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Functional Specifics of the MutL Protein of the DNA Mismatch Repair System in Different Organisms

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Abstract

A DNA mismatch repair (MMR) system is found in all living organisms. MMR dysfunction at any step of DNA repair leads to an accumulation of mutations in the cell, thus decreasing the viability. In most organisms, the MutL protein plays a key role in mismatch elimination. MutL is capable of introducing a single-strand break in the daughter DNA strand. The review summarizes information about the MMR systems of eukaryotes and prokaryotes, the MutL structure, and the interactions of MutL with DNA and other MMR proteins.

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REFERENCES

  1. Kunkel, T.A. and Erie, D.A., Annu. Rev. Biochem., 2005, vol. 74, pp. 681–710. https://doi.org/10.1146/annurev.biochem.74.082803.133243

    Article  CAS  PubMed  Google Scholar 

  2. Modrich, P. and Lahue, R., Annu. Rev. Biochem., 1996, vol. 65, pp. 101–133. https://doi.org/10.1146/annurev.bi.65.070196.000533

    Article  CAS  PubMed  Google Scholar 

  3. Jiricny, J., Cold Spring Harb. Perspect. Biol., 2013, vol. 5, a012633. https://doi.org/10.1101/cshperspect.a012633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Arana, M.E. and Kunkel, T.A., Semin. Cancer Biol., 2010, vol. 20, pp. 304–311. https://doi.org/10.1016/j.semcancer.2010.10.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Guarné, A., Progr. Mol. Biol. Transl. Sci., 2012, pp. 41–70. https://doi.org/10.1016/B978-0-12-387665-2.00003-1

  6. Peltomaki, P., J. Clin. Oncol., 2003, vol. 21, pp. 1174–1179. https://doi.org/10.1200/JCO.2003.04.060

    Article  CAS  PubMed  Google Scholar 

  7. Liu, J., Hanne, J., Britton, B.M., Bennett, J., Kim, D., Lee, J.-B., and Fishel, R., Nature, 2016, vol. 539, pp. 583–587. https://doi.org/10.1038/nature20562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kadyrova, L.Y. and Kadyrov, F.A., DNA Repair (Amst.), 2016, vol. 38, pp. 42–49. https://doi.org/10.1016/j.dnarep.2015.11.023

    Article  CAS  Google Scholar 

  9. Liu, J., Lee, J.-B., and Fishel, R., J. Mol. Biol., 2018, vol. 430, pp. 4456–4468. https://doi.org/10.1016/j.jmb.2018.05.039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Modrich, P., J. Biol. Chem., 1989, vol. 264, pp. 6597–6600.

    CAS  PubMed  Google Scholar 

  11. Grilley, M., Griffith, J., and Modrich, P., J. Biol. Chem., 1993, vol. 268, pp. 11 830–11 837.

    Google Scholar 

  12. Lamers, M.H., Perrakis, A., Enzlin, J.H., Winterwerp, H.H.K., Wind, N., and Sixma, T.K., Nature, 2000, vol. 407, pp. 711–717. https://doi.org/10.1038/35037523

    Article  CAS  PubMed  Google Scholar 

  13. Lahue, R., Au, K., and Modrich, P., Science, 1989, vol. 245, pp. 160–164. https://doi.org/10.1126/science.2665076

    Article  CAS  PubMed  Google Scholar 

  14. Acharya, S., Foster, P.L., Brooks, P., and Fishel, R., Mol. Cell, 2003, vol. 12, pp. 233–246. https://doi.org/10.1016/S1097-2765(03)00219-3

    Article  CAS  PubMed  Google Scholar 

  15. Obmolova, G., Ban, C., Hsieh, P., and Yang, W., Nature, 2000, vol. 407, pp. 703–710. https://doi.org/10.1038/35037509

    Article  CAS  PubMed  Google Scholar 

  16. Bjornson, K.P. and Modrich, P., J. Biol. Chem., 2003, vol. 278, pp. 18 557–18 562. https://doi.org/10.1074/jbc.M301101200

