Modern Aspects of the Structural and Functional Organization of the DNA Mismatch Repair System

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Abstract


This review is focused on the general aspects of the DNA mismatch repair (MMR) process. The key proteins of the DNA mismatch repair system are MutS and MutL. To date, their main structural and functional characteristics have been thoroughly studied. However, different opinions exist about the initial stages of the mismatch repair process with the participation of these proteins. This review aims to summarize the data on the relationship between the two MutS functions, ATPase and DNA-binding, and to systematize various models of coordination between the mismatch site and the strand discrimination site in DNA. To test these models, novel techniques for the trapping of short-living complexes that appear at different MMR stages are to be developed.


S. A. Perevoztchikova

Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University

Email: kubareva@belozersky.msu.ru

Russian Federation

E. A. Romanova

Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University

Email: kubareva@belozersky.msu.ru

Russian Federation

T. S. Oretskaya

Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University; Chemistry Department, Lomonosov Moscow State University

Email: kubareva@belozersky.msu.ru

Russian Federation

P. Friedhoff

Institute of Biochemistry, Justus Liebig University

Email: kubareva@belozersky.msu.ru

Germany

E. A. Kubareva

Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University

Author for correspondence.
Email: kubareva@belozersky.msu.ru

Russian Federation

  1. Lewin B. // Genes. Boston, MA // Jones Bartlett Publ 2008, P.892
  2. Futreal P.A., Coin L., Marshall M., Down T., Hubbard T., Wooster R., Rahman N., Stratton M.R. // Nat. Rev. Cancer 2004, V.4, P.177-183
  3. Drake J.W. // Ann. N.Y. Acad. Sci 1999, V.870, P.100-107
  4. Ayala F.J., Kiger J.A. // Modern genetics. University of California, Davis. 1984, V.2, P.296
  5. Friedberg E.C., Walker G.C., Siede W. // DNA repair and mutagenesis // Washington, D.C.: ASM Press 1995, P.698
  6. O’Neil N., Rose A. // WormBook 2006, P.1-12
  7. Koshland D.E. Jr. // Science 1994, V.266, P.1925
  8. Lavrik O.I. // Biochemistry (Mosc.) 2011, V.76, P.3
  9. Buermeyer A.B., Deschênes S.M., Baker S.M., Liskay R.M. // Annu. Rev. Genet 1999, V.33, P.533-564
  10. Hsieh P. // Mutat. Res. 2001, V.486, P.71-87
  11. Marti T.M., Kunz C., Fleck O. // J. Cell Physiol. 2002, V.191, P.28-41
  12. Barnes D.E., Lindahl T. // Annu. Rev. Genet. 2004, V.38, P.445-476
  13. Kunkel T.A., Erie D.A. // Annu. Rev. Biochem. 2005, V.74, P.681-710
  14. Iyer R.R., Pluciennik A., Burdett V., Modrich P.L. // Chem. Rev. 2006, V.106, P.302-323
