Determination of apoptosis, uracil incorporation, DNA strand breaks, and sister chromatid exchanges under conditions of thymidylate deprivation in a model of BER deficiency

Biochemical Pharmacology

Volumn 70, Issue 10, 2005, Pages 1458-1468

  Li, Li ^a   Connor, Ellen E ^a   Berger, Sondra H ^a   Wyatt, Michael D ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Base excision repair; Cancer chemotherapy; DNA polymerase ; DNA repair; Raltitrexed; Thymineless stress

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; RALTITREXED; THYMIDINE PHOSPHATE; URACIL; URACIL DNA GLYCOSYLTRANSFERASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA RECOMBINATION; DNA STRAND BREAKAGE; DRUG EFFECT; DRUG SENSITIVITY; EMBRYO; ENZYME ACTIVITY; EXCISION REPAIR; MOUSE; NONHUMAN; NULL CELL; PRIORITY JOURNAL; SISTER CHROMATID EXCHANGE; WILD TYPE;

ANIMALS; APOPTOSIS; CELL LINE; CELLS, CULTURED; DNA DAMAGE; DNA POLYMERASE BETA; DNA REPAIR; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO; FIBROBLASTS; HUMANS; MICE; POLY ADENOSINE DIPHOSPHATE RIBOSE; QUINAZOLINES; SISTER CHROMATID EXCHANGE; THIOPHENES; THYMIDYLATE SYNTHASE; TIME FACTORS; URACIL; URACIL-DNA GLYCOSIDASE;

EID: 26944498660     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2005.08.016     Document Type: Article

References (51)

