Exonuclease 1 (Exo1) is required for activating response to SN1 DNA methylating agents

DNA Repair

Volumn 11, Issue 12, 2012, Pages 951-964

  Izumchenko, Eugene ^a   Saydi, John ^a   Brown, Kevin D ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Cell cycle checkpoints; DNA damage response; Mismatch repair

Indexed keywords

6 O METHYLGUANINE; BETA TUBULIN; CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE 1; DOUBLE STRANDED DNA; EXONUCLEASE; EXONUCLEASE 1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HISTONE H2AX; HISTONE H2AX GAMMA; METHYLNITRONITROSOGUANIDINE; NUCLEASE; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH6; THYMINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL PROLIFERATION; CELL VIABILITY; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE; DNA METHYLATION; DNA REPLICATION; EMBRYO; ENZYME LOCALIZATION; GENE; GENOTOXICITY; IN VITRO STUDY; IN VIVO STUDY; MEXO1 GENE; MISMATCH REPAIR; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; WILD TYPE;

ALKYLATING AGENTS; ANIMALS; BASE PAIR MISMATCH; CELL PROLIFERATION; CELL SURVIVAL; CHROMATIN; CLONING, MOLECULAR; DNA METHYLATION; DNA MISMATCH REPAIR; DNA REPAIR ENZYMES; DNA, COMPLEMENTARY; EXODEOXYRIBONUCLEASES; FIBROBLASTS; G2 PHASE CELL CYCLE CHECKPOINTS; GENETIC VECTORS; HISTONES; HUMANS; METHYLNITRONITROSOGUANIDINE; MICE; MUTAGENESIS, SITE-DIRECTED; MUTS HOMOLOG 2 PROTEIN; PROTEIN INTERACTION MAPPING; PROTEIN KINASES; RECOMBINANT PROTEINS; RNA INTERFERENCE; TRANSFECTION;

EID: 84869162567     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2012.09.004     Document Type: Article

References (86)