  15. Jiricny J. // Nat. Rev. Mol. Cell Biol. 2006, V.7, P.335-346
  16. Fukui K. // Journal of Nucleic Acids. 2010, P.1-16
  17. Goliasnaia N.V., Tsvetkova N.A. // Mol. Biol. (Mosk). 2006, V.40, P.211-223
  18. Modrich P. // Annu. Rev. Genet. 1991, V.25, P.229-253
  19. Lichten M., Goyon C., Schultes N., Treco D., Szostak J.W., Haber J.E., Nicolas A. // Proc. Natl. Acad. Sci. U.S.A. 1990, V.87, P.7653-7657
  20. Reenan R.A., Kolodner R.D. // Genetics. 1992, V.132, P.975-985
  21. Modrich P., Lahue R. // Annu. Rev. Biochem. 1996, V.65, P.101-133
  22. Kolodner R.D., Marsischky G.T. // Curr. Opin. Genet. Dev. 1999, V.9, P.89-96
  23. Branch P., Aquilina G., Bignami M., Karran P. // Nature 1993, V.362, P.652-654
  24. Duckett D.R., Drummond J.T., Murchie A.I.H., Reardon J.T., Sancar A., Lilley D.M.J., Modrich P. // Proc. Natl. Acad. Sci. U.S.A. 1996, V.93, P.6443-6447
  25. Ni T.T., Marsischky G.T., Kolodner R.D. // Molecular Cell 1999, V.4, P.439-444
  26. Mazurek A., Berardini M., Fishel R. // J. Biol. Chem. 2002, V.277, P.8260-8266
  27. Li G.M., Wang H., Romano L.J. // J. Biol. Chem. 1996, V.271, P.24084-24088
  28. Feng W.Y., Lee E.H., Hays J.B. // Genetics. 1991, V.129, P.1007-1020
  29. Mu D., Tursun M., Duckett D.R., Drummond J.T., Modrich P., Sancar A. // Mol. Cell. Biol. 1997, V.17, P.760-769
  30. Wang H., Lawrence C. W., Li G. M., Hays J. B. // J. Biol. Chem. 1999, V.274, P.16894-1690
  31. Mello J.A., Acharya S., Fishel R., Essigmann P. // Chem. Biol. 1996, V.3, P.579-589
  32. Pabla N., Ma Z., McIlhatton M.A., Fishel R., Dong Z. // J. Biol. Chem. 2011, V.286, P.10411-10418
  33. Stojic L., Brun R., Jiricny J. // DNA Repair (Amst). 2004, V.3, P.1091-1101
  34. Greig D., Travisano M., Louis E.J., Borts R.H. // J. Evol. Biol. 2003, V.16, P.429-437
  35. Sia E.A., Kokoska R.J., Dominska M., Greenwell P., Petes T.D. // Mol. Cell Biol. 1997, V.17, P.2851-2858
  36. Wu B.P., Zhang Y.L., Zhou D.Y., Gao C.F., Lai Z.S. // World J. Gastroenterol. 2000, V.6, P.902-905
  37. Bechter O.E., Zou Y., Walker W., Wright W.E., Shay J.W. // Cancer Research 2004, V.64, P.3444-3451
  38. Nguyen B., Elmore L.W., Holt S.E. // Cancer Biol. Ther. 2004, V.3, P.293-295
  39. Evans E., Alani E. // Mol. Cell. Biol. 2000, V.20, P.7839-7844
  40. Schanz S., Castor D., Fischer F., Jiricny J. // Proc. Natl. Acad. Sci. U.S.A. 2009, V.106, P.5593-5598
  41. Chahwan R., Edelmann W., Scharff M.D., Roa S. // Biomed. Pharmacother. 2011, V.65, P.529-536
  42. Aravind L., Walker D.R., Koonin E. // Nucleic Acids Res. 1999, V.27, P.1223-1242
  43. Michailidi C., Papavassiliou A.G., Troungos C. // Curr. Mol. Med. 2012, V.12, P.237-246
  44. Qiu R., DeRocco V.C., Harris C., Sharma A., Hingorani M.M., Erie D.A., Weninger K.R. // EMBO J. 2012, V.31, P.2528-2540
