J. Biol. Chem., 1999, vol. 274, pp. 32950–32960.

    Article  CAS  PubMed  Google Scholar 

  102. Ireton, G.C., Stewart, L., Parker, L.H., and Champoux, J.J., J. Biol. Chem., 2000, vol. 275, pp. 25820–25830.

    Article  CAS  PubMed  Google Scholar 

  103. Levin, N.A., Bjornsti, M.A., and Fink, G.R., Genetics, 1993, vol. 133, pp. 799–814.

    CAS  PubMed  Google Scholar 

  104. Jensen, A.D. and Svejstrup, J.Q., Eur. J. Biochem., 1996, vol. 236, pp. 389–394.

    Article  CAS  PubMed  Google Scholar 

  105. Megonigal, M.D., Fertala, J., and Bjornsti, M.A., J. Biol. Chem., 1997, vol. 272, pp. 12801–12808.

    Article  CAS  PubMed  Google Scholar 

  106. Cheng, C., Wang, L.K., Sekiguchi, J., and Shuman, S., J. Biol. Chem., 1997, vol. 272, pp. 8263–8269.

    Article  CAS  PubMed  Google Scholar 

  107. Petersen, B.O. and Shuman, S., J. Biol. Chem., 1997, vol. 272, pp. 3891–3896.

    Article  CAS  PubMed  Google Scholar 

  108. Saenger, W., Principles of Nucleic Acid Structure, New York: Springer, 1984.

    Google Scholar 

  109. Slesarev, A.I., Lake, J.A., Stetter, K.O., Gellert, M., and Kozyavkin, S.A., J. Biol. Chem., 1994, vol. 269, pp. 3295–3303.

    CAS  PubMed  Google Scholar 

  110. Kozyavkin, S.A., Pushkin, A.V., Eiserling, F.A., Stetter, K.O., Lake, J.A., and Slesarev, A.I., J. Biol. Chem., 1995, vol. 270, pp. 13593–13595.

    Article  CAS  PubMed  Google Scholar 

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Original Russian Text © D.V. Bugreev, G.A. Nevinsky, 2010, published in Bioorganicheskaya Khimiya, 2010, Vol. 36, No. 3, pp. 293–311.

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Bugreev, D.V., Nevinsky, G.A. The structure and mechanism of the action of type-IB DNA topoisomerases. Russ J Bioorg Chem 36, 269–286 (2010). https://doi.org/10.1134/S1068162010030015

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