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Review

Progress on the non-canonical mismatch repair in Mycobacterium and its role in antibiotic resistance

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  • Institute of Modern Biopharmaceuticals, School of Life Sciences, Southwest University, Chongqing 400715, China

Received date: 2023-09-11

  Revised date: 2023-10-29

  Online published: 2023-11-03

Supported by

National Natural Science Foundation of China(82072246)

Abstract

Mismatch repair (MMR) is a common repair system after DNA replication, which is critical for maintaining genomic stability. Members of the MutS and MutL protein families are involved in key steps of mismatch repair. Despite the major importance of this repair pathway, MutS-MutL are absent in almost all Actinobacteria and many Archaea. Mycobacteria and others have another non-canonical MMR pathway, in which EndoMS/NucS plays a key role and has no structural homology compared to canonical MMR proteins (MutS/MutL). EndoMS/NucS mediated non-canonical mismatch repair plays an important role in DNA repair, mutation, homologous recombination and antibiotic resistance of Mycobacterium. By comparing the classical and non-canonical MMR pathways, this paper reviews the EndoMS/NucS-mediated non-canonical MMR pathway in Mycobacterium and its recent progress. We hope to bring new insights into the molecular mechanism of mycobacterial mismatch repair as well as to provide new research clues for mycobacterial antibiotic therapy.

Cite this article

Shasha Xiang, Jianping Xie . Progress on the non-canonical mismatch repair in Mycobacterium and its role in antibiotic resistance[J]. Hereditas(Beijing), 2023 , 45(11) : 1018 -1027 . DOI: 10.16288/j.yczz.23-236