  45. Jiricny J., Nystrom–Lahti M. // Curr. Opin. Genet. Dev. 2000, V.10, P.157-161
  46. Harfe B.D., Jinks–Robertson S. // Annu. Rev. Genet. 2000, V.34, P.359-399
  47. Peltomäki P. // J. Clin. Oncol. 2003, V.21, P.1174-1179
  48. Reuschenbach M., Kloor M., Morak M., Wentzensen N., Germann A., Garbe Y., Tariverdian M., Findeisen P., Neumaier M., Holinski–Feder E. // Fam. Cancer. 2010, V.9, P.173-179
  49. Lahue R.S., Au K.G., Modrich P. // Science. 1989, V.245, P.160-464
  50. Balganesh T.S., Lacks S.A. // Journal of Bacteriology 1985, V.162, P.979-984
  51. Radman M., Wagner R. // Annu. Rev. Genet. 1986, V.20, P.523-538
  52. Li G.M. // Cell Res. 2008, V.18, P.85-98
  53. Zhao J., Winkler M.E. // Journal of Bacteriology 2000, V.182, P.5025-5028
  54. L. Fourrier, P. Brooks, J.M. Malinge // J. Biol. Chem. 2003, V.278, P.21267-21275
  55. Lamers M.H., Perrakis A., Enzlin J.H., Winterwerp H.H.K., de Wind N., Sixma T.K. // Nature 2000, V.407, P.711-717
  56. Wildenberg J., Meselson M. // Proc. Natl. Acad. Sci. U.S.A. 1975, V.72, P.2202-2206
  57. Wagner R., Meselson M. // Proc. Natl. Acad. Sci. U.S.A. 1976, V.73, P.4135-4139
  58. Lyons S.M., Schendel F. // Journal of Bacteriology 1984, V.159, P.421-423
  59. Duppatla N.J., Rao D.N. // Prog. Nucleic Acid Res. Mol. Biol. 2006, V.81, P.1-49
  60. Lu A.–L., Clark S., Modrich P. // Proc. Natl. Acad. Sci. U.S.A. 1983, V.80, P.4639-4643
  61. Glickman B.W. // Mutat. Res. 1979, V.61, P.153-162
  62. Marinus M.G., Poteete A., Arraj J.A. // Gene. 1984, V.28, P.123-125
  63. Gorman J., Chowdhury A., Surtees J.A., Shimada J., Reichman D.R., Alani E., Greene E.C. // Molecular Cell 2007, V.28, P.359-370
  64. Nishant K.T., Plys A.J., Alani E. // Genetics. 2008, V.179, P.747-755
  65. Claverys J.–P., Mejean P., Gasc A.–M., Sicard A.M. // Proc. Natl. Acad. Sci. U.S.A. 1983, V.80, P.5956-5960
  66. Yamaguchi M., Dao V., Modrich P. // J. Biol. Chem. 1998, V.273, P.9197-9201
  67. Mechanic L.E., Frankel B.A., Matson S.W. // J. Biol. Chem. 2000, V.275, P.38337-38346
  68. Matson S.W., Robertson A.B. // Nucleic Acids Res. 2006, V.34, P.4089-4097
  69. Cooper D.L., Lahue R.S., Modrich P. // J. Biol. Chem. 1993, V.268, P.11823-11829
  70. Viswanathan M., Burdett P., Baitinger C., Modrich P., Lovett S.T. // J. Biol. Chem. 2001, V.276, P.31053-31058
  71. Han E.S., Cooper D.L., Persky N.S., Sutera V.A. Jr., Whitaker R.D., Montello M.L., Lovett I.O., S.T. I.O. // Nucleic Acids Res. 2006, V.34, P.1084-1091
  72. Lohman T.M., Ferrari M.E. // Annu. Rev. Biochem. 1994, V.63, P.527-570
  73. Bjornson K.P., Blackwell L. J., Sage H., Baitinger C., Allen D., Modrich P. // J. Biol. Chem. 2003, V.278, P.34667-34673