1. D.B. Longley, D.P. Harkin, and P.G. Johnston 5-Fluorouracil: mechanisms of action and clinical strategies Nat Rev Cancer 3 5 2003 330 338
2. G.W. Aherne, and S. Brown The role of uracil misincroporation in thymineless death A.L. Jackman Anticancer Drug Development Guide: Antifolate Drugs in Cancer Therapy 1999 Humana Press Inc. Totowa, NJ 409 421
3. C.E. Canman, E.H. Radany, L.A. Parsels, M.A. Davis, T.S. Lawrence, and J. Maybaum Induction of resistance to fluorodeoxyuridine cytotoxicity and DNA damage in human tumor cells by expression of Escherichia coli deoxyuridinetriphosphatase Cancer Res 54 9 1994 2296 2298
4. S.E. Koehler, and R.D. Ladner Small interfering RNA-mediated suppression of dUTPase sensitizes cancer cell lines to thymidylate synthase inhibition Mol Pharmacol 66 3 2004 620 626
5. L.A. Parsels, J.D. Parsels, L.M. Wagner, T.L. Loney, E.H. Radany, and J. Maybaum Mechanism and pharmacological specificity of dUTPase-mediated protection from DNA damage and cytotoxicity in human tumor cells Cancer Chemother Pharmacol 42 5 1998 357 362
6. B.A. Tinkelenberg, M.J. Hansbury, and R.D. Ladner dUTPase and uracil-DNA glycosylase are central modulators of antifolate toxicity in Saccharomyces cerevisiae Cancer Res 62 17 2002 4909 4915
7. S.D. Webley, S.J. Welsh, A.L. Jackman, and G.W. Aherne The ability to accumulate deoxyuridine triphosphate and cellular response to thymidylate synthase (TS) inhibition Br J Cancer 85 3 2001 446 452
8. S.D. Webley, A. Hardcastle, R.D. Ladner, A.L. Jackman, and G.W. Aherne Deoxyuridine triphosphatase (dUTPase) expression and sensitivity to the thymidylate synthase (TS) inhibitor ZD9331 Br J Cancer 83 6 2000 792 799
9. J.A. Houghton, D.M. Tillman, and F.G. Harwood Ratio of 2′-deoxyadenosine-5′-triphosphate/thymidine-5′-triphosphate influences the commitment of human colon carcinoma cells to thymineless death Clin Cancer Res 1 7 1995 723 730
10. H.E. Krokan, F. Drablos, and G. Slupphaug Uracil in DNA - occurrence, consequences and repair Oncogene 21 58 2002 8935 8948
11. M. Otterlei, E. Warbrick, T.A. Nagelhus, T. Haug, G. Slupphaug, and M. Akbari Post-replicative base excision repair in replication foci EMBO J 18 13 1999 3834 3844
12. S.J. Welsh, S. Hobbs, and G.W. Aherne Expression of uracil DNA glycosylase (UDG) does not affect cellular sensitivity to thymidylate synthase (TS) inhibition Eur J Cancer 39 3 2003 378 387
13. S. Andersen, T. Heine, R. Sneve, I. König, H.E. Krokan, and B. Epe Incorporation of dUMP into DNA is a major source of spontaneous DNA damage, while excision of uracil is not required for cytotoxicity of fluoropyrimidines in mouse embryonic fibroblasts Carcinogenesis 26 3 2005 547 555
14. M. Meyers, M.W. Wagner, A. Mazurek, C. Schmutte, R. Fishel, and D.A. Boothman DNA mismatch repair-dependent response to fluoropyrimidine-generated damage J Biol Chem 280 7 2005 5516 5526
15. F. Petronzelli, A. Riccio, G.D. Markham, S.H. Seeholzer, J. Stoerker, and M. Genuardi Biphasic kinetics of the human DNA repair protein MED1 (MBD4), a mismatch-specific DNA N-glycosylase J Biol Chem 275 42 2000 32422 32429
16. U. Hardeland, M. Bentele, J. Jiricny, and P. Schar Separating substrate recognition from base hydrolysis in human thymine DNA glycosylase by mutational analysis J Biol Chem 275 43 2000 33449 33456
17. R.W. Sobol, M. Kartalou, K.H. Almeida, D.F. Joyce, B.P. Engelward, and J.K. Horton Base excision repair intermediates induce p53-independent cytotoxic and genotoxic responses J Biol Chem 278 41 2003 39951 39959
18. J.K. Horton, D.F. Joyce-Gray, B.F. Pachkowski, J.A. Swenberg, and S.H. Wilson Hypersensitivity of DNA polymerase beta null mouse fibroblasts reflects accumulation of cytotoxic repair intermediates from site-specific alkyl DNA lesions DNA Repair 2 1 2003 27 48
19. L. Li, S.H. Berger, and M.D. Wyatt Involvement of base excision repair in response to therapy targeted at thymidylate synthase Mol Cancer Ther 3 6 2004 747 753
20. R.W. Sobol, J.K. Horton, R. Kuhn, H. Gu, R.K. Singhal, and R. Prasad Requirement of mammalian DNA polymerase-beta in base-excision repair Nature 379 6561 1996 183 186
21. R.W. Sobol, R. Prasad, A. Evenski, A. Baker, X.P. Yang, and J.K. Horton The lyase activity of the DNA repair protein beta-polymerase protects from DNA-damage-induced cytotoxicity Nature 405 6788 2000 807 810
22. O.I. Lavrik, R. Prasad, R.W. Sobol, J.K. Horton, E.J. Ackerman, and S.H. Wilson Photoaffinity labeling of mouse fibroblast enzymes by a base excision repair intermediate: Evidence for the role of poly(ADP-ribose) polymerase-1 in DNA repair J Biol Chem 276 27 2001 25541 25548
23. V. Spanswick, J. Hartley, T. Ward, and J. Hartley Measurement of drug-induced DNA interstrand crosslinking using the single-cell gel electrophoresis (Comet) assay R. Brown U. Boger-Brown Cytotoxic Drug Resistance Mechanisms vol. 28 1999 Humana Press Totowa, NJ 143 154
24. C. Helma, and M. Uhl A public domain image-analysis program for the single-cell gel-electrophoresis (comet) assay Mutat Res 466 1 2000 9 15
25. S.T. Mashiyama, C. Courtemanche, I. Elson-Schwab, J. Crott, B.L. Lee, and C.N. Ong Uracil in DNA, determined by an improved assay, is increased when deoxynucleosides are added to folate-deficient cultured human lymphocytes Anal Biochem 330 1 2004 58 69
