DNA Polymerases as Potential Therapeutic Targets for Cancers Deficient in the DNA Mismatch Repair Proteins MSH2 or MLH1

Cancer Cell

Volumn 17, Issue 3, 2010, Pages 235-248

  Martin, Sarah A ^a   McCabe, Nuala ^a   Mullarkey, Michelle ^b   Cummins, Robert ^b   Burgess, Darren J ^a   Nakabeppu, Yusaku ^c   Oka, Sugako ^c   Kay, Elaine ^b   Lord, Christopher J ^a   Ashworth, Alan ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

CELLCYCLE

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; DNA DIRECTED DNA POLYMERASE GAMMA; PROTEIN MLH1; PROTEIN MSH2;

ARTICLE; CANCER INHIBITION; CANCER RESEARCH; CONTROLLED STUDY; DRUG TARGETING; ENZYME INHIBITION; GENE SILENCING; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEFICIENCY;

EID: 77649311945     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2009.12.046     Document Type: Article

References (57)

1. Aquilina G., Ceccotti S., Martinelli S., Hampson R., and Bignami M. N-(2-chloroethyl)-N′-cyclohexyl-N-nitrosourea sensitivity in mismatch repair-defective human cells. Cancer Res. 58 (1998) 135-141
2. Argueso J.L., Smith D., Yi J., Waase M., Sarin S., and Alani E. Analysis of conditional mutations in the Saccharomyces cerevisiae MLH1 gene in mismatch repair and in meiotic crossing over. Genetics 160 (2002) 909-921
3. Arnold C.N., Goel A., and Boland C.R. Role of hMLH1 promoter hypermethylation in drug resistance to 5-fluorouracil in colorectal cancer cell lines. Int. J. Cancer 106 (2003) 66-73
4. Bettstetter M., Dechant S., Ruemmele P., Grabowski M., Keller G., Holinski-Feder E., Hartmann A., Hofstaedter F., and Dietmaier W. Distinction of hereditary nonpolyposis colorectal cancer and sporadic microsatellite-unstable colorectal cancer through quantification of MLH1 methylation by real-time PCR. Clin. Cancer Res. 13 (2007) 3221-3228
5. Boiteux S., and Radicella J.P. The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis. Arch. Biochem. Biophys. 377 (2000) 1-8
6. Bonner W.M., Redon C.E., Dickey J.S., Nakamura A.J., Sedelnikova O.A., Solier S., and Pommier Y. γH2AX and cancer. Nat. Rev. Cancer 8 (2008) 957-967
7. Boudsocq F., Benaim P., Canitrot Y., Knibiehler M., Ausseil F., Capp J.P., Bieth A., Long C., David B., Shevelev I., et al. Modulation of cellular response to cisplatin by a novel inhibitor of DNA polymerase β. Mol. Pharmacol. 67 (2005) 1485-1492
8. Boyer J.C., Umar A., Risinger J.I., Lipford J.R., Kane M., Yin S., Barrett J.C., Kolodner R.D., and Kunkel T.A. Microsatellite instability, mismatch repair deficiency, and genetic defects in human cancer cell lines. Cancer Res. 55 (1995) 6063-6070
9. Bryant H.E., Schultz N., Thomas H.D., Parker K.M., Flower D., Lopez E., Kyle S., Meuth M., Curtin N.J., and Helleday T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434 (2005) 913-917
10. Claros M.G., and Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241 (1996) 779-786
11. Colussi C., Parlanti E., Degan P., Aquilina G., Barnes D., Macpherson P., Karran P., Crescenzi M., Dogliotti E., and Bignami M. The mammalian mismatch repair pathway removes DNA 8-oxodGMP incorporated from the oxidized dNTP pool. Curr. Biol. 12 (2002) 912-918
12. de Souza-Pinto N.C., Mason P.A., Hashiguchi K., Weissman L., Tian J., Guay D., Lebel M., Stevnsner T.V., Rasmussen L.J., and Bohr V.A. Novel DNA mismatch-repair activity involving YB-1 in human mitochondria. DNA Repair (Amst.) 8 (2009) 704-719
13. Druker B.J., Talpaz M., Resta D.J., Peng B., Buchdunger E., Ford J.M., Lydon N.B., Kantarjian H., Capdeville R., Ohno-Jones S., and Sawyers C.L. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N. Engl. J. Med. 344 (2001) 1031-1037
14. Echeverri C.J., Beachy P.A., Baum B., Boutros M., Buchholz F., Chanda S.K., Downward J., Ellenberg J., Fraser A.G., Hacohen N., et al. Minimizing the risk of reporting false positives in large-scale RNAi screens. Nat. Methods 3 (2006) 777-779
15. Edwards S.L., Brough R., Lord C.J., Natrajan R., Vatcheva R., Levine D.A., Boyd J., Reis-Filho J.S., and Ashworth A. Resistance to therapy caused by intragenic deletion in BRCA2. Nature 451 (2008) 1111-1115