    Article  CAS  Google Scholar 

  17. Antony, E. and Hingorani, M.M., Biochemistry, 2004, vol. 43, pp. 13 115–13 128. https://doi.org/10.1021/bi049010t

    Article  CAS  Google Scholar 

  18. Hingorani, M.M., DNA Repair (Amst.), 2016, vol. 38, pp. 24–31. https://doi.org/10.1016/j.dnarep.2015.11.017

    Article  CAS  Google Scholar 

  19. Groothuizen, F.S., Winkler, I., Cristovao, M., Fish, A., Winterwerp, H.H., Reumer, A., Marx, A.D., Hermans, N., Nicholls, R.A., Murshudov, G.N., Lebbink, J.H., Friedhoff, P., and Sixma, T.K., Elife, 2015, vol. 4, e06744. https://doi.org/10.7554/eLife.06744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Dutta, R. and Inouye, M., Trends Biochem. Sci., 2000, vol. 25, pp. 24–28. https://doi.org/10.1016/S0968-0004(99)01503-0

    Article  CAS  PubMed  Google Scholar 

  21. Sancar, A. and Hearst, J., Science, 1993, vol. 259, pp. 1415–1420. https://doi.org/10.1126/science.8451638

    Article  CAS  PubMed  Google Scholar 

  22. Au, K.G., Welsh, K., and Modrich, P., J. Biol. Chem., 1992, vol. 267, pp. 12 142–12 148.

    Google Scholar 

  23. Welsh, K.M., Lu, A.L., Clark, S., and Modrich, P., J. Biol. Chem., 1987, vol. 262, pp. 15 624–15 629.

    Google Scholar 

  24. Hall, M.C., EMBO J., 1998, vol. 17, pp. 1535–1541. https://doi.org/10.1093/emboj/17.5.1535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. de Saro, F.J. and O’Donnell, M., Proc. Natl. Acad. Sci. U. S. A., 2001, vol. 98, pp. 8376–8380. https://doi.org/10.1073/pnas.121009498

    Article  Google Scholar 

  26. Correa, E.M.E., Martina, M.A., Tullio, L.De., Argaraña, C.E., and Barra, J.L., DNA Repair (Amst.), 2011, vol. 10, pp. 1106–1113. https://doi.org/10.1016/j.dnarep.2011.08.007

    Article  CAS  Google Scholar 

  27. 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., and Guarne, A., Mol. Cell, 2010, vol. 39, pp. 145–151. https://doi.org/10.1016/j.molcel.2010.06.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Duppatla, V., Bodda, C., Urbanke, C., Friedhoff, P., and Rao, D.N., Biochem. J., 2009, vol. 423, pp. 265–277. https://doi.org/10.1042/BJ20090626

    Article  CAS  PubMed  Google Scholar 

  29. Iino, H., Kim, K., Shimada, A., Masui, R., Kuramitsu, S., and Fukui, K., Biosci. Rep., vol. 31, pp. 309–322. https://doi.org/10.1007/s00792-015-0745-2

  30. Fukui, K., Nishida, M., Nakagawa, N., Masui, R., and Kuramitsu, S., J. Biol. Chem., 2008, vol. 283, pp. 12 136–12 145. https://doi.org/10.1074/jbc.M800110200

    Article  CAS  Google Scholar 

  31. Monakhova, M.V., Penkina, A.I., Pavlova, A.V., Lyashchuk, A.M., Kucherenko, V.V., Alekseevskii, A.V., Lunin, V.G., Fridkhoff, P., Klug, G., Oretskaya, T.S., and Kubareva, E.A., Biochemistry (Moscow), 2018, vol. 83, pp. 281–293. https://doi.org/10.1134/S0006297918030082

    Article  CAS  PubMed  Google Scholar 

  32. Bende, S.M. and Grafstrom, R.H., Nucleic Acids Res., 1991, vol. 19, pp. 1549–1555. https://doi.org/10.1093/nar/19.7.1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Drotschmann, K., Hall, M.C., Shcherbakova, P.V., Wang, H., Erie, D.A., Brownewell, F.R., Kool., E.T., and Kunkel, T.A., Biol. Chem., 2002, vol. 383, pp. 969–975. https://doi.org/10.1515/BC.2002.103

    Article  CAS  PubMed  Google Scholar 

  34. Drummond, J., Li, G., Longley, M., and Modrich, P., Science, 1995, vol. 268, pp. 1909–1912. https://doi.org/10.1126/science.7604264