References

[1] Chatterjee N, Walker GC. Mechanisms of DNA damage, repair, and mutagenesis. Environ Mol Mutagen, 2017, 58(5): 235-263.
[2] Olave MC, Graham RP. Mismatch repair deficiency: the what, how and why it is important. Genes Chromosomes Cancer, 2022, 61(6): 314-321.
[3] Lenhart JS, Pillon MC, Guarné A, Biteen JS, Simmons LA. Mismatch repair in Gram-positive bacteria. Res Microbiol, 2016, 167(1): 4-12.
[4] Dos Vultos T, Mestre O, Tonjum T, Gicquel B. DNA repair in Mycobacterium tuberculosis revisited. FEMS Microbiol Rev, 2009, 33(3): 471-487.
[5] Fishel R. Mismatch repair. J Biol Chem, 2015, 290(44): 26395-26403.
[6] Hsieh P, Yamane K. DNA mismatch repair: molecular mechanism, cancer, and ageing. Mech Ageing Dev, 2008, 129(7-8): 391-407.
[7] Putnam CD. Evolution of the methyl directed mismatch repair system in Escherichia coli. DNA Repair (Amst), 2016, 38: 32-41.
[8] Barras F, Marinus MG. The great GATC: DNA methylation in E. coli. Trends Genet, 1989, 5(5): 139-43.
[9] Hu CK, Zhao YQ, Sun HY, Yang YX.Synergism of Dam, MutH, and MutS in methylation-directed mismatch repair in Escherichia coli. Mutat Res, 2017, 795: 31-33.
[10] Groothuizen FS, Sixma TK. The conserved molecular machinery in DNA mismatch repair enzyme structures. DNA Repair (Amst), 2016, 38: 14-23.
[11] Junop MS, Yang W, Funchain P, Clendenin W, Miller JH. In vitro and in vivo studies of MutS, MutL and MutH mutants: correlation of mismatch repair and DNA recombination. DNA Repair (Amst), 2003, 2(4): 387-405.
[12] Jeong C, Cho WK, Song KM, Cook C, Yoon TY, Ban C, Fishel R, Lee JB. MutS switches between two fundamentally distinct clamps during mismatch repair. Nat Struct Mol Biol, 2011, 18(3): 379-385.
[13] Au KG, Welsh K, Modrich P. Initiation of methyl-directed mismatch repair. J Biol Chem, 1992, 267(17): 12142-12148.
[14] Yamaguchi M, Dao V, Modrich P. MutS and MutL activate DNA helicase II in a mismatch-dependent manner. J Biol Chem, 1998, 273(15): 9197-9201.
[15] Grilley M, Griffith J, Modrich P. Bidirectional excision in methyl-directed mismatch repair. J Biol Chem, 1993, 268(16): 11830-11837.
[16] Modrich P, Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem, 1996, 65: 101-133.
[17] Hsieh P. Molecular mechanisms of DNA mismatch repair. Mutat Res, 2001, 486(2): 71-87.
[18] Liu DK, Keijzers G, Rasmussen LJ. DNA mismatch repair and its many roles in eukaryotic cells. Mutat Res Rev Mutat Res, 2017, 773: 174-187.
[19] Schroering AG, Edelbrock MA, Richards TJ, Williams KJ. The cell cycle and DNA mismatch repair. Exp Cell Res, 2007, 313(2): 292-304.
[20] Iyer RR, Pluciennik A, Burdett V, Modrich PL. DNA mismatch repair: functions and mechanisms. Chem Rev, 2006, 106(2): 302-323.
[21] McCulloch SD, Gu LY, Li GM. Bi-directional processing of DNA loops by mismatch repair-dependent and -independent pathways in human cells. J Biol Chem, 2003, 278(6): 3891-3896.
[22] Manhart CM, Alani E. Roles for mismatch repair family proteins in promoting meiotic crossing over. DNA Repair (Amst), 2016, 38: 84-93.
[23] Plotz G, Raedle J, Brieger A, Trojan J, Zeuzem S. hMutSalpha forms an ATP-dependent complex with hMutLalpha and hMutLbeta on DNA. Nucleic Acids Res, 2002, 30(3): 711-718.
[24] Kadyrov FA, Dzantiev L, Constantin N, Modrich P. Endonucleolytic function of MutLalpha in human mismatch repair. Cell, 2006, 126(2): 297-308.
[25] Tran PT, Erdeniz N, Symington LS, Liskay RM. EXO1-A multi-tasking eukaryotic nuclease. DNA Repair (Amst), 2004, 3(12): 1549-1559.
[26] Nielsen FC, J?ger AC, Lützen A, Bundgaard JR, Rasmussen LJ. Characterization of human exonuclease 1 in complex with mismatch repair proteins, subcellular localization and association with PCNA. Oncogene, 2004, 23(7): 1457-1468.
[27] Longley MJ, Pierce AJ, Modrich P. DNA polymerase delta is required for human mismatch repair in vitro. J Biol Chem, 1997, 272(16): 10917-10921.
[28] Ban C, Junop M, Yang W. Transformation of MutL by ATP binding and hydrolysis: a switch in DNA mismatch repair. Cell, 1999, 97(1): 85-97.
[29] Mizrahi V, Andersen SJ. DNA repair in Mycobacterium tuberculosis. What have we learnt from the genome sequence?. Mol Microbiol, 1998, 29(6): 1331-1339.
[30] Ren B, Kühn J, Meslet-Cladiere L, Briffotaux J, Norais C, Lavigne R, Flament D, Ladenstein R, Myllykallio H. Structure and function of a novel endonuclease acting on branched DNA substrates. EMBO J, 2009, 28(16): 2479-2489.
[31] Casta?eda-García A, Prieto AI, Rodríguez-Beltrán J, Alonso N, Cantillon D, Costas C, Pérez-Lago L, Zegeye ED, Herranz M, Plociński P, Tonjum T, García de Viedma D, Paget M, Waddell SJ, Rojas AM, Doherty AJ, Blázquez J. A non-canonical mismatch repair pathway in prokaryotes. Nat Commun, 2017, 8: 14246.
[32] Meslet-Cladiére L, Norais C, Kuhn J, Briffotaux J, Sloostra JW, Ferrari E, Hübscher U, Flament D, Myllykallio H. A novel proteomic approach identifies new interaction partners for proliferating cell nuclear antigen. J Mol Biol, 2007, 372(5): 1137-1148.
[33] Ishino S, Nishi Y, Oda S, Uemori T, Sagara T, Takatsu N, Yamagami T, Shirai T, Ishino Y. Identification of a mismatch-specific endonuclease in hyperthermophilic Archaea. Nucleic Acids Res, 2016, 44(7): 2977-2986.