16. Farmer H., McCabe N., Lord C.J., Tutt A.N., Johnson D.A., Richardson T.B., Santarosa M., Dillon K.J., Hickson I., Knights C., et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434 (2005) 917-921
17. Fong P.C., Boss D.S., Yap T.A., Tutt A., Wu P., Mergui-Roelvink M., Mortimer P., Swaisland H., Lau A., O'Connor M.J., et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med. 361 (2009) 123-134
18. Hartwell L.H., Szankasi P., Roberts C.J., Murray A.W., and Friend S.H. Integrating genetic approaches into the discovery of anticancer drugs. Science 278 (1997) 1064-1068
19. Hegde M.R., and Roa B.B. Genetic testing for hereditary nonpolyposis colorectal cancer (HNPCC). Curr. Protoc. Hum. Genet. (2009) Chapter 10, Unit 10.12
20. Horton J.K., Baker A., Berg B.J., Sobol R.W., and Wilson S.H. Involvement of DNA polymerase β in protection against the cytotoxicity of oxidative DNA damage. DNA Repair (Amst.) 1 (2002) 317-333
21. Hu H.Y., Horton J.K., Gryk M.R., Prasad R., Naron J.M., Sun D.A., Hecht S.M., Wilson S.H., and Mullen G.P. Identification of small molecule synthetic inhibitors of DNA polymerase β by NMR chemical shift mapping. J. Biol. Chem. 279 (2004) 39736-39744
22. Jacob S., and Praz F. DNA mismatch repair defects: role in colorectal carcinogenesis. Biochimie 84 (2002) 27-47
23. Jiricny J. The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell Biol. 7 (2006) 335-346
24. Kaelin Jr. W.G. The concept of synthetic lethality in the context of anticancer therapy. Nat. Rev. Cancer 5 (2005) 689-698
25. Kamiya H. Mutagenic potentials of damaged nucleic acids produced by reactive oxygen/nitrogen species: approaches using synthetic oligonucleotides and nucleotides: survey and summary. Nucleic Acids Res. 31 (2003) 517-531
26. Kastrinos F., Stoffel E.M., Balmana J., Steyerberg E.W., Mercado R., and Syngal S. Phenotype comparison of MLH1 and MSH2 mutation carriers in a cohort of 1,914 individuals undergoing clinical genetic testing in the United States. Cancer Epidemiol. Biomarkers Prev. 17 (2008) 2044-2051
27. Klungland A., and Bjelland S. Oxidative damage to purines in DNA: role of mammalian Ogg1. DNA Repair (Amst.) 6 (2007) 481-488
28. Koi M., Umar A., Chauhan D.P., Cherian S.P., Carethers J.M., Kunkel T.A., and 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. 54 (1994) 4308-4312
29. Lewis W., Simpson J.F., and Meyer R.R. Cardiac mitochondrial DNA polymerase-γ is inhibited competitively and noncompetitively by phosphorylated zidovudine. Circ. Res. 74 (1994) 344-348
30. Lewis W., Day B.J., Kohler J.J., Hosseini S.H., Chan S.S., Green E.C., Haase C.P., Keebaugh E.S., Long R., Ludaway T., et al. Decreased mtDNA, oxidative stress, cardiomyopathy, and death from transgenic cardiac targeted human mutant polymerase γ. Lab. Invest. 87 (2007) 326-335
31. Loeb L.A., and Monnat Jr. R.J. DNA polymerases and human disease. Nat. Rev. Genet. 9 (2008) 594-604
32. Luo J., Solimini N.L., and Elledge S.J. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 136 (2009) 823-837
33. Macpherson P., Barone F., Maga G., Mazzei F., Karran P., and Bignami M. 8-oxoguanine incorporation into DNA repeats in vitro and mismatch recognition by MutSα. Nucleic Acids Res. 33 (2005) 5094-5105
34. Martin S.A., McCarthy A., Barber L.J., Burgess D.J., Parry S., Lord C.J., and Ashworth A. Methotrexate induces oxidative DNA damage and is selectively lethal to tumour cells with defects in the DNA mismatch repair gene MSH2. EMBO Mol. Med. 1 (2009) 323-337
35. Mazzucco C.E., Hamatake R.K., Colonno R.J., and Tenney D.J. Entecavir for treatment of hepatitis B virus displays no in vitro mitochondrial toxicity or DNA polymerase γ inhibition. Antimicrob. Agents Chemother. 52 (2008) 598-605
36. Mizushina Y., Takahashi N., Ogawa A., Tsurugaya K., Koshino H., Takemura M., Yoshida S., Matsukage A., Sugawara F., and Sakaguchi K. The cyanogenic glucoside, prunasin (D-mandelonitrile-β-D-glucoside), is a novel inhibitor of DNA polymerase β. J. Biochem. 126 (1999) 430-436
37. Mizushina Y., Kamisuki S., Kasai N., Shimazaki N., Takemura M., Asahara H., Linn S., Yoshida S., Matsukage A., Koiwai O., et al. A plant phytotoxin, solanapyrone A, is an inhibitor of DNA polymerase β and λ. J. Biol. Chem. 277 (2002) 630-638
