Hypersensitivity of DNA polymerase β null mouse fibroblasts reflects accumulation of cytotoxic repair intermediates from site-specific alkyl DNA lesions

DNA Repair

Volumn 2, Issue 1, 2003, Pages 27-48

  Horton, Julie K ^a   Joyce Gray, Donna F ^a   Pachkowski, Brian F ^b   Swenberg, James A ^b   Wilson, Samuel H ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

5 Hydroxymethyl 2 deoxyuridine; Base excision repair; Cell cycle; DNA alkylation; DNA polymerase ; Monofunctional alkylating agent

Indexed keywords

3 METHYLADENINE; 5 HYDROXYMETHYLDEOXYURIDINE; ALKYLATING AGENT; DNA; DNA DIRECTED DNA POLYMERASE BETA; GUANINE DERIVATIVE; MESYLIC ACID METHYL ESTER; METHYLNITROSOUREA; THYMIDINE DERIVATIVE; ANTINEOPLASTIC AGENT; CONGOCIDINE; DRUG DERIVATIVE; METHYL LEXITROPSIN;

ANIMAL CELL; ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CONTROLLED STUDY; CYTOTOXICITY; DNA ADDUCT; DNA DAMAGE; DNA METHYLATION; DNA SYNTHESIS; EMBRYO; EXCISION REPAIR; FIBROBLAST; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; WILD TYPE; ALKYLATION; ANIMAL; CELL LINE; DNA REPAIR; GENETICS; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; TIME;

ANIMALIA;

ALKYLATING AGENTS; ALKYLATION; ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE; DNA; DNA DAMAGE; DNA POLYMERASE BETA; DNA REPAIR; FIBROBLASTS; MICE; NETROPSIN; TIME FACTORS;

EID: 0037413370     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1568-7864(02)00184-2     Document Type: Article

References (65)