1. Bignami M., O'Driscoll M., Aquilina G., Karran P. Unmasking a killer: DNA O(6)-methylguanine and the cytotoxicity of methylating agents. Mutat. Res. 2000, 462:71-82.
2. Gerson S.L. MGMT: its role in cancer aetiology and cancer therapeutics. Nat. Rev. Cancer 2004, 4:296-307.
3. Lindahl T., Demple B., Robins P. Suicide inactivation of the E. coli O6-methylguanine-DNA methyltransferase. EMBO J. 1982, 1:1359-1363.
4. Eadie J.S., Conrad M., Toorchen D., Topal M.D. Mechanism of mutagenesis by O6-methylguanine. Nature 1984, 308:201-203.
5. Modrich P., Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu. Rev. Biochem. 1996, 65:101-133.
6. Kolodner R.D., Marsischky G.T. Eukaryotic DNA mismatch repair. Curr. Opin. Genet. Dev. 1999, 9:89-96.
7. Lynch H.T., Smyrk T., Lynch J.F. Overview of natural history, pathology, molecular genetics and management of HNPCC (Lynch Syndrome). Int. J. Cancer 1996, 69:38-43.
8. Duckett D.R., Drummond J.T., Murchie A.I., Reardon J.T., Sancar A., Lilley D.M., Modrich P. Human MutSalpha recognizes damaged DNA base pairs containing O6-methylguanine, O4-methylthymine, or the cisplatin-d(GpG) adduct. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:6443-6447.
9. Stojic L., Brun R., Jiricny J. Mismatch repair and DNA damage signalling. DNA Repair (Amst.) 2004, 3:1091-1101.
10. Aquilina G., Zijno A., Moscufo N., Dogliotti E., Bignami M. Tolerance to methylnitrosourea-induced DNA damage is associated with 6-thioguanine resistance in CHO cells. Carcinogenesis 1989, 10:1219-1223.
11. Goldmacher V.S., Cuzick R.A., Thilly W.G. Isolation and partial characterization of human cell mutants differing in sensitivity to killing and mutation by methylnitrosourea and N-methyl-N'-nitro-N-nitrosoguanidine. J. Biol. Chem. 1986, 261:12462-12471.
12. Kat A., Thilly W.G., Fang W.H., Longley M.J., Li G.M., Modrich P. An alkylation-tolerant, mutator human cell line is deficient in strand-specific mismatch repair. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:6424-6428.
13. Koi M., Umar A., Chauhan D.P., Cherian S.P., Carethers J.M., Kunkel T.A., Boland C.R. Human chromosome 3 corrects mismatch repair deficiency and microsatellite instability and reduces N-methyl-N'-nitro-N-nitrosoguanidine tolerance in colon tumor cells with homozygous hMLH1 mutation. Cancer Res. 1994, 54:4308-4312.
14. Aquilina G., Biondo R., Dogliotti E., Bignami M. Genetic consequences of tolerance to methylation DNA damage in mammalian cells. Carcinogenesis 1993, 14:2097-2103.
15. Adamson A.W., Beardsley D.I., Kim W.J., Gao Y., Baskaran R., Brown K.D. Methylator-induced, mismatch repair-dependent G2 arrest is activated through Chk1 and Chk2. Mol. Biol. Cell 2005, 16:1513-1526.
16. Beardsley D.I., Kim W.J., Brown K.D. N-methyl-N'-nitro-N-nitrosoguanidine activates cell-cycle arrest through distinct mechanisms activated in a dose-dependent manner. Mol. Pharmacol. 2005, 68:1049-1060.
17. Stojic L., Cejka P., Jiricny J. High doses of SN1 type methylating agents activate DNA damage signaling cascades that are largely independent of mismatch repair. Cell Cycle 2005, 4:473-477.
18. Stojic L., Mojas N., Cejka P., Di Pietro M., Ferrari S., Marra G., Jiricny J. Mismatch repair-dependent G2 checkpoint induced by low doses of SN1 type methylating agents requires the ATR kinase. Genes Dev. 2004, 18:1331-1344.
19. Yoshioka K., Yoshioka Y., Hsieh P. ATR kinase activation mediated by MutSalpha and MutLalpha in response to cytotoxic O6-methylguanine adducts. Mol. Cell 2006, 22:501-510.
20. Yamane K., Taylor K., Kinsella T.J. Mismatch repair-mediated G2/M arrest by 6-thioguanine involves the ATR-Chk1 pathway. Biochem. Biophys. Res. Commun. 2004, 318:297-302.
21. Wang J.Y., Edelmann W. Mismatch repair proteins as sensors of alkylation DNA damage. Cancer Cell 2006, 9:417-418.
22. York S.J., Modrich P. Mismatch repair-dependent iterative excision at irreparable O6-methylguanine lesions in human nuclear extracts. J. Biol. Chem. 2006, 281:22674-22683.
23. Wang Y., Qin J. MSH2 and ATR form a signaling module and regulate two branches of the damage response to DNA methylation. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:15387-15392.
24. Lin D.P., Wang Y., Scherer S.J., Clark A.B., Yang K., Avdievich E., Jin B., Werling U., Parris T., Kurihara N., Umar A., Kucherlapati R., Lipkin M., Kunkel T.A., Edelmann W. An Msh2 point mutation uncouples DNA mismatch repair and apoptosis. Cancer Res. 2004, 64:517-522.
25. Lieber M.R. The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair. Bioessays 1997, 19:233-240.
26. Lee B.I., Wilson D.M. The RAD2 domain of human exonuclease 1 exhibits 5' to 3' exonuclease and flap structure-specific endonuclease activities. J. Biol. Chem. 1999, 274:37763-37769.
27. Genschel J., Modrich P. Mechanism of 5'-directed excision in human mismatch repair. Mol. Cell 2003, 12:1077-1086.
28. Genschel J., Bazemore L.R., Modrich P. Human exonuclease I is required for 5' and 3' mismatch repair. J. Biol. Chem. 2002, 277:13302-13311.
29. Tishkoff D.X., Boerger A.L., Bertrand P., Filosi N., Gaida G.M., Kane M.F., Kolodner R.D. Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:7487-7492.
30. Tran P.T., Fey J.P., Erdeniz N., Gellon L., Boiteux S., Liskay R.M. A mutation in EXO1 defines separable roles in DNA mismatch repair and post-replication repair. DNA Repair (Amst.) 2007, 6:1572-1583.
31. Sokolsky T., Alani E. EXO1 and MSH6 are high-copy suppressors of conditional mutations in the MSH2 mismatch repair gene of Saccharomyces cerevisiae. Genetics 2000, 155:589-599.
32. Rudolph C., Fleck O., Kohli J. Schizosaccharomyces pombe exo1 is involved in the same mismatch repair pathway as msh2 and pms1. Curr. Genet. 1998, 34:343-350.
33. Wei K., Clark A.B., Wong E., Kane M.F., Mazur D.J., Parris T., Kolas N.K., Russell R., Hou H., Kneitz B., Yang G., Kunkel T.A., Kolodner R.D., Cohen P.E., Edelmann W. Inactivation of exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev. 2003, 17:603-614.
34. Harris R.S., Ross K.J., Lombardo M.J., Rosenberg S.M. Mismatch repair in Escherichia coli cells lacking single-strand exonucleases ExoI, ExoVII, and RecJ. J. Bacteriol. 1998, 180:989-993.
35. Viswanathan M., Lovett S.T. Single-strand DNA-specific exonucleases in Escherichia coli. Roles in repair and mutation avoidance. Genetics 1998, 149:7-16.
36. Viswanathan M., Lovett S.T., Exonuclease X of Escherichia coli. A novel 3'-5' DNase and Dnaq superfamily member involved in DNA repair. J. Biol. Chem. 1999, 274:30094-30100.
37. Burdett V., Baitinger C., Viswanathan M., Lovett S.T., Modrich P. In vivo requirement for RecJ, ExoVII, ExoI, and ExoX in methyl-directed mismatch repair. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:6765-6770.
38. Constantin N., Dzantiev L., Kadyrov F.A., Modrich P. Human mismatch repair: reconstitution of a nick-directed bidirectional reaction. J. Biol. Chem. 2005, 280:39752-39761.
39. Kadyrov F.A., Genschel J., Fang Y., Penland E., Edelmann W., Modrich P. A possible mechanism for exonuclease 1-independent eukaryotic mismatch repair. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:8495-8500.
40. Amin N.S., Nguyen M.N., Oh S., Kolodner R.D. exo1-Dependent mutator mutations: model system for studying functional interactions in mismatch repair. Mol. Cell. Biol. 2001, 21:5142-5155.
41. Schmutte C., Marinescu R.C., Sadoff M.M., Guerrette S., Overhauser J., Fishel R. Human exonuclease I interacts with the mismatch repair protein hMSH2. Cancer Res. 1998, 58:4537-4542.
42. Dherin C., Gueneau E., Francin M., Nunez M., Miron S., Liberti S.E., Rasmussen L.J., Zinn-Justin S., Gilquin B., Charbonnier J.B., Boiteux S. Characterization of a highly conserved binding site of Mlh1 required for exonuclease I-dependent mismatch repair. Mol. Cell. Biol. 2009, 29:907-918.
43. Tishkoff D.X., Amin N.S., Viars C.S., Arden K.C., Kolodner R.D. Identification of a human gene encoding a homologue of Saccharomyces cerevisiae EXO1, an exonuclease implicated in mismatch repair and recombination. Cancer Res. 1998, 58:5027-5031.
44. Nielsen F.C., Jager A.C., Lutzen A., Bundgaard J.R., Rasmussen L.J. Characterization of human exonuclease 1 in complex with mismatch repair proteins, subcellular localization and association with PCNA. Oncogene 2004, 23:1457-1468.
45. Tran P.T., Erdeniz N., Symington L.S., Liskay R.M. EXO1-A multi-tasking eukaryotic nuclease. DNA Repair (Amst.) 2004, 3:1549-1559.
46. Jager A.C., Rasmussen M., Bisgaard H.C., Singh K.K., Nielsen F.C., Rasmussen L.J. HNPCC mutations in the human DNA mismatch repair gene hMLH1 influence assembly of hMutLalpha and hMLH1-hEXO1 complexes. Oncogene 2001, 20:3590-3595.
47. Schmutte C., Sadoff M.M., Shim K.S., Acharya S., Fishel R. The interaction of DNA mismatch repair proteins with human exonuclease I. J. Biol. Chem. 2001, 276:33011-33018.
48. Liberti S.E., Andersen S.D., Wang J., May A., Miron S., Perderiset M., Keijzers G., Nielsen F.C., Charbonnier J.B., Bohr V.A., Rasmussen L.J. Bi-directional routing of DNA mismatch repair protein human exonuclease 1 to replication foci and DNA double strand breaks. DNA Repair (Amst.) 2011, 10:73-86.
49. Tran P.T., Erdeniz N., Dudley S., Liskay R.M. Characterization of nuclease-dependent functions of Exo1p in Saccharomyces cerevisiae. DNA Repair (Amst.) 2002, 1:895-912.
50. Lutzen A., de Wind N., Georgijevic D., Nielsen F.C., Rasmussen L.J. Functional analysis of HNPCC-related missense mutations in MSH2. Mutat. Res. 2008, 645:44-55.
51. Sun X., Zheng L., Shen B. Functional alterations of human exonuclease 1 mutants identified in atypical hereditary nonpolyposis colorectal cancer syndrome. Cancer Res. 2002, 62:6026-6030.
52. Pabla N., Ma Z., McIlhatton M.A., Fishel R., Dong Z. hMSH2 recruits ATR to DNA damage sites for activation during DNA damage-induced apoptosis. J. Biol. Chem. 2011, 286:10411-10418.
53. Guo G., Wang W., Bradley A. Mismatch repair genes identified using genetic screens in Blm-deficient embryonic stem cells. Nature 2004, 429:891-895.
54. Burma S., Chen B.P., Murphy M., Kurimasa A., Chen D.J. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 2001, 276:42462-42467.
55. Dickey J.S., Redon C.E., Nakamura A.J., Baird B.J., Sedelnikova O.A., Bonner W.M. H2AX: functional roles and potential applications. Chromosoma 2009, 118:683-692.
56. Gradia S., Acharya S., Fishel R. The human mismatch recognition complex hMSH2-hMSH6 functions as a novel molecular switch. Cell 1997, 91:995-1005.
57. Marsischky G.T., Kolodner R.D. Biochemical characterization of the interaction between the Saccharomyces cerevisiae MSH2-MSH6 complex and mispaired bases in DNA. J. Biol. Chem. 1999, 274:26668-26682.
58. Segurado M., Diffley J.F. Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forks. Genes Dev. 2008, 22:1816-1827.
59. Nimonkar A.V., Ozsoy A.Z., Genschel J., Modrich P., Kowalczykowski S.C. Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:16906-16911.
60. Dzantiev L., Constantin N., Genschel J., Iyer R.R., Burgers P.M., Modrich P. A defined human system that supports bidirectional mismatch-provoked excision. Mol. Cell 2004, 15:31-41.
61. Stojic L., Cejka P., Jiricny J. High doses of S(N)1 type methylating agents activate DNA damage signaling cascades that are largely independent of mismatch repair. Cell Cycle 2005, 4.
62. Yoshioka K.-I., Yoshioka Y., Hseih P. ATR kinase activation mediated by MutSa and MutLa in response to cytotoxic O6-methylguanine adducts. Mol. Cell 2006, 22:501-510.
63. Klapacz J., Meira L.B., Luchetti D.G., Calvo J.A., Bronson R.T., Edelmann W., Samson L.D. O6-methylguanine-induced cell death involves exonuclease 1 as well as DNA mismatch recognition in vivo. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:576-581.
64. Tomimatsu N., Mukherjee B., Burma S. Distinct roles of ATR and DNA-PKcs in triggering DNA damage responses in ATM-deficient cells. EMBO Rep. 2009, 10:629-635.
65. Giannattasio M., Follonier C., Tourriere H., Puddu F., Lazzaro F., Pasero P., Lopes M., Plevani P., Muzi-Falconi M. Exo1 competes with repair synthesis, converts NER intermediates to long ssDNA gaps, and promotes checkpoint activation. Mol. Cell 2010, 40:50-62.
66. Tomimatsu N., Mukherjee B., Deland K., Kurimasa A., Bolderson E., Khanna K.K., Burma S. Exo1 plays a major role in DNA end resection in humans and influences double-strand break repair and damage signaling decisions. DNA Repair (Amst.) 2012, 11:441-448.
67. Bonner W.M., Redon C.E., Dickey J.S., Nakamura A.J., Sedelnikova O.A., Solier S., Pommier Y. GammaH2AX and cancer. Nat. Rev. Cancer 2008, 8:957-967.
68. Rogakou E.P., Boon C., Redon C., Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 1999, 146:905-916.
69. Kalamegham R., Warmels-Rodenhiser S., MacDonald H., Ebisuzaki K. O6-methylguanine-DNA methyltransferase-defective human cell mutant: O6-methylguanine, DNA strand breaks and cytotoxicity. Carcinogenesis 1988, 9:1749-1753.
70. Rajesh P., Rajesh C., Wyatt M.D., Pittman D.L. RAD51D protects against MLH1-dependent cytotoxic responses to O(6)-methylguanine. DNA Repair (Amst.) 2010, 9:458-467.
71. Banath J.P., Klokov D., MacPhail S.H., Banuelos C.A., Olive P.L. Residual gammaH2AX foci as an indication of lethal DNA lesions. BMC Cancer 2010, 10:4.
72. Staszewski O., Nikolova T., Kaina B. Kinetics of gamma-H2AX focus formation upon treatment of cells with UV light and alkylating agents. Environ. Mol. Mutagen. 2008, 49:734-740.
73. Mirzoeva O.K., Kawaguchi T., Pieper R.O. The Mre11/Rad50/Nbs1 complex interacts with the mismatch repair system and contributes to temozolomide-induced G2 arrest and cytotoxicity. Mol. Cancer Ther. 2006, 5:2757-2766.
74. Bai H., Madabushi A., Guan X., Lu A.L. Interaction between human mismatch repair recognition proteins and checkpoint sensor Rad9-Rad1-Hus1. DNA Repair (Amst.) 2010, 9:478-487.
75. Short S.C., Giampieri S., Worku M., Alcaide-German M., Sioftanos G., Bourne S., Lio K.I., Shaked-Rabi M., Martindale C. Rad51 inhibition is an effective means of targeting DNA repair in glioma models and CD133+ tumor-derived cells. Neuro Oncol. 2011, 13:487-499.
76. Meador J.A., Zhao M., Su Y., Narayan G., Geard C.R., Balajee A.S. Histone H2AX is a critical factor for cellular protection against DNA alkylating agents. Oncogene 2008, 27:5662-5671.
77. Campbell M.R., Wang Y., Andrew S.E., Liu Y. Msh2 deficiency leads to chromosomal abnormalities, centrosome amplification, and telomere capping defect. Oncogene 2006, 25:2531-2536.
78. Edelmann W., Cohen P.E., Kane M., Lau K., Morrow B., Bennett S., Umar A., Kunkel T., Cattoretti G., Chaganti R., Pollard J.W., Kolodner R.D., Kucherlapati R. Meiotic pachytene arrest in MLH1-deficient mice. Cell 1996, 85:1125-1134.
79. Palombo F., Gallinari P., Iaccarino I., Lettieri T., Hughes M., D'Arrigo A., Truong O., Hsuan J.J., Jiricny J. GTBP a 160-kilodalton protein essential for mismatch-binding activity in human cells. Science 1995, 268:1912-1914.
80. Christmann M., Tomicic M.T., Kaina B. Phosphorylation of mismatch repair proteins MSH2 and MSH6 affecting MutSalpha mismatch-binding activity. Nucl. Acids Res. 2002, 30:1959-1966.
81. Cejka P., Mojas N., Gillet L., Schar P., Jiricny J. Homologous recombination rescues mismatch-repair-dependent cytotoxicity of S(N)1-type methylating agents in S. cerevisiae. Curr. Biol. 2005, 15:1395-1400.
82. Christmann M., Kaina B. Nuclear translocation of mismatch repair proteins MSH2 and MSH6 as a response of cells to alkylating agents. J. Biol. Chem. 2000, 275:36256-36262.
83. Schroering A.G., Williams K.J. Rapid induction of chromatin-associated DNA mismatch repair proteins after MNNG treatment. DNA Repair (Amst.) 2008, 7:951-969.
84. Hidaka M., Takagi Y., Takano T.Y., Sekiguchi M. PCNA-MutSalpha-mediated binding of MutLalpha to replicative DNA with mismatched bases to induce apoptosis in human cells. Nucl. Acids Res. 2005, 33:5703-5712.
85. Brown K.D., Rathi A., Kamath R., Beardsley D.I., Zhan Q., Mannino J.L., Baskaran R. The mismatch repair system is required for S-phase checkpoint activation. Nat. Genet. 2003, 33:80-84.
86. Yang G., Scherer S.J., Shell S.S., Yang K., Kim M., Lipkin M., Kucherlapati R., Kolodner R.D., Edelmann W. Dominant effects of an Msh6 missense mutation on DNA repair and cancer susceptibility. Cancer Cell 2004, 6:139-150.