[34] Cebrián-Sastre E, Martín-Blecua I, Gullón S, Blázquez J, Casta?eda-García A. Control of genome stability by EndoMS/NucS-mediated non-canonical mismatch repair. Cells, 2021, 10(6): 1314.
[35] Nakae S, Hijikata A, Tsuji T, Yonezawa K, Kouyama KI, Mayanagi K, Ishino S, Ishino Y, Shirai T. Structure of the EndoMS-DNA complex as mismatch restriction endonuclease. Structure, 2016, 24(11): 1960-1971.
[36] Pingoud A, Fuxreiter M, Pingoud V, Wende W. Type II restriction endonucleases: structure and mechanism. Cell Mol Life Sci, 2005, 62(6): 685-707.
[37] Takemoto N, Numata I, Su'etsugu M, Miyoshi-Akiyama T. Bacterial EndoMS/NucS acts as a clamp-mediated mismatch endonuclease to prevent asymmetric accumulation of replication errors. Nucleic Acids Res, 2018, 46(12): 6152-6165.
[38] Kunkel TA, Bebenek K. DNA replication fidelity. Annu Rev Biochem, 2000, 69: 497-529.
[39] Xie ZH. The fidelity mechanism of DNA synthesis. Hereditas(Beijing), 2012, 34(6): 679-686.
[39] 谢兆辉. DNA合成的忠实性机制. 遗传, 2012, 34(6): 679-686.
[40] Rock JM, Lang UF, Chase MR, Ford CB, Gerrick ER, Gawande R, Coscolla M, Gagneux S, Fortune SM, Lamers MH. DNA replication fidelity in Mycobacterium tuberculosis is mediated by an ancestral prokaryotic proofreader. Nat Genet, 2015, 47(6): 677-681.
[41] Grabowski B, Kelman Z. Archeal DNA replication: eukaryal proteins in a bacterial context. Annu Rev Microbiol, 2003, 57: 487-516.
[42] Creze C, Ligabue A, Laurent S, Lestini R, Laptenok SP, Khun J, Vos MH, Czjzek M, Myllykallio H, Flament D. Modulation of the Pyrococcus abyssi NucS endonuclease activity by replication clamp at functional and structural levels. J Biol Chem, 2012, 287(19): 15648-15660.
[43] Ishino S, Skouloubris S, Kudo H l'Hermitte-Stead C, Es-Sadik A, Lambry JC, Ishino Y, Myllykallio H. Activation of the mismatch-specific endonuclease EndoMS/NucS by the replication clamp is required for high fidelity DNA replication. Nucleic Acids Res, 2018, 46(12): 6206-6217.
[44] Casta?eda-García A, Martín-Blecua I, Cebrián-Sastre E, Chiner-Oms A, Torres-Puente M, Comas I, Blázquez J. Specificity and mutagenesis bias of the mycobacterial alternative mismatch repair analyzed by mutation accumulation studies. Sci Adv, 2020, 6(7): eaay4453.
[45] Garibyan L, Huang T, Kim M, Wolff E, Nguyen A, Nguyen T, Diep A, Hu K, Iverson A, Yang H, Miller JH. Use of the rpoB gene to determine the specificity of base substitution mutations on the Escherichia coli chromosome. DNA Repair (Amst), 2003, 2(5): 593-608.
[46] Schofield MJ, Hsieh P. DNA mismatch repair: molecular mechanisms and biological function. Annu Rev Microbiol, 2003, 57: 579-608.
[47] Tham KC, Kanaar R, Lebbink JHG. Mismatch repair and homeologous recombination. DNA Repair (Amst), 2016, 38: 75-83.
[48] Tham KC, Hermans N, Winterwerp HHK, Cox MM, Wyman C, Kanaar R, Lebbink JHG. Mismatch repair inhibits homeologous recombination via coordinated directional unwinding of trapped DNA structures. Mol Cell, 2013, 51(3): 326-337.
[49] Worth L Jr, Clark S, Radman M, Modrich P. Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs. Proc Natl Acad Sci USA, 1994, 91(8): 3238-3241.
[50] Spies M, Fishel R. Mismatch repair during homologous and homeologous recombination. Cold Spring Harb Perspect Biol, 2015, 7(3): a022657.
[51] Matic I, Radman M, Taddei F, Picard B, Doit C, Bingen E, Denamur E, Elion J. Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science, 1997, 277(5333): 1833-1834.
[52] Taddei F, Radman M, Maynard-Smith J, Toupance B, Gouyon PH, Godelle B. Role of mutator alleles in adaptive evolution. Nature, 1997, 387(6634): 700-702.
[53] Gutierrez A, Laureti L, Crussard S, Abida H, Rodríguez- Rojas A, Blázquez J, Baharoglu Z, Mazel D, Darfeuille F, Vogel J, Matic I. β-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat Commun, 2013, 4: 1610.
[54] Oliver A, Mena A. Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin Microbiol Infect, 2010, 16(7): 798-808.
[55] Gagneux S. Ecology and evolution of Mycobacterium tuberculosis. Nat Rev Microbiol, 2018, 16(4): 202-213.
[56] Ford CB, Shah RR, Maeda MK, Gagneux S, Murray MB, Cohen T, Johnston JC, Gardy J, Lipsitch M, Fortune SM. Mycobacterium tuberculosis mutation rate estimates from different lineages predict substantial differences in the emergence of drug-resistant tuberculosis. Nat Genet, 2013, 45(7): 784-790.
[57] Fressatti Cardoso R, Martín-Blecua I, Pietrowski Baldin V, Meneguello JE, Valverde JR, Blázquez J, Casta?eda-García A. Noncanonical mismatch repair protein NucS modulates the emergence of antibiotic resistance in Mycobacterium abscessus. Microbiol Spectr, 2022, 10(6): e0222822.
[58] Daley CL, Iaccarino JM, Lange C, Cambau E, Wallace RJ Jr, Andrejak C, B?ttger EC, Brozek J, Griffith DE, Guglielmetti L, Huitt GA, Knight SL, Leitman P, Marras TK, Olivier KN, Santin M, Stout JE, Tortoli E, van Ingen J, Wagner D, Winthrop KL. Treatment of nontuberculous mycobacterial pulmonary disease: an official ATS/ERS/ESCMID/IDSA clinical practice guideline. Eur Respir J, 2020, 56(1): 2000535.
[59] Boshoff HI, Myers TG, Copp BR, McNeil MR, Wilson MA, Barry CE 3rd. The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J Biol Chem, 2004, 279(38): 40174-40184.
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