    Article  CAS  PubMed  Google Scholar 

  35. Li, G.M. and Modrich, P., Proc. Natl. Acad. Sci. U. S. A., 1995, vol. 92, pp. 1950–1954. https://doi.org/10.1073/pnas.92.6.1950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Strand, M., Prolla, T.A., Liskay, R.M., and Petes, T.D., Nature, 1993, vol. 365, pp. 274–276. https://doi.org/10.1038/365274a0

    Article  CAS  PubMed  Google Scholar 

  37. Harfe, B.D. and Jinks-Robertson, S., Ann. Rev. Genet., 2000, vol. 34, pp. 359–399. https://doi.org/10.1146/annurev.genet.34.1.359

    Article  CAS  PubMed  Google Scholar 

  38. McCulloch, S.D., Gu, L., and Li, G.-M., J. Biol. Chem., 2003, vol. 278, pp. 3891–3896. https://doi.org/10.1074/jbc.M210687200

    Article  CAS  PubMed  Google Scholar 

  39. Bowen, N., Smith, C.E., Srivatsan, A., Willcox, S., Griffith, J.D., and Kolodner, R.D., Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, pp. 18 472–18 477. https://doi.org/10.1073/pnas.1318971110

    Article  CAS  Google Scholar 

  40. Szankasi, P. and Smith, G., Science, 1995, vol. 267, pp. 1166–1169. https://doi.org/10.1126/science.7855597

    Article  CAS  PubMed  Google Scholar 

  41. Tishkoff, D.X., Boerger, A.L., Bertrand, P., Filosi, N., Gaida, G.M., Kane, M.F., and Kolodner, R.D., Proc. Natl. Acad. Sci. U. S. A., 1997, vol. 94, pp. 7487–7492. https://doi.org/10.1073/pnas.94.14.7487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Genschel, J., Bazemore, L.R., and Modrich, P., J. Biol. Chem., 2002, vol. 277, pp. 13 302–13 311. https://doi.org/10.1074/jbc.M111854200

    Article  CAS  Google Scholar 

  43. Umar, A., Buermeyer, A.B., Simon, J.A., Thomas, D.C., Clark, A.B., Liskay, R.M., and Kunkel, T.A., Cell, 1996, vol. 87, pp. 65–73. https://doi.org/10.1016/S0092-8674(00)81323-9

    Article  CAS  PubMed  Google Scholar 

  44. Johnson, R.E., Kovvali, G.K., Guzder, S.N., Amin, N.S., Holm, C., Habraken, Y., Sung, P., Prakash, L., and Prakash, S., J. Biol. Chem., 1996, vol. 271, pp. 27 987–27 990. https://doi.org/10.1074/jbc.271.45.27987

    Article  Google Scholar 

  45. Almawi, A.W., Scotland, M.K., Randall, J.R., Liu, L., Martin, H.K., Sacre, L., Shen, Y., Pillon, M.C., Simmons, L.A., Sutton, M.D., and Guarné, A., Nucleic Acids Res., 2019, vol. 47, pp. 4831–4842. https://doi.org/10.1093/nar/gkz115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Genschel, J. and Modrich, P., Mol. Cell, 2003, vol. 12, pp. 1077–1086. https://doi.org/10.1016/S1097-2765(03)00428-3

    Article  CAS  PubMed  Google Scholar 

  47. Dzantiev, L., Constantin, N., Genschel, J., Iyer, R.R., Burgers, P.M., and Modrich, P., Mol. Cell, 2004, vol. 15, pp. 31–41. https://doi.org/10.1016/j.molcel.2004.06.016

    Article  CAS  PubMed  Google Scholar 

  48. Lin, Y.-L., Shivji, M.K.K., Chen, C., Kolodner, R., Wood, R.D., and Dutta, A., J. Biol. Chem., 1998, vol. 273, pp. 1453–1461. https://doi.org/10.1074/jbc.273.3.1453

    Article  CAS  PubMed  Google Scholar 

  49. Qiu, H. and Wang, Y., J. Proteome Res., 2009, vol. 8, pp. 1983–1991. https://doi.org/10.1021/pr8009319

    Article  CAS  PubMed Central  Google Scholar 

  50. Zhang, Y., Yuan, F., Presnell, S.R., Tian, K., Gao, Y., Tomkinson, A.E., Gu, L., and Li, G.-M., Cell, 2005, vol. 122, pp. 693–705. https://doi.org/10.1016/j.cell.2005.06.027