1. B. Singer, D. Grunberger, Molecular Biology of Mutagens and Carcinogens, Plenum Press, New York, 1983.
2. Beranek D.T. Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents. Mutat. Res. 231:1990;11-30.
3. Roy R., Brooks C., Mitra S. Purification and biochemical characterization of recombinant N-methylpurine-DNA glycosylase of the mouse. Biochemistry. 33:1994;15131-15140.
4. Srivastava D.K., Vande Berg B.J., Prasad R., Molina J.T., Beard W.A., Tomkinson A.E., Wilson S.H. Mammalian abasic site base excision repair. Identification of the reaction sequence and rate-determining steps. J. Biol. Chem. 273:1998;21203-21209.
5. Sobol R.W., Horton J.K., Kuhn R., Gu H., Singhal R.K., Prasad R., Rajewsky K., Wilson S.H. Requirement of mammalian DNA polymerase β in base-excision repair. Nature. 379:1996;183-186.
6. Biade S., Sobol R.W., Wilson S.H., Matsumoto Y. Impairment of proliferating cell nuclear antigen-dependent apurinic/apyrimidinic site repair on linear DNA. J. Biol. Chem. 273:1998;898-902.
7. Dianov G.L., Prasad R., Wilson S.H., Bohr V.A. Role of DNA polymerase β in the excision step of long patch mammalian base excision repair. J. Biol. Chem. 274:1999;13741-13743.
8. Horton J.K., Prasad R., Hou E., Wilson S.H. Protection against methylation-induced cytotoxicity by DNA polymerase β-dependent long patch base excision repair. J. Biol. Chem. 275:2000;2211-2218.
9. Sobol R.W., Prasad R., Evenski A., Baker A., Yang X.-P., Horton J.K., Wilson S.H. The lyase activity of the DNA repair protein β-polymerase protects from DNA-damage-induced cytotoxicity. Nature. 405:2000;807-810.
10. Brennand J., Margison G.P. Reduction of the toxicity and mutagenicity of alkylating agents in mammalian cells harboring the E. coli alkyltransferase gene. Proc. Natl. Acad. Sci. U.S.A. 83:1986;6292-6296.
11. 6-methylguanine-DNA methyltransferase (MGMT) cDNA in Chinese hamster cells: the role of MGMT in protection against the genotoxic effects of alkylating agents. Carcinogenesis. 12:1991;1857-1867.
12. 6-alkylguanine-DNA alkyltransferase: regulation and importance in response to alkylating carcinogenic and therapeutic agents. Cancer Res. 50:1990;6119-6129.
13. 6-alkylguanine-DNA alkyltransferase and nucleotide excision repair activities in human cells. Cancer Res. 52:1992;2008-2011.
14. 4-methylthymine repair by eukaryotic methyltransferases. J. Biol. Chem. 266:1991;2767-2771.
15. 6-benzylguanine. Cancer Res. 53:1993;3895-3898.
16. Larson K., Sahm J., Shenkar R., Strauss B. Methylation-induced blocks to in vitro DNA replication. Mutat. Res. 150:1985;77-84.
17. Zhang Y., Chen F.X., Mehta P., Gold B. Groove- and sequence-selective alkylation of DNA by sulfonate esters tethered to lexitropsins. Biochemistry. 32:1993;7954-7965.
18. Boorstein R.J., Chiu L.-N., Teebor G.W. A mammalian cell line deficient in activity of the DNA repair enzyme 5-hydroxymethyluracil-DNA glycosylase is resistant to the toxic effects of the thymidine analog 5-hydroxymethyl-2′-deoxyuridine. Mol. Cell Biol. 12:1992;5536-5540.
19. Boorstein R.J., Cummings A. Jr., Marenstein D.R., Chan M.K., Ma Y., Neubert T.A., Brown S.M., Teebor G.W. Definitive identification of mammalian 5-hydroxymethyluracil DNA N-glycosylase activity as SMUG1. J. Biol. Chem. 276:2001;41991-41997.
20. Baker D., Liu P., Burdzy A., Sowers L.C. Characterization of the substrate specificity of a human 5- hydroxymethyluracil glycosylase activity. Chem. Res. Toxicol. 15:2002;33-39.
21. Kaufmann W.K., Paules R.S. DNA damage and cell cycle checkpoints. FASEB J. 10:1996;238-247.
22. Shackelford R.E., Kaufmann W.K., Paules R.S. Cell cycle control, checkpoint mechanisms, and genotoxic stress. Environ. Health Perspect. 107(Suppl 1):1999;5-24.
23. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2001;2177-2196.
24. Bartek J., Falck J., Lukas J. CHK2 kinase - a busy messenger. Nat. Rev. Mol. Cell Biol. 2:2001;877-886.
25. Bartek J., Lukas J. Mammalian G1- and S-phase checkpoints in response to DNA damage. Curr. Opin. Cell Biol. 13:2001;738-747.
26. Butler W.B. Preparing nuclei from cells in monolayer cultures suitable for counting and for following synchronized cells through the cell cycle. Anal. Biochem. 141:1984;70-73.
