Caffeine and human DNA metabolism: The magic and the mystery

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 532, Issue 1-2, 2003, Pages 85-102

  Kaufmann, William K ^a,b   Heffernan, Timothy P ^a   Beaulieu, Lea M ^a   Doherty, Sharon ^a,c   Frank, Alexandra R ^a   Zhou, Yingchun ^a   Bryant, Miriam F ^a   Zhou, Tong ^a   Luche, Douglas D ^a   Nikolaishvili Feinberg, Nana ^a   Simpson, Dennis A ^a   Cordeiro Stone, Marila ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

ATM; ATR; Caffeine; Checkpoints; DNA repair; Ionizing radiation; Ultraviolet radiation

Indexed keywords

CAFFEINE; DNA POLYMERASE; PROTEIN P21; PROTEIN P53;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CONTROLLED STUDY; CULTURAL ANTHROPOLOGY; DNA METABOLISM; DNA REPAIR; DNA SYNTHESIS; FIBROBLAST; GENOTOXICITY; HUMAN; HUMAN CELL; INCUBATION TIME; IONIZING RADIATION; IRRADIATION; PHOSPHORYLATION; PRIORITY JOURNAL; WILD TYPE;

EID: 10744219561     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2003.08.012     Document Type: Article

References (67)

1. Sarkaria J.N., Busby E.C., Tibbetts R.S., Roos P., Taya Y., Karnitz L.M., Abraham R.T. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59:1999;4375-4382.
2. Blasina A., Price B.D., Turenne G.A., McGowan C.H. Caffeine inhibits the checkpoint kinase ATM. Curr. Biol. 9:1999;1135-1138.
3. Tolmach L., Jones R.W., Busse P.M. The action of caffeine on X-irradiated HeLa cells. I. Delayed inhibition of DNA synthesis. Radiat. Res. 71:1977;653-665.
4. Savitsky K., Bar-Shira A., Gilad S., Rotman G., Ziv Y., Vanagaite L., Tagle D.A., Smith S., Uziel T., Sfez S.et al. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science. 268:1995;1749-1753.
5. 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.
6. Wright J.A., Keegan K.S., Herendeen D.R., Bentley N.J., Carr A.M., Hoekstra M.F., Concannon P. Protein kinase mutants of human ATR increase sensitivity to UV and ionizing radiation and abrogate cell cycle checkpoint control. Proc. Natl. Acad. Sci. U.S.A. 95:1998;7445-7450.
7. Hartwell L.H., Weinert T.A. Checkpoints: controls that ensure the order of cell cycle events. Science. 246:1989;629-634.
8. Vaugeois J.M. Signal transduction: positive feedback from coffee. Nature. 418:2002;734-736.
9. Busse P.M., Bose S.K., Jones R.W., Tolmach L.J. The action of caffeine on X-irradiated HeLa cells. II. Synergistic lethality. Radiat. Res. 71:1977;666-677.
10. Powell S.N., DeFrank J.S., Connell P., Eogan M., Preffer F., Dombkowski D., Tang W., Friend S. Differential sensitivity of p53(-) and p53(+) cells to caffeine-induced radiosensitization and override of G2 delay. Cancer Res. 55:1995;1643-1648.
11. Nomura T. Similarity of the mechanism of chemical carcinogen-initiated teratogenesis and carcinogenesis in mice. Cancer Res. 37:1977;969-973.
12. Murnane J.P., Byfield J.E., Ward J.F., Calabro-Jones P. Effects of methylated xanthines on mammalian cells treated with bifunctional alkylating agents. Nature. 285:1980;326-329.
13. Murnane J.P., Byfield J.E., Chen C.T., Wang C.H. The structure of methylated xanthines in relation to their effects on DNA synthesis and cell lethality in nitrogen mustard-treated cells. Biophys. J. 35:1981;665-676.
14. Domon M., Rauth A.M. Ultraviolet-light irradiation of mouse L cells: effects on cells in the DNA synthesis phase. Radiat. Res. 40:1969;414-429.
15. V.M. Maher, J.J. McCormick, Effect of DNA repair on the cytotoxicity and mutagenicity of UV irradiation and of chemical carcinogens in normal and xeroderma pigmentosum cells, in: J.M. Yuhas, et al. (Eds.), Biology of Radiation Carcinogensis. Raven Press, New York, 1976, pp. 129-145.
16. Nevaldine B., Longo J.A., Vilenchik M., King G.A., Hahn P.J. Induction and repair of DNA double-strand breaks in the same dose range as the shoulder of the survival curve. Radiat. Res. 140:1994;161-165.
17. Russell K.J., Wiens L.W., Demers G.W., Galloway D.A., Plon S.E., Groudine M. Abrogation of the G2 checkpoint results in differential radiosensitization of G1 checkpoint-deficient and G1 checkpoint-competent cells. Cancer Res. 55:1995;1639-1642.
18. Wang Q., Fan S., Eastman A., Worland P.J., Sausville E.A., O'Connor P.M. UCN-01: a potent abrogator of G2 checkpoint function in cancer cells with disrupted p53. J. Natl. Cancer Inst. 88:1996;956-965.
19. Konze-Thomas B., Hazard R.M., Maher V.M., McCormick J.J. Extent of excision repair before DNA synthesis determines the mutagenic but not the lethal effect of UV radiation. