Nuclear reorganization of DNA mismatch repair proteins in response to DNA damage

DNA Repair

Volumn 9, Issue 2, 2010, Pages 120-133

  Mastrocola, Adam S ^a   Heinen, Christopher D ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Cell cycle; Chromatin; DNA mismatch repair; DNA replication; hMSH2 hMSH6; Nucleolus

Indexed keywords

ALKYLATING AGENT; CYCLINE; MISMATCH REPAIR PROTEIN; PROTEIN MLH1; PROTEIN MSH2; SMALL INTERFERING RNA;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL POPULATION; CELL SYNCHRONIZATION; CHROMATIN; COMPLEX FORMATION; CONFOCAL IMMUNOFLUORESCENCE; CONTROLLED STUDY; DNA ALKYLATION; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA RESPONSIVE ELEMENT; HELA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MISMATCH REPAIR; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL CYCLE; CELL NUCLEUS; CHROMATIN; DNA DAMAGE; DNA MISMATCH REPAIR; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; METHYLNITRONITROSOGUANIDINE; MICROSCOPY, CONFOCAL; MUTS HOMOLOG 2 PROTEIN; NUCLEAR PROTEINS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BINDING; PROTEIN TRANSPORT; S PHASE;

EID: 75149143337     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2009.11.003     Document Type: Article

References (64)