27. Park J.-W., Ames B.N. 7-Methylguanine adducts in DNA are normally present at high levels and increase on aging: Analysis by HPLC with electrochemical detection. Proc. Natl. Acad. Sci. U.S.A. 85:1988;7467-7470.
28. Kastan M.B., Onyekwere O., Sidransky D., Vogelstein B., Craig R.W. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:1991;6304-6311.
29. 6-benzylguanine provides a means to evaluate the role of this protein in protection against carcinogenic and therapeutic alkylating agents. Proc. Natl. Acad. Sci. U.S.A. 87:1990;5368-5372.
30. 6-benzylguanine on the sensitivity of human tumor xenografts to 1,3-bis(2-chloroethyl)-1-nitrosourea and on DNA interstrand cross-link formation. Cancer Res. 52:1992;1171-1175.
31. Spiro T., Liu L., Gerson S. New cytotoxic agents for the treatment of metastatic malignant melanoma: temozolomide and related alkylating agents in combination with guanine analogues to abrogate drug resistance. Forum. 10:2000;274-285.
32. Kelly J.D., Inga A., Chen F.X., Dande P., Shah D., Monti P., Aprile A., Burns P.A., Scott G., Abbondandolo A., Gold B., Fronza G. Relationship between DNA methylation and mutational patterns induced by a sequence selective minor groove methylating agent. J. Biol. Chem. 274:1999;18327-18334.
33. Smith S.A., Engelward B.P. In vivo repair of methylation damage in Aag 3-methyladenine DNA glycosylase null mouse cells. Nucleic Acids Res. 28:2000;3294-3300.
34. Engelward B.P., Dreslin A., Christensen J., Huszar D., Kurahara C., Samson L. Repair-deficient 3-methyladenine DNA glycosylase homozygous mutant mouse cells have increased sensitivity to alkylation-induced chromosome damage and cell killing. EMBO J. 15:1996;945-952.
35. Engelward B.P., Weeda G., Wyatt M.D., Broekhof J.L., de Wit J., Donker I., Allan J.M., Gold B., Hoeijmakers J.H., Samson L.D. Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 94:1997;13087-13092.
36. Wemmer D.E. Designed sequence-specific minor groove ligands. Annu. Rev. Biophys. Biomol. Struct. 29:2000;439-461.
37. 32P -end-labeled DNA Biochemistry. 29:1990;6827-6838.
38. McCarthy T.V., Lindahl T. Methyl phosphotriesters in alkylated DNA are repaired by the Ada regulatory protein of E. coli. Nucleic Acids Res. 13:1985;2683-2698.
39. Den Engelse L., Menkveld G.J., De Brij R.J., Tates A.D. Formation and stability of alkylated pyrimidines and purines (including imidazole ring-opened 7-alkylguanine) and alkylphosphotriesters in liver DNA of adult rats treated with ethylnitrosourea or dimethylnitrosamine. Carcinogenesis. 7:1986;393-403.
40. Fornace A.J. Jr., Zmudzka B., Hollander M.C., Wilson S.H. Induction of β-polymerase mRNA by DNA-damaging agents in Chinese hamster ovary cells. Mol. Cell. Biol. 9:1989;851-853.
41. Kedar P.S., Widen S.G., Englander E.W., Fornace A.J. Jr., Wilson S.H. The ATF/CREB transcription factor-binding site in the polymerase β promoter mediates the positive effect of N-methyl-N′-nitro-N-nitrosoguanidine on transcription. Proc. Natl. Acad. Sci. U.S.A. 88:1991;3729-3733.
42. Srivastava D.K., Rawson T.Y., Showalter S.D., Wilson S.H. Phorbol ester abrogates up-regulation of DNA polymerase β by DNA-alkylating agents in Chinese hamster ovary cells. J. Biol. Chem. 270:1995;16402-16408.
43. Wang G., Yu Y., Chen X., Xie H. Low concentration N-methyl-N′-nitro-N-nitrosoguanidine activates DNA polymerase β expression via cyclic-AMP-protein kinase A-cAMP response element binding protein pathway. Mutat. Res. 478:2001;177-184.
44. 6-methylguanine and the cytotoxicity of methylating agents. Mutat. Res. 462:2000;71-82.
45. Friedman H.S., Kerby T., Calvert H. Temozolomide and treatment of malignant glioma. Clin. Cancer Res. 6:2000;2585-2597.
46. Yung W.K. Future directions for temozolomide therapy. Semin. Oncol. 28:2001;43-46.
47. Denny B.J., Wheelhouse R.T., Stevens M.F.G., Tsang L.L., Slack J.A. NMR and molecular modeling investigation of the mechanism of activation of the antitumor drug temozolomide and its interaction with DNA. Biochemistry. 33:1994;9045-9051.
48. Liu L., Taverna P., Whitacre C.M., Chatterjee S., Gerson S.L. Pharmacologic disruption of base excision repair sensitizes mismatch repair-deficient and -proficient colon cancer cells to methylating agents. Clin. Cancer Res. 5:1999;2908-2917.
49. Taverna P., Liu L., Hwang H.S., Hanson A.J., Kinsella T.J., Gerson S.L. Methoxyamine potentiates DNA single strand breaks and double strand breaks induced by temozolomide in colon cancer cells. Mutat. Res. 485:2001;269-281.
50. Moritz T., Mackay W., Glassner B.J., Williams D.A., Samson L. Retrovirus-mediated expression of a DNA repair protein in bone marrow protects hematopoietic cells from nitrosourea-induced toxicity in vitro and in vivo. Cancer Res. 55:1995;2608-2614.
51. 6-methylguanine-DNA methyltransferase gene into a murine hematopoietic stem cell line and resistance to the toxic effects of certain alkylating agents. Biochem. Pharmacol. 51:1996;1221-1228.
52. Glassner B.J., Weeda G., Allan J.M., Broekhof J.L., Carls N.H., Donker I., Engelward B.P., Hampson R.J., Hersmus R., Hickman M.J., Roth R.B., Warren H.B., Wu M.M., Hoeijmakers J.H., Samson L.D. DNA repair methyltransferase (Mgmt) knockout mice are sensitive to the lethal effects of chemotherapeutic alkylating agents. Mutagenesis. 14:1999;339-347.
53. Engelward B.P., Allan J.M., Dreslin A.J., Kelly J.D., Wu M.M., Gold B., Samson L.D. A chemical and genetic approach together define the biological consequences of 3-methyladenine lesions in the mammalian genome. J. Biol. Chem. 273:1998;5412-5418.
54. Margison G.P., O'Connor P.J. Biological implications of the instability of the N-glycosidic bone of 3-methyldeoxyadenosine in DNA. Biochim. Biophys. Acta. 331:1973;349-356.
55. Elder R.H., Jansen J.G., Weeks R.J., Willington M.A., Deans B., Watson A.J., Mynett K.J., Bailey J.A., Cooper D.P., Rafferty J.A., Heeran M.C., Wijnhoven S.W., van Zeeland A.A., Margison G.P. Alkylpurine-DNA-N-glycosylase knockout mice show increased susceptibility to induction of mutations by methyl methanesulfonate. Mol. Cell. Biol. 18:1998;5828-5837.
56. Calléja F., Jansen J.G., Vrieling H., Laval F., van Zeeland A.A. Modulation of the toxic and mutagenic effects induced by methyl methanesulfonate in Chinese hamster ovary cells by overexpression of the rat N-alkylpurine-DNA glycosylase. Mutat. Res. 425:1999;185-194.
57. Ibeanu G., Hartenstein B., Dunn W.C., Chang L.Y., Hofmann E., Coquerelle T., Mitra S., Kaina B. Overexpression of human DNA repair protein N-methylpurine-DNA glycosylase results in the increased removal of N-methylpurines in DNA without a concomitant increase in resistance to alkylating agents in Chinese hamster ovary cells. Carcinogenesis. 13:1992;1989-1995.
58. Graham A., Fox M. The role of suppression of DNA synthesis and inhibition of cell cycle progression in cellular sensitivity to alkylation damage. Carcinogenesis. 4:1983;269-274.
59. Morris S.M., Domon O.E., McGarrity L.J., Kodell R.L., Casciano D.A. Flow cytometric evaluation of cell cycle progression in ethyl methanesulfonate and methyl methanesulfonate-exposed P3 cells: relationship to the induction of sister-chromatid exchanges and cellular toxicity. Environ. Mol. Mutagen. 18:1991;139-149.
60. Painter R.B. Inhibition of initiation of HeLa cell replicons by methyl methanesulfonate. Mutat. Res. 42:1977;299-303.
61. Cliby W.A., Roberts C.J., Cimprich K.A., Stringer C.M., Lamb J.R., Schreiber S.L., Friend S.H. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17:1998;159-169.
62. Mi L.J., Chaung W., Horowitz R., Teebor G.W., Boorstein R.J. Excessive base excision repair of 5-hydroxymethyluracil from DNA induces apoptosis in Chinese hamster V79 cells containing mutant p53. Carcinogenesis. 22:2001;179-186.
63. Tominaga K., Morisaki H., Kaneko Y., Fujimoto A., Tanaka T., Ohtsubo M., Hirai M., Okayama H., Ikeda K., Nakanishi M. Role of human Cds1 (Chk2) kinase in DNA damage checkpoint and its regulation by p53. J. Biol. Chem. 274:1999;31463-31467.
64. 6-ethylguanine as molecular dosimeter for extrapolation from cells in culture to the mouse. Environ. Health Perspect. 62:1985;163-169.
65. 6-alkylguanine function. Nucleic Acids Res. 18:1990;3961-3966.