Phosphorylated hMSH6: DNA mismatch versus DNA damage recognition

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 706, Issue 1-2, 2011, Pages 36-45

  Kaliyaperumal, Saravanan ^a   Patrick, Steve M ^a   Williams, Kandace J ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

Alkylation damage; DNA mismatch repair; HMSH6; HMutS ; MMR dependent damage signaling

Indexed keywords

6 O METHYLGUANINE; 7 HYDROXYSTAUROSPORINE; CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE 1; GUANINE; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOSERINE; PROTEIN MSH6; PROTEIN MUTS; PROTEIN TYROSINE PHOSPHATASE; RECOMBINANT PROTEIN; THYMINE;

ANIMAL CELL; ARTICLE; BASE MISPAIRING; CELL CYCLE ARREST; CONTROLLED STUDY; DNA ALKYLATION; DNA DAMAGE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE MUTATION; HELA CELL; HUMAN; HUMAN CELL; INDEL MUTATION; MISMATCH REPAIR; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANIMALS; BASE PAIR MISMATCH; CELL LINE; CELL LINE, TUMOR; DNA; DNA DAMAGE; DNA MISMATCH REPAIR; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HELA CELLS; HUMANS; IMMUNOBLOTTING; MICE; MOLECULAR SEQUENCE DATA; MUTATION; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE INHIBITORS; SERINE; SIGNAL TRANSDUCTION; SPODOPTERA; STAUROSPORINE;

EID: 78650419880     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2010.10.008     Document Type: Article

References (67)