    Article  CAS  PubMed  Google Scholar 

  51. Longley, M.J., Pierce, A.J., and Modrich, P., J. Biol. Chem., 1997, vol. 272, pp. 10 917–10 921. https://doi.org/10.1074/jbc.272.16.10917

    Article  Google Scholar 

  52. Constantin, N., Dzantiev, L., Kadyrov, F.A., and Modrich, P., J. Biol. Chem., 2005, vol. 280, pp. 39 752–39 761. https://doi.org/10.1074/jbc.M509701200

    Article  CAS  Google Scholar 

  53. Kadyrov, F.A., Genschel, J., Fang, Y., Penland, E., Edelmann, W., and Modrich, P., Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, pp. 8495–8500. https://doi.org/10.1073/pnas.0903654106

    Article  PubMed  PubMed Central  Google Scholar 

  54. Flores-Rozas, H. and Kolodner, R.D., Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, pp. 12 404–12 409. https://doi.org/10.1073/pnas.95.21.12404

    Article  Google Scholar 

  55. Nishant, K.T., Plys, A.J., and Alani, E., Genetics, 2008, vol. 179, pp. 747–755. https://doi.org/10.1534/genetics.108.086645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Cannavo, E., Marra, G., Sabates-Bellver, J., Menigatti, M., Lipkin, S.M., Fischer, F., Cejka, P., and Jiricny, J., Cancer Res., 2005, vol. 65, pp. 10 759–10 766. https://doi.org/10.1158/0008-5472.CAN-05-2528

    Article  CAS  Google Scholar 

  57. Ghodgaonkar, M.M., Lazzaro, F., Olivera-Pimentel, M., Artola-Borán, M., Cejka, P., Reijns, M.A., Jackson, A.P., Plevani, P., Muzi-Falconi, M., and Jiricny, J., Mol. Cell, 2013, vol. 50, pp. 323–332. https://doi.org/10.1016/j.molcel.2013.03.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Lujan, S.A., Williams, J.S., Clausen, A.R., Clark, A.B., and Kunkel, T.A., Mol. Cell, 2013, vol. 50, pp. 437–443. https://doi.org/10.1016/j.molcel.2013.03.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Liu, Y., Kadyrov, F.A., and Modrich, P., DNA Repair (Amst.), 2011, vol. 10, pp. 1145–1153. https://doi.org/10.1016/j.dnarep.2011.08.012

    Article  CAS  Google Scholar 

  60. Kadyrova, L.Y., Blanko, E.R., and Kadyrov, F.A., Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, pp. 2753–2758. https://doi.org/10.1073/pnas.1015914108

    Article  PubMed  PubMed Central  Google Scholar 

  61. Li, F., Mao, G., Tong, D., Huang, J., Gu, L., Yang, W., and Li, G.-M., Cell, 2013, vol. 153, pp. 590–600. https://doi.org/10.1016/j.cell.2013.03.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Liu, D., Keijzers, G., and Rasmussen, L.J., Mutat. Res., 2017, vol. 773, pp. 174–187. https://doi.org/10.1016/j.mrrev.2017.07.001

    Article  CAS  PubMed  Google Scholar 

  63. Pluciennik, A., Dzantiev, L., Iyer, R.R., Constantin, N., Kadyrov, F.A., and Modrich, P., Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, pp. 16 066–16 071. https://doi.org/10.1073/pnas.1010662107

    Article  Google Scholar 

  64. Moldovan, G.-L., Pfander, B., and Jentsch, S., Cell, 2007, vol. 129, pp. 665–679. https://doi.org/10.1016/j.cell.2007.05.003

  65. Mossi, R., Jonsson, Z.O., Allen, B.L., Hardin, S.H., and Hubscher, U., J. Biol. Chem., 1997. https://doi.org/10.1074/jbc.272.3.1769

  66. Clark, A.B., Valle, F., Drotschmann, K., Gary, R.K., and Kunkel, T.A., J. Biol. Chem., 2000, vol. 275, pp. 36 498–36 501. https://doi.org/10.1074/jbc.C000513200