1. Li G.M. Mechanisms and functions of DNA mismatch repair. Cell Res. 18 (2008) 85-98
2. Cannavo E., Marra G., Sabates-Bellver J., Menigatti M., Lipkin S.M., Fischer F., Cejka P., and Jiricny J. Expression of the MutL homologue hMLH3 in human cells and its role in DNA mismatch repair. Cancer Res. 65 (2005) 10759-10766
3. Bielas J.H., and Loeb L.A. Mutator phenotype in cancer: timing and perspectives. Environ. Mol. Mutagen. 45 (2005) 206-213
4. Fishel R., Lescoe M.K., Rao M.R., Copeland N.G., Jenkins N.A., Garber J., Kane M., and Kolodner R. The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75 (1993) 1027-1038
5. Leach F.S., Nicolaides N.C., Papadopoulos N., Liu B., Jen J., Parsons R., Peltomaki P., Sistonen P., Aaltonen L.A., Nystrom-Lahti M., et al. Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell 75 (1993) 1215-1225
6. Papadopoulos N., Nicolaides N.C., Wei Y.F., Ruben S.M., Carter K.C., Rosen C.A., Haseltine W.A., Fleischmann R.D., Fraser C.M., Adams M.D., et al. Mutation of a mutL homolog in hereditary colon cancer. Science 263 (1994) 1625-1629
7. Constantin N., Dzantiev L., Kadyrov F.A., and Modrich P. Human mismatch repair: reconstitution of a nick-directed bidirectional reaction. J. Biol. Chem. 280 (2005) 39752-39761
8. Dzantiev L., Constantin N., Genschel J., Iyer R.R., Burgers P.M., and Modrich P. A defined human system that supports bidirectional mismatch-provoked excision. Mol. Cell 15 (2004) 31-41
9. Zhang Y., Yuan F., Presnell S.R., Tian K., Gao Y., Tomkinson A.E., Gu L., and Li G.M. Reconstitution of 5′-directed human mismatch repair in a purified system. Cell 122 (2005) 693-705
10. Fishel R. Mismatch repair, molecular switches, and signal transduction. Genes Dev. 12 (1998) 2096-2101
11. Gradia S., Acharya S., and Fishel R. The human mismatch recognition complex hMSH2-hMSH6 functions as a novel molecular switch. Cell 91 (1997) 995-1005
12. Gradia S., Subramanian D., Wilson T., Acharya S., Makhov A., Griffith J., and Fishel R. hMSH2-hMSH6 forms a hydrolysis-independent sliding clamp on mismatched DNA. Mol. Cell 3 (1999) 255-261
13. Heinen C.D., Wilson T., Mazurek A., Berardini M., Butz C., and Fishel R. HNPCC mutations in hMSH2 result in reduced hMSH2-hMSH6 molecular switch functions. Cancer Cell 1 (2002) 469-478
14. Acharya S., Foster P.L., Brooks P., and Fishel R. The coordinated functions of the E. coli MutS and MutL proteins in mismatch repair. Mol. Cell 12 (2003) 233-246
15. Gu L., Hong Y., McCulloch S., Watanabe H., and Li G.M. ATP-dependent interaction of human mismatch repair proteins and dual role of PCNA in mismatch repair. Nucleic Acids Res. 26 (1998) 1173-1178
16. Plotz G., Raedle J., Brieger A., Trojan J., and Zeuzem S. hMutSalpha forms an ATP-dependent complex with hMutLalpha and hMutLbeta on DNA. Nucleic Acids Res. 30 (2002) 711-718
17. Plotz G., Raedle J., Brieger A., Trojan J., and Zeuzem S. N-terminus of hMLH1 confers interaction of hMutLalpha and hMutLbeta with hMutSalpha. Nucleic Acids Res. 31 (2003) 3217-3226
18. Matton N., Simonetti J., and Williams K. Identification of mismatch repair protein complexes in HeLa nuclear extracts and their interaction with heteroduplex DNA. J. Biol. Chem. 275 (2000) 17808-17813
19. Kleczkowska H.E., Marra G., Lettieri T., and Jiricny J. hMSH3 and hMSH6 interact with PCNA and colocalize with it to replication foci. Genes Dev. 15 (2001) 724-736
20. Shell S.S., Putnam C.D., and Kolodner R.D. The N terminus of Saccharomyces cerevisiae Msh6 is an unstructured tether to PCNA. PNAS 104 (2007) 10956-10961
21. Clark A.B., Valle F., Drotschmann K., Gary R.K., and Kunkel T.A. Functional interaction of proliferating cell nuclear antigen with MSH2-MSH6 and MSH2-MSH3 complexes. J. Biol. Chem. 275 (2000) 36498-36501
22. Flores-Rozas H., Clark D., and Kolodner R.D. Proliferating cell nuclear antigen and Msh2p-Msh6p interact to form an active mispair recognition complex. Nat. Genet. 26 (2000) 375-378
23. Lee S.D., and Alani E. Analysis of interactions between mismatch repair initiation factors and the replication processivity factor PCNA. J. Mol. Biol. 355 (2006) 175-184
24. Schroering A.G., and Williams K.J. Rapid induction of chromatin-associated DNA mismatch repair proteins after MNNG treatment. DNA Repair (Amst.) 7 (2008) 951-969
25. Umar A., Buermeyer A.B., Simon J.A., Thomas D.C., Clark A.B., Liskay R.M., and Kunkel T.A. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell 87 (1996) 65-73
26. Stojic L., Brun R., and Jiricny J. Mismatch repair and DNA damage signalling. DNA Repair 3 (2004) 1091-1101
27. Kaina B., Christmann M., Naumann S., and Roos W.P. MGMT: key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair (Amst.) 6 (2007) 1079-1099
28. Duckett D., Drummond J.T., Murchie A.I., Reardon J.T., Sancar A., Lilley D.M., and 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. 93 (1996) 6443-6447
29. Mojas N., Lopes M., and Jiricny J. Mismatch repair-dependent processing of methylation damage gives rise to persistent single-stranded gaps in newly replicated DNA. Genes Dev. 21 (2007) 3342-3355
30. Stojic L., Mojas N., Cejka P., di Pietro M., Ferrari S., Marra G., and Jiricny J. Mismatch repair-dependent G2 checkpoint induced by low doses of SN1 type methylating agents requires the ATR kinase. Genes Dev. 18 (2004) 1331-1344
31. Karran P. Mechanisms of tolerance to DNA damaging therapeutic drugs. Carcinogenesis 22 (2001) 1931-1937
32. Schroering A.G., Kothandapani A., Patrick S.M., Kaliyaperumal S., Sharma V.P., and Williams K.J. Prolonged cell cycle response of HeLa cells to low-level alkylation exposure. Cancer Res. 69 (2009) 6307-6314