1. Marra G., Boland C.R. Hereditary nonpolyposis colorectal cancer: the syndrome, the genes, and the historical perspectives. J. Natl. Cancer Inst. 1995, 87:1114-1125.
2. Boland C.R. Evolution of the nomenclature for the hereditary colorectal cancer syndromes. Familial Cancer 2005, 4:211-218.
3. 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.
4. Jiricny J. The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell Biol. 2006, 7:335-347.
5. Goel A., Nagasaka T., Hamelin R., Boland C.R. An optimized pentaplex PCR for detecting DNA mismatch repair-deficient colorectal cancers. PLoS One 2010, 5:e9393.
6. Kunkel T.A., Erie D.A. DNA mismatch repair. Annu. Rev. Biochem. 2005, 74:681-710.
7. Buermeyer A.B., Deschenes S.M., Baker S.M., Liskay R.M. Mammalian DNA mismatch repair. Annu. Rev. Genet. 1999, 33:533-564.
8. Modrich P., Lahue R.S. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu. Rev. Biochem. 1996, 65:101-133.
9. Genschel J., Littman S.J., Drummond J.T., Modrich P. Isolation of MutSbeta from human cells and comparison of the mismatch repair specificities of MutSbeta and MutSalpha. J. Biol. Chem. 1998, 273:19895-19901.
10. Dzantiev L., Constantin N., Genschel J., Lyer R.R., Burgers P.M., Modrich P. A defined human system that supports bidirectional mismatch-provoked excision. Mol. Cell 2004, 15:31-41.
11. Genschel J., Modrich P. Analysis of the excision step in human DNA mismatch repair. Methods Enzymol. 2006, 408:273-284.
12. Edelbrock M.E., Kaliyaperumal S., Williams K.J. DNA mismatch repair efficiency and fidelity are elevated during DNA synthesis in human cells. Mut. Res. 2009, 662:59-66.
13. Schroering A.G., Edelbrock M.A., Richards T.J., Williams K.J. The cell cycle and DNA mismatch repair. Exp. Cell Res. 2007, 313:292-304.
14. Schroering A.G., Williams K.J. Rapid induction of chromatin-associated DNA mismatch repair proteins after MNNG treatment. DNA Repair 2008, 7:951-969.
15. Schroering A.G., Kothandapani A., Patrick S.M., Kaliyaperumal S., Sharma V.P., Williams K.J. Prolonged cell cycle response of HeLa cells to low-level alkylation exposure. Cancer Res. 2009, 69:6307-6314.
16. Drablos F., Feyzi E., Aas P.A., Vaagbo C.B., Kavli B., Bratlie M.S., Pena-Diaz J., Otterlei M., Slupphaug G., Krokan H.E. Alkylation damage in DNA and RNA - repair mechanisms and medical significance. DNA Repair 2004, 3:1389-1407.
17. Sedgwick B., Bates P.A., Paik J., Jacobs S.C., Lindahl T. Repair of alkylated DNA: recent advances. DNA Repair 2007, 6:429-442.
18. Trivedi R.N., Almeida K.L., Forsaglio J.L., Schamus S., Sobol R.W. The role of base excision repair in the sensitivity and resistance to temozolomide-mediated cell death. Cancer Res. 2005, 65:6394-6400.
19. Gerson S.L. MGMT: it's role in cancer aetiology and cancer therapeutics. Nat. Rev. Cancer 2004, 4:296-307.
20. Karran P., Hampson R. Genomic instability and tolerance to alkylating agents. Cancer Surveys 1996, 28:69-85.
21. Tomita-Mitchell A., Kat A.G., Marcelino L.A., Li-Sucholeiki X.-C., Goodluck-Griffith J., Thilly W.G. Mismatch repair deficient human cells: spontaneous and MNNG-induced mutational spectra in the HPRT gene. Mut. Res. 2000, 450:125-138.
22. 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.
23. 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.
24. Yoshioka K.-I., Yoshioka Y., Hsieh P. ATR kinase activation mediated by MutSα and MutLα in response to cytotoxic O6-methylguanine adducts. Mol. Cell 2006, 22:501-510.
25. York S.J., Modrich P. Mismatch repair-dependent iterative excision at irreparable O6methylguanine lesions in human nuclear extracts. J. Biol. Chem. 2006, 281:22674-22683.
26. Dosch J., Christmann M., Kaina B. Mismatch G-T binding activity and MSH2 expression is quantitatively related to sensitivity of cells to methylating agents. Carcinogenesis 1998, 19:567-573.
27. Hickman M.J., Samson L.D. Apoptotic signaling in response to a single type of DNA lesion, O6-methylguanine. Mol. Cell 2004, 14:105-116.
28. Schofield M.J., Hsieh P. DNA mismatch repair: molecular mechanisms and biological function. Annu. Rev. Microbiol. 2003, 57:579-608.
29. 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.
30. Cantin G.T., Yi W., Lu B., Park S.K., Xu T., Lee J.-D., Yates J.R.I. Combining protein-based IMAC, peptide-based IMAC, and MudPIT for efficient phosphoproteome analysis. J. Proteome Res. 2008, 7:1346-1351.
31. Daub H., Olsen J.V., Bairlein M., Gnad F., Oppermann F.S., Korner R., Greff Z., Keri G., Stemmann O., Mann M. Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol. Cell 2008, 31:438-448.
32. Dephoure N., Zhou C., Villen J., Beausoleil S.A., Bakalarski C.E., Elledge S.J., Gygi S.P. A quantitative atlas of mitotic phosphorylation. PNAS 2008, 105:10762-10767.
33. Nousiainen M., Sillje H.H.W., Sauer G., Nigg E.A., Koerner R. Phosphoproteome analysis of the human mitotic spindle. PNAS 2006, 103:5391-5396.
34. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., Mann M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
35. Beausoleil S.A, Jedrychowski M., Schwartz D., Elias J.E., Villen J., Li J., Cohn M.A., Cantley L.C., Gygi S.P. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:12130-12135.
36. Beausoleil S.A., Villen J., Gerber S.A., Rush J., Gygi S.P. A probability-based approach for high-throughput protein phosporylation analysis and site localization. Nat. Biotechnol. 2006, 24:1285-1292.
37. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S.P., Elledge S.J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1164.
38. 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.