    Article  Google Scholar 

  67. Genschel, J., Kadyrova, L.Y., Iyer, R.R., Dahal, B.K., Kadyrov, F.A., and Modrich, P., Proc. Natl. Acad. Sci. U. S. A., 2017, vol. 114, pp. 4930–4935. https://doi.org/10.1073/pnas.1702561114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Gradia, S., Acharya, S., and Fishel, R., Cell, 1997, vol. 91, pp. 995–1005. https://doi.org/10.1016/S0092-8674(00)80490-0

    Article  CAS  PubMed  Google Scholar 

  69. Pillon, M.C., Babu, V.M.P., Randall, J.R., Cai, J., Simmons, L.A., Sutton, M.D., and Guarné, A., Nucleic Acids Res., 2015, vol. 43, pp. 10 746–10 759. https://doi.org/10.1093/nar/gkv918

    Article  CAS  Google Scholar 

  70. Friedhoff, P., Li, P., and Gotthardt, J., DNA Repair (Amst.), 2016, vol. 38, pp. 50–57. https://doi.org/10.1016/j.dnarep.2015.11.013

    Article  CAS  Google Scholar 

  71. Pillon, M.C., Miller, J.H., and Guarné, A., DNA Repair (Amst.), 2011, vol. 10, pp. 87–93. https://doi.org/10.1016/j.dnarep.2010.10.003

    Article  CAS  Google Scholar 

  72. Liu, L., Ortiz Castro, M.C., Rodríguez González, J., Pillon, M.C., and Guarné, A., DNA Repair (Amst.), 2019, vol. 73, pp. 1–6. https://doi.org/10.1016/j.dnarep.2018.10.003

    Article  CAS  Google Scholar 

  73. Fukui, K., Baba, S., Kumasaka, T., and Yano, T., J. Biol. Chem., 2016, vol. 291, p. 1074. https://doi.org/10.1074/jbc.M116.739664

    Article  CAS  Google Scholar 

  74. Shimada, A., Kawasoe, Y., Hata, Y., Takahashi, T.S., Masui, R., Kuramitsu, S., and Fukui, K., FEBS J., 2013, vol. 280, pp. 3467–3479. https://doi.org/10.1111/febs.12344

    Article  CAS  PubMed  Google Scholar 

  75. Kadyrov, F.A., Dzantiev, L., Constantin, N., and Modrich, P., Cell, 2006, vol. 126, pp. 297–308. https://doi.org/10.1016/j.cell.2006.05.039

    Article  CAS  PubMed  Google Scholar 

  76. Lyer, R.R., Pluciennik, A., Burdett, V., and Modrich, P.L., Chem. Rev., 2006, vol. 106, pp. 302–323. https://doi.org/10.1021/cr0404794

    Article  CAS  Google Scholar 

  77. Manhart, C.M. and Alani, E., DNA Repair (Amst.), 2016, vol. 38, pp. 84–93. https://doi.org/10.1016/j.dnarep.2015.11.024

    Article  CAS  Google Scholar 

  78. Zakharyevich, K., Tang, S., Ma, Y., and Hunter, N., Cell, 2012, vol. 149, pp. 334–347. https://doi.org/10.1016/j.cell.2012.03.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Ranjha, L., Anand, R., and Cejka, P., J. Biol. Chem., 2014, vol. 289, pp. 5674–5686. https://doi.org/10.1074/jbc.M113.533810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Duroc, Y., Kumar, R., Ranjha, L., Adam, C., Guérois, R., Md, MuntazK., Marsolier-Kergoat, M.-C., Dingli, F., Laureau, R., Loew, D., Llorente, B., Charbonnier, J.-B., Cejka, P., and Borde, V., Elife, 2017, vol. 6, e21900. https://doi.org/10.7554/eLife.21900

    Article  PubMed  PubMed Central  Google Scholar 

  81. Gomes-Pereira, M., Hum. Mol. Genet., 2004, vol. 13, pp. 1815–1825. https://doi.org/10.1093/hmg/ddh186

    Article  CAS  PubMed  Google Scholar 

  82. Pluciennik, A., Burdett, V., Baitinger, C., Iyer, R.R., Shi, K., and Modrich, P., Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, pp. 12 277–12 282. https://doi.org/10.1073/pnas.1311325110

    Article  Google Scholar 

  83. Pinto, R.M., Dragileva, E., Kirby, A., Lloret, A., Lopez, E., Claire, J.St., Panigrahi, G.B., Hou, C., Holloway, K., Gillis, T., Guide, J.R., Cohen, P.E., Li, G.-M., Pearson, C.E., Daly, M.J., and Wheeler, V.C., PLoS Genet., Zeitlin, S.O., Ed., 2013, vol. 9, e1003930. https://doi.org/10.1371/journal.pgen.1003930

  84. Halabi, A., Fuselier, K.T.B., and Grabczyk, E., Nucleic Acids Res., 2018, vol. 46, pp. 4022–4032. https://doi.org/10.1093/nar/gky143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Zhao, X., Zhang, Y., Wilkins, K., Edelmann, W., and Usdin, K., PLoS Genet., 2018, vol. 14, e1007719. https://doi.org/10.1371/journal.pgen.1007719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Lee, J.-M., Correia, K., Loupe, J., Kim, K.-H., Barker, D., Hong, E.P., Chao, M.J., Long, J.D., Lucente, D., Vonsattel, J.P.G., Pinto, R.M., Abu, ElneelK., Ramos, E.M., Mysore, J.S., Gillis, T., Wheeler, V.C., Macdonald, M.E., Gusella, J.F., Mcallister, B., Massey, T., Medway, C., Stone, T.C., Hall, L., Jones, L., Holmans, P., Kwak, S., Ehrhardt, A.G., Sampaio, C., Ciosi, M., Maxwell, A., Chatzi, A., Monckton, D.G., Orth, M., Landwehrmeyer, B.G., Paulsen, J.S., Dorsey, E.R., Shoulson, I., and Myers, R.H., Cell, 2019, vol. 178, pp. 887–900, e14. https://doi.org/10.1016/j.cell.2019.06.036

  87. Ciosi, M., Maxwell, A., Cumming, S.A., Hensman Moss, D.J., Alshammari, A.M., Flower, M.D., Durr, A., Leavitt, B.R., Roos, R.A.C., Holmans, P., Jones, L., Langbehn, D.R., Kwak, S., Tabrizi, S.J., and Monckton, D.G., EBioMedicine, 2019, vol. 48, pp. 568–580. https://doi.org/10.1016/j.ebiom.2019.09.020

    Article  PubMed  PubMed Central  Google Scholar 

  88. Kadyrova, L.Y., Gujar, V., Burdett, V., Modrich, P.L., and Kadyrov, F.A., Proc. Natl. Acad. Sci. U. S. A., 2020, vol. 117, pp. 3535–3542. https://doi.org/10.1073/pnas.1914718117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Guarné, A. and Charbonnier, J.-B., Prog. Biophys. Mol. Biol., 2015, vol. 117, pp. 149–156. https://doi.org/10.1016/j.pbiomolbio.2015.02.002

    Article  CAS  PubMed  Google Scholar 

  90. Fukui, K., Iino, H., Baba, S., Kumasaka, T., Kuramitsu, S., and Yano, T., Biochim. Biophys. Acta—Proteins Proteomics, 2017, vol. 1865, pp. 1178–1187. https://doi.org/10.1016/j.bbapap.2017.06.024

    Article  CAS  Google Scholar 

  91. Ban, C. and Yang, W., Cell, 1998, vol. 95, pp. 541–552. https://doi.org/10.1016/S0092-8674(00)81621-9

    Article  CAS  PubMed  Google Scholar 

  92. Guarné, A., EMBO J., 2001, vol. 20, pp. 5521–5531. https://doi.org/10.1093/emboj/20.19.5521

    Article  PubMed  PubMed Central  Google Scholar 

  93. Ban, C., Junop, M., and Yang, W., Cell, 1999, vol. 97, pp. 85–97. https://doi.org/10.1016/S0092-8674(00)80717-5

    Article  CAS  PubMed  Google Scholar 

  94. Arana, M.E., Holmes, S.F., Fortune, J.M., Moon, A.F., Pedersen, L.C., and Kunkel, T.A., DNA Repair (Amst.), 2010, vol. 9, pp. 448–457. https://doi.org/10.1016/j.dnarep.2010.01.010