33. Bostock C.J., Prescott D.M., and Kirkpatrick J.B. An evaluation of the double thymidine block for synchronizing mammalian cells at the G1-S border. Exp. Cell Res. 68 (1971) 163-168
34. Watanabe Y., Haugen-Strano A., Umar A., Yamada K., Hemmi H., Kikuchi Y., Takano S., Shibata Y., Barrett J.C., Kunkel T.A., and Koi M. Complementation of an hMSH2 defect in human colorectal carcinoma cells by human chromosome 2 transfer. Mol. Carcinog. 29 (2000) 37-49
35. Yoshioka K., Yoshioka Y., and Hsieh P. ATR kinase activation mediated by MutSa and MutLa in response to cytotoxic O6-methylguanine adducts. Mol. Cell 22 (2006) 501-510
36. O'Brien V., and Brown R. Signalling cell cycle arrest and cell death through the MMR System. Carcinogenesis 27 (2006) 682-692
37. Moldovan G.-L., Pfander B., and Jentsch S. PCNA, the maestro of the replication fork. Cell 129 (2007) 665-679
38. Knudsen N.O., Nielsen F.C., Vinther L., Bertelsen R., Holten-Andersen S., Liberti S.E., Hofstra R., Kooi K., and Rasmussen L.J. Nuclear localization of human DNA mismatch repair protein exonuclease 1 (hEXO1). Nucleic Acids Res. 35 (2007) 2609-2619
39. Stojic L.C.P., and Jiricny J. High doses of SN1 type methylating agents activate DNA damage signaling cascades that are largely independent of mismatch repair. Cell Cycle 4 (2005) 473-477
40. Marra G., Iaccarino I., Lettieri T., Roscilli G., Delmastro P., and Jiricny J. Mismatch repair deficiency associated with overexpression of the MSH3 gene. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 8568-8573
41. Junop M.S., Obmolova G., Rausch K., Hsieh P., and Yang W. Composite active site of an ABC ATPase: MutS uses ATP to verify mismatch recognition and authorize DNA repair. Mol. Cell 7 (2001) 1-12
42. Allen D.J., Makhov A., Grilley M., Taylor J., Thresher R., Modrich P., and Griffith J.D. MutS mediates heteroduplex loop formation by a translocation mechanism. EMBO J. 16 (1997) 4467-4476
43. Hidaka M., Takagi Y., Takano T.Y., and Sekiguchi M. PCNA-MutS{alpha}-mediated binding of MutL{alpha} to replicative DNA with mismatched bases to induce apoptosis in human cells. Nucleic Acids Res. 33 (2005) 5703-5712
44. Lau P.J., and Kolodner R.D. Transfer of the MSH2-MSH6 complex from proliferating cell nuclear antigen to mispaired bases in DNA. J. Biol. Chem. 278 (2003) 14-17
45. Goldmacher V.S., Cuzick Jr. R.A., and 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. 261 (1986) 12462-12471
46. York S.J., and Modrich P. Mismatch repair-dependent iterative excision at irreparable O6-methylguanine lesions in human nuclear extracts. J. Biol. Chem. 281 (2006) 22674-22683
47. Cejka P., Mojas N., Gillet L., Schär P., and Jiricny J. Homologous recombination rescues mismatch-repair-dependent cytotoxicity of SN1-type methylating agents in S. cerevisiae. Curr. Biol. 15 (2005) 1395-1400
48. Fishel R. Signaling mismatch repair in cancer. Nat. Med. 5 (1999) 1239-1241
49. Kat A., Thilly W.G., Fang W.H., Longley M.J., Li G.M., and Modrich P. An alkylation-tolerant, mutator human cell line is deficient in strand-specific mismatch repair. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 6424-6428
50. Wang Y., and 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. 100 (2003) 15387-15392
51. Warren J.J., Pohlhaus T.J., Changela A., Iyer R.R., Modrich P.L., and Beese L.S. Structure of the human MutSalpha DNA lesion recognition complex. Mol. Cell 26 (2007) 579-592
52. Berardini M., Mazurek A., and Fishel R. The effect of O6-methylguanine DNA adducts on the adenosine nucleotide switch functions of hMSH2-hMSH6 and hMSH2-hMSH3. J. Biol. Chem. 275 (2000) 27851-27857
53. 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., and Edelmann W. An Msh2 point mutation uncouples DNA mismatch repair and apoptosis. Cancer Res. 64 (2004) 517-522
54. Yang G., Scherer S.J., Shell S.S., Yang K., Kim M., Lipkin M., Kucherlapati R., Kolodner R.D., and Edelmann W. Dominant effects of an Msh6 missense mutation on DNA repair and cancer susceptibility. Cancer Cell 6 (2004) 139-150
55. Adamson A., Beardsley D., Kim W., Gao Y., Baskaran R., and Brown K. Methylator-induced, mismatch repair-dependent G2 arrest is activated through Chk1 and Chk2. Mol. Biol. Cell 16 (2005) 1513-1526
56. Brown K.D., Rathi A., Kamath R., Beardsley D.I., Zhan Q., Mannino J.L., and Baskaran R. The mismatch repair system is required for S-phase checkpoint activation. Nat. Genet. 33 (2002) 80-84
57. Dart D.A., Adams K.E., Akerman I., and Lakin N.D. Recruitment of the cell cycle checkpoint kinase ATR to chromatin during S-phase. J. Biol. Chem. 279 (2004) 16433-16440
58. Jiang K., Pereira E., Maxfield M., Russell B., Goudelock D.M., and Sanchez Y. Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J. Biol. Chem. 278 (2003) 25207-25217
59. Wilsker D., Petermann E., Helleday T., and Bunz F. Essential function of Chk1 can be uncoupled from DNA damage checkpoint and replication control. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 20752-20757
60. Zhang Y.-W., Otterness D., Chiang G., Xie W., Liu Y.-C., Mercurio F., and Abraham R. Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol. Cell 19 (2005) 607-618
61. Hsieh P., and Yamane K. DNA mismatch repair: molecular mechanism, cancer, and ageing. Mech. Ageing Dev. 129 (2008) 391-407
62. Sirri V., Urcuqui-Inchima S., Roussel P., and Hernandez-Verdun D. Nucleolus: the fascinating nuclear body. Histochem. Cell Biol. 129 (2008) 13-31
63. Bernardi R., Scaglioni P.P., Bergmann S., Horn H.F., Vousden K.H., and Pandolfi P.P. PML regulates p53 stability by sequestering Mdm2 to the nucleolus. Nat. Cell Biol. 6 (2004) 665-672
64. Ahmad Y., Boisvert F.M., Gregor P., Cobley A., and Lamond A.I. NOPdb: nucleolar proteome database-2008 update. Nucleic Acids Res. 37 (2009) D181-184