39. Christmann M., Tomicic M.T., Kaina B. Phosphorylation of mismatch repair proteins MSH2 and MSH6 affecting MutSα mismatch-binding activity. Nucleic Acids Res. 2002, 30:1959-1966.
40. Hernandez-Pigeon H., Qillet-Mary A., Louat T., Schambourg A., Humbert O., Selves J., Salles B., Laurent G., Lautier D. Phosphorylation of mismatch repair proteins MSH2 and MSH6 affecting MutSα mismatch-binding activity. Nucleic Acids Res. 2005, 348:63-74.
41. Humbert O., Hermine T., Hernandez H., Bouget T., Selves J., Laurent G., Salles B., Lautier D. Implication of protein kinase C in the regulation of DNA mismatch repair protein expression and function. J. Biol. Chem. 2002, 277:18061-18068.
42. Edelbrock M., He H., Schroering A.G., Fernstrom M., Bathala S., Williams K.J. Recognition and binding of mismatch repair proteins at an oncogenic hot spot. BMC Mol. Biol. 2005, 6:6.
43. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983, 11:1475-1489.
44. Duckett D.R., Drummond J.T., Murchie A.I.H., Reardon J.T., Sancar A., Lilley D.M.J., Modrich P. Human MutSα recognizes damaged DNA basepairs containing O6-methylguanine O4-methylthymine, or the cisplatin-d(GPG) adduct. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:6443-6447.
45. Griffin S., Branch P., Xu Y.-Z., Karran P. DNA mismatch binding and incision at modified guanine bases by extracts of mammalian cells: implications for tolerance to DNA methylation damage. Biochemistry 1994, 33:4787-4793.
46. Gradia S., Subramanian S., Wilson T., Acharya S., Makhov A., Griffith J.D., Fishel R. hMSH2-hMSH6 forms a hydrolysis-independent sliding clamp on mismatched DNA. Mol. Cell. 1999, 3:255-261.
47. Blackwell L.J., Martik D., Bjornson K.P., Modrich P. Nucleotide-promoted release of hMutSalpha from heteroduplex DNA is consistent with an ATP-dependent translocation mechanism. J. Biol. Chem. 1998, 273:32055-32062.
48. Schmit T.L., Ahmad N. Regulation of mitosis via mitotic kinases: new opportunities of cancer management. Mol. Cancer Ther. 2007, 6:1920-1931.
49. Kohn E.A., Ruth N.D., Brown M.K., Livingston M., Eastman A. Abrogation of the S phase DNA damage checkpoint results in S phase progression or premature mitosis depending ont the concentration of 7-hydroxystaurosporine and the kinetics of Ccd25C activation. J. Biol. Chem. 2002, 277:26553-26564.
50. Busby E.C., Leistritz D.F., Abraham R.T., Karnitz L.M., Sarkaria J.N. The radiosensitizing agent 7-hydroxystaurosporine (UCN-01) inhibits the DNA damage checkpoint kinase hChk1. Cancer Res. 2000, 60:2108-2112.
51. Hutchins J.R.A., Clarke P.R. Many fingers on the mitotic trigger. Cell Cycle 2004, 3:41-45.
52. Linding R., Jensen L.J., Ostheimer G.J., van Vugt M.A.T.M., Jorgensen C., Miron I.M., Diella F., Colwill K., Taylor L., Elder K., Metalnikov P., Nguyen V., Pasculescu A., Jin J., Park J.G., Samson L.D., Woodgett J.R., Russell R.B., Bork P., Yaffe M.B., Pawson T. Systemic discovery of in vivo phosphorylation networks. Cell 2007, 129:1415-1426.
53. St-Denis N.A., Litchfield D.W. From birth to death: the role of protein kinase CK2 in the regulation of cell proliferation and survival. Cell. Mol. Life Sci. 2009, 66:1817-1829.
54. Johnson S.A., Hunter T. Kinomics: methods for deciphering the kinome. Nat. Methods 2005, 2:17-25.
55. Shell S.S., Putnam C.D., Kolodner R.D. The N terminus of Saccharomyces cerrevisiae Msh6 is an unstructured tether to PCNA. Mol. Cell 2007, 26:565-578.
56. Kleczkowska H.E., Marra G., Lettieri T., Jiricny J. hMSH3 and hMSH6 interact with PCNA and colocalize with it to replication foci. Genes Dev. 2001, 15:724-736.
57. Clark A.B., Deterding L., Tomer K.B., Kunkel T.A. Multiple functions for the N-terminal region of Msh6. Nucleic Acids Res. 2007, 35:4114-4123.
58. Warren J.J., Pohlhaus T.J., Changela A., Iyer R.R.P. Modrich structure of the human MutSa DNA lesion recognition complex. Mol. Cell 2007, 26:579-592.
59. Oakley G.G., Patrick S.M., Yao J., Carty M.P., Turchi J.J., Dixon K. RPA phosphorylation in mitosis alters DNA binding and protein-protein interactions. Biochemistry 2003, 42:3255-3264.
60. Deng X., Prakash A., Dhar K., Baia G.S., Kolar C., Oakley G.C., Borgstahl G.E.O. Human repliation protein A-Rad52-single-stranded DNA complex: stoichiometry and evidence for strand transfer regulation by phosphorylation. Biochemistry 2009, 48:6633-6643.
61. Lee H., Yuan C., Hammet A., Mahajan A., Chen E.S.-W., Wu M.-R., Su M.-I., Heierhorst J., Tsai M.-D. Diphosphothreonine-specific interaction between an SQ/TQ cluster and an FHA domain in the rad53-dun1 kinase cascade. Mol. Cell 2008, 30:767-778.
62. Mendez A., Burns M.E., Roca A., Lem J., Wu L.-W., Simon M.I., Baylor D.A., Chen J. Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron 2000, 28:153-164.
63. Park K.-S., Mohapatra D.P., Misonou H., Trimmer J.S. Graded regulation of the Kv2.1 potassium channel by variable phosphorylation. Science 2006, 313:976-979.
64. Newton A.C. Protein kinase C: poised to signal. Am. J. Physiol. Endocrinol. Metab. 2009, 298:E395-E402.
65. Bain J., Plater L., Elliot M., Shpiro N., Hastie C.J., McLauchlan H., Klevernic I., Arthur J.S.C., Alessi D.R., Cohen P. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 2007, 408:297-315.
66. Graves P.R., Yu L., Schwarz J.K., Gales J., Sausville E.A., O'Connor P.M., Piwnica-Worms H. The Chk1 protein kinase and the Cdc25C regulatory pathways are targets of the anticancer agent UCN-01. J. Biol. Chem. 2000, 275:5600-5605.
67. Genschel J., Modrich P. Mechanism of 5'-directed excision in human mismatch repair. Mol. Cell 2003, 12:1077-1086.