26. R.I. Freshney Culture of Animal Cells 2000 Wiley-Liss New York
27. Y. Mizushina, N. Takahashi, A. Ogawa, K. Tsurugaya, H. Koshino, and M. Takemura The cyanogenic glucoside, prunasin (d-mandelonitrile-beta-d-glucoside), is a novel inhibitor of DNA polymerase beta J Biochem (Tokyo) 126 2 1999 430 436
28. M.T. Tomicic, R. Thust, R.W. Sobol, and B. Kaina DNA polymerase beta mediates protection of mammalian cells against ganciclovir-induced cytotoxicity and DNA breakage Cancer Res 61 20 2001 7399 7403
29. J.C. Ame, C. Spenlehauer, and G. de Murcia The PARP superfamily Bioessays 26 8 2004 882 893
30. M.A. Babich, and R.S. Day III Potentiation of cytotoxicity by 3-aminobenzamide in DNA repair-deficient human tumor cell lines following exposure to methylating agents or anti-neoplastic drugs Carcinogenesis 9 4 1988 541 546
31. J.E. Cleaver Stimulation of repair replication by 3-aminobenzamide in human fibroblasts with ligase I deficiency Carcinogenesis 17 1 1996 1 3
32. F. Le Page, V. Schreiber, C. Dherin, G. De Murcia, and S. Boiteux Poly(ADP-ribose) polymerase-1 (PARP-1) is required in murine cell lines for base excision repair of oxidative DNA damage in the absence of DNA polymerase beta J Biol Chem 278 20 2003 18471 18477
33. V. Burkart, Z.Q. Wang, J. Radons, B. Heller, Z. Herceg, and L. Stingl Mice lacking the poly(ADP-ribose) polymerase gene are resistant to pancreatic beta-cell destruction and diabetes development induced by streptozocin Nat Med 5 3 1999 314 319
34. H.C. Ha, and S.H. Snyder Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion Proc Natl Acad Sci USA 96 24 1999 13978 13982
35. C.E. Canman, H.Y. Tang, D.P. Normolle, T.S. Lawrence, and J. Maybaum Variations in patterns of DNA damage induced in human colorectal tumor cells by 5-fluorodeoxyuridine: implications for mechanisms of resistance and cytotoxicity Proc Natl Acad Sci USA 89 21 1992 10474 10478
36. H.A. Ingraham, L. Dickey, and M. Goulian DNA fragmentation and cytotoxicity from increased cellular deoxyuridylate Biochemistry 25 11 1986 3225 3230
37. A. Yoshioka, S. Tanaka, O. Hiraoka, Y. Koyama, Y. Hirota, and D. Ayusawa Deoxyribonucleoside triphosphate imbalance. 5-Fluorodeoxyuridine-induced DNA double strand breaks in mouse FM3A cells and the mechanism of cell death J Biol Chem 262 17 1987 8235 8241
38. S.I. Matsui, M.A. Arredondo, C. Wrzosek, and Y.M. Rustum DNA damage and p53 induction do not cause ZD1694-induced cell cycle arrest in human colon carcinoma cells Cancer Res 56 20 1996 4715 4723
39. W.D. Sedwick, M. Kutler, and O.E. Brown Antifolate-induced misincorporation of deoxyuridine monophosphate into DNA: inhibition of high molecular weight DNA synthesis in human lymphoblastoid cells Proc Natl Acad Sci USA 78 2 1981 917 921
40. Y. Mishina, D. Ayusawa, T. Seno, and H. Koyama Thymidylate stress induces homologous recombination activity in mammalian cells Mutat Res 246 1 1991 215 220
41. D. Ayusawa, H. Koyama, K. Shimizu, S. Kaneda, K. Takeishi, and T. Seno Induction, by thymidylate stress, of genetic recombination as evidenced by deletion of a transferred genetic marker in mouse FM3A cells Mol Cell Biol 6 10 1986 3463 3469
42. D. Ayusawa, K. Shimizu, H. Koyama, K. Takeishi, and T. Seno Accumulation of DNA strand breaks during thymineless death in thymidylate synthase-negative mutants of mouse FM3A cells J Biol Chem 258 20 1983 12448 12454
43. K. Ochs, J. Lips, S. Profittlich, and B. Kaina Deficiency in DNA polymerase beta provokes replication-dependent apoptosis via DNA breakage, Bcl-2 decline and caspase-3/9 activation Cancer Res 62 5 2002 1524 1530
44. W.P. Osheroff, H.K. Jung, W.A. Beard, S.H. Wilson, and T.A. Kunkel The fidelity of DNA polymerase beta during distributive and processive DNA synthesis J Biol Chem 274 6 1999 3642 3650
45. C. Schober, J.F. Gibbs, M.B. Yin, H.K. Slocum, and Y.M. Rustum Cellular heterogeneity in DNA damage and growth inhibition induced by ICI D1694, thymidylate synthase inhibitor, using single cell assays Biochem Pharmacol 48 5 1994 997 1002
46. J.L. Tonkinson, P. Marder, S.L. Andis, R.M. Schultz, L.S. Gossett, and C. Shih Cell cycle effects of antifolate antimetabolites: implications for cytotoxicity and cytostasis Cancer Chemother Pharmacol 39 6 1997 521 531
47. H.H. el-Hajj, L. Wang, and B. Weiss Multiple mutant of Escherichia coli synthesizing virtually thymineless DNA during limited growth J Bacteriol 174 13 1992 4450 4456
48. B.J. Barclay, and J.G. Little Genetic damage during thymidylate starvation in Saccharomyces cerevisiae Mol Gen Genet 160 1 1978 33 40
49. B.J. Barclay, B.A. Kunz, J.G. Little, and R.H. Haynes Genetic and biochemical consequences of thymidylate stress Can J Biochem 60 3 1982 172 184
50. B.A. Kunz, and R.H. Haynes DNA repair and the genetic effects of thymidylate stress in yeast Mutat Res 93 1982 353 375
51. B.K. Tye, P.O. Nyman, I.R. Lehman, S. Hochhauser, and B. Weiss Transient accumulation of Okazaki fragments as a result of uracil incorporation into nascent DNA Proc Natl Acad Sci USA 74 1 1977 154 157