  74. Kang J., Huang S., Blaser M.J. // Journal of Bacteriology 2005, V.187, P.3528-3537
  75. Snowden T., Acharya S., Butz C., Berardini M., Fishel R. // Molecular Cell 2004, V.15, P.437-451
  76. Hollingsworth N.M., Ponte L., Halsey C. // Genes Dev. 1995, №9, P.1728-1739
  77. Culligan K.M., Meyer–Gauen G., Lyons–Weiler J., Hays J.B. // Nucleic Acids Res. 2000, V.28, P.463-471
  78. Obmolova G., Ban C., Hsieh P., Yang W. // Nature 2000, V.407, P.703-710
  79. Junop M.S., Obmolova G., Rausch K., Hsieh P., Yang W. // Molecular Cell 2001, V.7, P.1-12
  80. Lamers M.H., Winterwerp H.H.K., Sixma T.K. // The EMBO Journal. 20003, V.22, P.746-756
  81. Natrajan G., Lamers M.H., Enzlin J.H., Winterwerp H.H.K., Perrakis A., Sixma T.K. // Nucleic Acids Res. 2003, V.31, P.4814-4821
  82. Alani E., Lee J.Y., Schofield M.J., Kijas A.W., Hsieh P., Yang W. // J. Biol. Chem. 2003, V.278, P.16088-16094
  83. Lebbink J.H.G., Fish A., Reumer A., Natrajan G., Winterwerp H.H., Sixma T.K. // J. Biol. Chem. 2010, V.285, P.13131-13141
  84. Lebbink J.H.G., Georgijevic D., Natrajan G., Fish A., Winterwerp H.H.K., Sixma T.K., de Wind N. // The EMBO J. 2006, V.25, P.409-419
  85. Lamers M.H., Georgijevic D., Lebbink J.H., Winterwerp H.H., Agianian B., de Wind N., Sixma T.K. // J. Biol. Chem. 2004, V.279, P.43879-43885
  86. Warren J.J., Pohlhaus T.J., Changela A., Iyer R.R., Modrich P.L., Beese L.S. // Molecular Cell 2007, V.26, P.579-592
  87. Jiricny J. // Curr. Biol. 2000, V.10, P.788-790
  88. Biswas I., Hsieh P. // J. Biol. Chem. 1997, V.272, P.13355-13364
  89. Sixma T. K. // Curr. Opin. Struct. Biol. 2001, V.11, P.47-52
  90. Yamamoto A., Schofield M.J., Biswas I., Hsieh P. // Nucleic Acids Res. 2000, V.28, P.3564-3569
  91. Junop M.S., Yang W., Funchain P., Clendenin W., Miller J.H. // DNA Repair (Amst). 2003, V.2, P.387-405
  92. Hunter W.N., Brown T., Kneale G., Anand N.N., Rabinovich D., Kennard O. // J. Biol. Chem. 1987, V.262, P.9962-9970
  93. Skelly J., Edwards K.J., Jenkins T.C., Neidle S. // Proc. Natl. Acad. Sci. U.S.A. 1993, V.90, P.804-808
  94. Werntges H., Steger G., Riesner D., Fritz H.J. // Nucleic Acids Res. 1986, V.14, P.3773-3790
  95. Wang H., Yang Y., Schofield M.J., Du C., Fridman Y., Lee S.D., Larson E.D., Drummond J.T., Alani E., Hsieh P. // Proc. Natl. Acad. Sci. U.S.A. 2003, V.100, P.14822-14827
  96. Hirano M., Hirano T. // EMBO J. 2002, V.21, P.5733-5744
  97. Verdon G., Albers S., van Oosterwijk N., Dijkstra B.W., Driessen A.J., Thunnissen A.M. // J. Mol. Biol. 2003, V.334, P.255-267
  98. Gradia S., Subramanian D., Wilson T., Acharya S., Makhov A., Griffith J., Fishel R. // Molecular Cell 1999, V.3, P.255-261
  99. Joshi A., Rao B.J. // Biochemistry. 2002, V.41, P.3654-3666