    Article  CAS  PubMed Central  Google Scholar 

  95. Banasik, M. and Sachadyn, P., Mutat. Res. Mol. Mech. Mutagen., 2014, vol. 769, pp. 69–79. https://doi.org/10.1016/j.mrfmmm.2014.07.006

    Article  CAS  Google Scholar 

  96. Räschle, M., Dufner, P., Marra, G., and Jiricny, J., J. Biol. Chem., 2002, vol. 277, pp. 21 810–21 820. https://doi.org/10.1074/jbc.M108787200

    Article  CAS  Google Scholar 

  97. Yang, W., Mutat. Res. Repair, 2000, vol. 460, pp. 245–256. https://doi.org/10.1016/S0921-8777(00)00030-6

    Article  CAS  Google Scholar 

  98. Sacho, E.J., Kadyrov, F.A., Modrich, P., Kunkel, T.A., and Erie, D.A., Mol. Cell, 2008, vol. 29, pp. 112–121. https://doi.org/10.1016/j.molcel.2007.10.030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Schopf, F.H., Biebl, M.M., and Buchner, J., Nat. Rev. Mol. Cell Biol., 2017, vol. 18, pp. 345–360. https://doi.org/10.1038/nrm.2017.20

    Article  CAS  PubMed  Google Scholar 

  100. Polosina, Y.Y. and Cupples, C.G., BioEssays, 2010, vol. 32, pp. 51–59. https://doi.org/10.1002/bies.200900089

  101. Mauris, J. and Evans, T.C., PLoS One, Marinus, M.G., Ed., 2009, vol. 4, e7175. https://doi.org/10.1371/journal.pone.0007175

  102. Guarné, A., Ramon-Maiques, S., Wolff, E.M., Ghirlando, R., Hu, X., Miller, J.H., and Yang, W., EMBO J., 2004, vol. 23, pp. 4134–4145. https://doi.org/10.1038/sj.emboj.7600412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Schorzman, A.N., Perera, L., Cutalo-Patterson, J.M., Pedersen, L.C., Pedersen, L.G., Kunkel, T.A., and Tomer, K.B., DNA Repair (Amst.), 2011, vol. 10, pp. 454–465. https://doi.org/10.1016/j.dnarep.2011.01.010

    Article  CAS  PubMed Central  Google Scholar 

  104. Hall, M.C., Wang, H., Erie, D.A., and Kunkel, T.A., J. Mol. Biol., 2001, vol. 312, pp. 637–647. https://doi.org/10.1006/jmbi.2001.4958

    Article  CAS  PubMed  Google Scholar 

  105. Robertson, A., Pattishall, S.R., and Matson, S.W., J. Biol. Chem., 2006, vol. 281, pp. 8399–8408. https://doi.org/10.1074/jbc.M509184200

    Article  CAS  PubMed  Google Scholar 

  106. Junop, M., DNA Repair (Amst.), 2003, vol. 2, pp. 387–405. https://doi.org/10.1016/S1568-7864(02)00245-8

    Article  CAS  Google Scholar 

  107. Monakhova, M., Ryazanova, A., Kunetsky, V., Li, P., Shilkin, E., Kisil, O., Rao, D.N., Oretskaya, T., Friedhoff, P., and Kubareva, E., Biochimie, 2020, vols. 171–172, pp. 43–54. https://doi.org/10.1016/j.biochi.2020.02.004

    Article  CAS  PubMed  Google Scholar 

  108. Niedziela-Majka, A., Maluf, N.K., Antony, E., and Lohman, T.M., Biochemistry, 2011, vol. 50, pp. 7868–7880. https://doi.org/10.1021/bi200753b

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Monakhova, M.V., Kubareva, E.A., Romanova, E.A., Semkina, A.S., Naberezhnov, D.S., Rao, D.N., Zatsepin, T.S., and Oretskaya, T.S., Russ. J. Bioorg. Chem., vol. 45, pp. 144–154. https://doi.org/10.1134/S1068162019020079

  110. Bjornson, K.P., Allen, D.J., and Modrich, P., Biochemistry, 2000, vol. 39, pp. 3176–3183. https://doi.org/10.1021/bi992286u