38. Mootha V.K., Bunkenborg J., Olsen J.V., Hjerrild M., Wisniewski J.R., Stahl E., Bolouri M.S., Ray H.N., Sihag S., Kamal M., et al. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115 (2003) 629-640
39. Morrison A., Johnson A.L., Johnston L.H., and Sugino A. Pathway correcting DNA replication errors in Saccharomyces cerevisiae. EMBO J. 12 (1993) 1467-1473
40. Ogi T., and Lehmann A.R. The Y-family DNA polymerase κ (pol κ) functions in mammalian nucleotide-excision repair. Nat. Cell Biol. 8 (2006) 640-642
41. Oka S., Ohno M., Tsuchimoto D., Sakumi K., Furuichi M., and Nakabeppu Y. Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs. EMBO J. 27 (2008) 421-432
42. Palomaki G.E., McClain M.R., Melillo S., Hampel H.L., and Thibodeau S.N. EGAPP supplementary evidence review: DNA testing strategies aimed at reducing morbidity and mortality from Lynch syndrome. Genet. Med. 11 (2009) 42-65
43. Parsons J.L., Tait P.S., Finch D., Dianova I.I., Allinson S.L., and Dianov G.L. CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol. Cell 29 (2008) 477-487
44. Pavlov Y.I., Nguyen D., and Kunkel T.A. Mutator effects of overproducing DNA polymerase η (Rad30) and its catalytically inactive variant in yeast. Mutat. Res. 478 (2001) 129-139
45. Peltomaki P., and Vasen H. Mutations associated with HNPCC predisposition-update of ICG-HNPCC/INSiGHT mutation database. Dis. Markers 20 (2004) 269-276
46. Saffhill R., and Ockey C.H. Strand breaks arising from the repair of the 5-bromodeoxyuridine-substituted template and methyl methanesulphonate-induced lesions can explain the formation of sister chromatid exchanges. Chromosoma 92 (1985) 218-224
47. Sasaki R., Suzuki Y., Yonezawa Y., Ota Y., Okamoto Y., Demizu Y., Huang P., Yoshida H., Sugimura K., and Mizushina Y. DNA polymerase γ inhibition by vitamin K3 induces mitochondria-mediated cytotoxicity in human cancer cells. Cancer Sci. 99 (2008) 1040-1048
48. Shia J. Immunohistochemistry versus microsatellite instability testing for screening colorectal cancer patients at risk for hereditary nonpolyposis colorectal cancer syndrome. Part I. The utility of immunohistochemistry. J. Mol. Diagn. 10 (2008) 293-300
49. Siehler S.Y., Schrauder M., Gerischer U., Cantor S., Marra G., and Wiesmuller L. Human MutL-complexes monitor homologous recombination independently of mismatch repair. DNA Repair (Amst.) 8 (2009) 242-252
50. Strathdee G., MacKean M.J., Illand M., and Brown R. A role for methylation of the hMLH1 promoter in loss of hMLH1 expression and drug resistance in ovarian cancer. Oncogene 18 (1999) 2335-2341
51. Sun D.A., Starck S.R., Locke E.P., and Hecht S.M. DNA polymerase β inhibitors from Sandoricum koetjape. J. Nat. Prod. 62 (1999) 1110-1113
52. Tran H.T., Keen J.D., Kricker M., Resnick M.A., and Gordenin D.A. Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol. Cell. Biol. 17 (1997) 2859-2865
53. Umar A., Koi M., Risinger J.I., Glaab W.E., Tindall K.R., Kolodner R.D., Boland C.R., Barrett J.C., and Kunkel T.A. Correction of hypermutability, N-methyl-N′-nitro-N-nitrosoguanidine resistance, and defective DNA mismatch repair by introducing chromosome 2 into human tumor cells with mutations in MSH2 and MSH6. Cancer Res. 57 (1997) 3949-3955
54. Wu Q., and Vasquez K.M. Human MLH1 protein participates in genomic damage checkpoint signaling in response to DNA interstrand crosslinks, while MSH2 functions in DNA repair. PLoS Genet. 4 (2008) e1000189
55. Wu Q., Christensen L.A., Legerski R.J., and Vasquez K.M. Mismatch repair participates in error-free processing of DNA interstrand crosslinks in human cells. EMBO Rep. 6 (2005) 551-557
56. Zhang N., Lu X., Zhang X., Peterson C.A., and Legerski R.J. hMutSβ is required for the recognition and uncoupling of psoralen interstrand cross-links in vitro. Mol. Cell. Biol. 22 (2002) 2388-2397
57. Zheng H., Wang X., Legerski R.J., Glazer P.M., and Li L. Repair of DNA interstrand cross-links: interactions between homology-dependent and homology-independent pathways. DNA Repair (Amst.) 5 (2006) 566-574