  100. Hess M.T., Gupta R.D., Kolodner R.D. // J. Biol. Chem. 2002, V.277, P.25545-25553
  101. Joseph N., Duppatla V., Rao D.N. // Prog. Nucleic Acid Res. Mol. Biol. 2006, V.81, P.1-49
  102. Antony E., Hingorani M.M. // Biochemistry. 2004, V.43, P.13115-13128
  103. Calmann M.A., Nowosielska A., Marinus M.G. // Nucleic Acids Res. 2005, V.33, P.1193-1200
  104. Jeong C., Cho W.K., Song K.M., Cook C., Yoon T.Y., Ban C., Fishel R., Lee J.B. // Nat. Struct. Mol. Biol. 2011, V.18, P.379-385
  105. Cheng X., Blumenthal R.M. // Structure. 1996, V.4, P.639-645
  106. Bischerour J., Chalmers R. // PLoS One. 2009, V.4
  107. Gradia S., Acharya S., Fishel R. // Cell. 1997, V.91, P.995-1005
  108. Fishel R. // Genes Dev. 1998, V.12, P.2096-2101
  109. Antony E., Hingorani M.M. // Biochemistry. 2003, V.42, P.7682-7693
  110. Martik D., Baitinger C., Modrich P. // J. Biol. Chem. 2004, V.279, P.28402-28410
  111. Drotschmann K., Hall M.C., Shcherbakova P.V., Wang H., Erie D.A., Brownewell F.R., Kool E.T., Kunkel T.A. // Biol. Chem. 2002, V.383, P.969-975
  112. Kijas A.W., Studamire B., Alani E. // J. Mol. Biol. 2003, V.331, P.123-138
  113. Acharya S., Foster P.L., Brooks P., Fishel R. // Molecular Cell 2003, V.12, P.233-246
  114. Bowers J., Sokolsky T., Quach T., Alani E. // J. Biol. Chem. 1999, V.274, P.16115-16125
  115. Mukherjee S., Law S.M., Feig M. // Biophysical J. 2009, V.96, P.1707-1720
  116. Polosina Y.Y., Cupples C.G. // Mutat. Res. 2010, V.705, P.228-238
  117. Zhao N., Zhu F., Yuan F., Haick A.K., Fukushige S., Gu L., Her C. // Biochem. Biophys. Res. Commun. 2008, V.370, P.338-343
  118. Dherin C., Gueneau E., Francin M., Nunez M., Miron S., Liberti S.E., Rasmussen L.J., Zinn-Justin S., Gilquin B., Charbonnier J.B. // Mol. Cell. Biol. 2009, V.29, P.907-918
  119. Kanao R., Hanaoka F., Masutani C. // Biochem. Biophys. Res. Commun. 2009, V.389, P.40-45
  120. Bende S.M., Grafstrom R.H. // Nucleic Acids Res. 1991, V.19, P.1549-1555
  121. Grilley M., Welsh K.M., Su S.S., Modrich P. // J. Biol. Chem. 1989, V.264, P.1000-1004
  122. Ban C., Junop M., Yang W. // Cell. 1999, V.97, P.85-97
  123. Ban C., Yang W. // Cell. 1998, V.95, P.541-552
  124. Hu X., Machius M., Yang W. // FEBS Lett. 2003, V.544, P.268-273
  125. Guarné A., Ramon–Maiques S., Wolff E.M., Ghirlando R., Hu X., Miller J.H., Yang W. // EMBO J. 2004, V.23, P.4134-4145
  126. Pillon M.C., Lorenowicz J.J., Uckelmann M., Klocko A.D., Mitchell R.R., Chung Y.S., Modrich P., Walker G.C., Simmons L.A., Friedhoff P., Guarné A. // Molecular Cell 2010, V.39, P.145-511
  127. Namadurai S., Jain D., Kulkarni D.S., Tabib C.R., Friedhoff P., Rao D.N., Nair D.T. // PloS One 2010, V.5, P.e13726-e13726
  128. Kosinski J., Steindorf I., Bujnicki J.M., Giron-Monzon L., Friedhoff P. // J. Mol. Biol. 2005, V.351, P.895-909