    Article  CAS  PubMed  Google Scholar 

  111. Gueneau, E., Dherin, C., Legrand, P., Tellier-Lebegue, C., Gilquin, B., Bonnesoeur, P., Londino, F., Quemener, C., Le Du, M.-H., Márquez, J.A., Moutiez, M., Gondry, M., Boiteux, S., and Charbonnier, J.-B., Nat. Struct. Mol. Biol., 2013, vol. 20, pp. 461–468. https://doi.org/10.1038/nsmb.2511

    Article  CAS  PubMed  Google Scholar 

  112. Kadyrov, F.A., Holmes, S.F., Arana, M.E., Lukianova, O.A., O’Donnell, M., Kunkel, T.A., and Modrich, P., J. Biol. Chem., 2007, vol. 282, pp. 37 181–37 190. https://doi.org/10.1074/jbc.M707617200

    Article  CAS  Google Scholar 

  113. Kosinski, J., Plotz, G., Guarne, A., Bujnicki, J.M., and Friedhoff, P., J. Mol. Biol., 2008, vol. 382, pp. 610–627. https://doi.org/10.1016/j.jmb.2008.06.056

    Article  CAS  PubMed  Google Scholar 

  114. Erdeniz, N., Nguyen, M., Deschênes, S.M., and Liskay, R.M., DNA Repair (Amst.), 2007, vol. 6, pp. 1463–1470. https://doi.org/10.1016/j.dnarep.2007.04.013

    Article  CAS  Google Scholar 

  115. Yang, W., Nat. Struct. Mol. Biol., 2008, vol. 15, pp. 1228–1231. https://doi.org/10.1038/nsmb.1502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Stapleton, B., Walker, L.R., and Logan, T.M., Biochemistry, 2013, vol. 52, pp. 1927–1938. https://doi.org/10.1021/bi301608p

    Article  CAS  PubMed  Google Scholar 

  117. Namadurai, S., Jain, D., Kulkarni, D.S., Tabib, C.R., Friedhoff, P., Rao, D.N., and Nair, D.T., PLoS One, 2010, vol. 5, e13726. https://doi.org/10.1371/journal.pone.0013726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Fukui, K., Baba, S., Kumasaka, T., and Yano, T., FEBS Lett., 2018, vol. 592, pp. 1611–1619. https://doi.org/10.1002/1873-3468.13050

    Article  CAS  PubMed  Google Scholar 

  119. Groothuizen, F.S. and Sixma, T.K., DNA Repair (Amst.), 2016, vol. 38, pp. 14–23. https://doi.org/10.1016/j.dnarep.2015.11.012

    Article  CAS  Google Scholar 

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ACKNOWLEDGMENTS

We are grateful to A.V. Pavlova (Student, Department of Chemistry, Lomonosov Moscow State University) and V.A. Anashkin (Senior Researcher, A.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University) for help in figure preparation.

Funding

This work was supported by the Russian Foundation for Basic Research (project no. 18-34-00768).

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Authors and Affiliations

  1. Department of Chemistry and Belozersky Institute of Physicochemical Biology, Moscow State University, 119991, Moscow, Russia

    M. V. Monakhova, M. A. Milakina, T. S. Oretskaya & E. A. Kubareva

  2. MIREA—Russian Technological University, Lomonosov Institute of Fine Chemical Technologies, 119571, Moscow, Russia

    R. M. Trikin

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  1. M. V. Monakhova
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  2. M. A. Milakina
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Correspondence to T. S. Oretskaya.

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This work does not contain any studies involving animal or human subjects performed by any of the authors.

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Translated by T. Tkacheva

Abbreviations: CTD, C-terminal domain of MutL; GHKL, gyrase, Hsp90, histidine kinase, MutL (ATPase family) ; IdeR, iron-dependent repressors; MMR, mismatch repair; NTD, N‑terminal domain of MutL; PCNA, proliferating сell nuclear antigen; RER, ribonucleotide excision repair; SSB, single-strand binding protein; β-clamp, β-subunit of DNA polymerase III; XRC, X-ray crystallography

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Monakhova, M.V., Milakina, M.A., Trikin, R.M. et al. Functional Specifics of the MutL Protein of the DNA Mismatch Repair System in Different Organisms. Russ J Bioorg Chem 46, 875–890 (2020). https://doi.org/10.1134/S1068162020060217

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