  129. Jones D.T. // J. Mol. Biol. 1999, V.292, P.195-202
  130. Jun S.H., Kim T.G. // FEBS J. 2006, V.273, P.1609-1619
  131. Sacho E.J., Kadyrov F.A., Modrich P., Kunkel T.A., Erie D.A. // Molecular Cell 2008, V.29, P.112-121
  132. Spampinato C., Modrich P. // J. Biol. Chem. 200, V.275, P.9863-9869
  133. Giron-Monzon L., Manelyte L., Ahrends R., Kirsch D., Spengler B., Friedhoff P. // J. Biol. Chem. 2004, V.279, P.49338-49345
  134. Schofield M.J., Hsieh P. // Annu. Rev. Microbiol. 2003, V.57, P.579-608
  135. Robertson A., Pattishall S.R. // J. Biol. Chem. 2006, V.281, P.8399-8408
  136. Kadyrov F.A., Dzantiev L. // Cell. 2006, V.126, P.297-308
  137. Ban C., Yang W. // EMBO J. 1998, V.17, P.1526-1534
  138. Yang W. // Mutat. Res. 2000, V.460, P.245-256
  139. Friedhoff P., Thomas E., Pingoud A. // J. Mol. Biol. 2003, V.325, P.285-297
  140. Lee J.Y., Chang J., Joseph N., Ghirlando R., Rao D.N., Yang W. // Molecular Cell 2005, V.20, P.155-166
  141. Toedt G.H., Krishnan R., Friedhoff P. // Nucleic Acids Res. 2003, V.31, P.819-825
  142. Polosina Y.Y., Cupples C.G. // BioEssays. 2010, V.32, P.51-59
  143. Mendillo M.L., Hargreaves V.V., Jamison J.W., Mo A.O., Li S., Putnam C.D., Woods V.L. Jr., Kolodner R.D. // Proc. Natl. Acad. Sci. U.S.A. 2009, V.106, P.22223-22228
  144. Winkler I., Marx A.D., Lariviere D., Heinze R.J., Cristovao M., Reumer A., Curth U., Sixma T.K., Friedhoff P. // J. Biol. Chem. 2011, V.286, P.17326-17337
  145. Kolodner R.D., Mendillo M.L., Putnam C.D. // Proc. Natl. Acad. Sci. U.S.A. 2007, V.104, P.12953-12964
  146. Pluciennik A., Modrich P. // Proc. Natl. Acad. Sci. U.S.A. 2007, V.104, P.12709-12713
  147. Dzantiev L., Constantin N., Genschel J., Iyer R.R., Burgers M., Modrich P. // Molecular Cell 2004, V.15, P.31-41
  148. Allen D.J., Makhov A., Grilley M., Taylor J., Thresher R., Modrich P., Griffith J.D. // EMBO J. 1997, V.16, P.4467-4476
  149. Blackwell L.J., Martik D., Bjornson K., Bjornson E.S., Modrich P. J. // Biol. Chem. 1998, V.273, P.32055-32062
  150. Blackwell L.J., Wang S., Modrich P. // J. Biol. Chem. 2001, V.276, P.33233-33240
  151. Mazur D.J., Mendillo M.L., Kolodner R.D. // Molecular Cell 2006, V.22, P.39-49
  152. Schofield M.J., Nayak S., Scott T.H., Du C., Hsieh P. // J. Biol. Chem. 2001, V.276, P.28291-28299
  153. Modrich P. // Annu. Rev. Biochem. 1987, V.56, P.435-466
  154. Elez M., Radman M., Matic I. // Nucleic Acids Res. 2012, V.40, P.3929-3938
  155. Jiang Y., Marszalek E. // EMBO J. 2011, V.30, P.2881-2893
  156. Heinze R.J., Sekerina S., Winkler I., Biertümpfel C., Oretskaya T.S., Kubareva E., Friedhoff P. // Mol. Biosyst. 2012, V.8, P.1861-1864

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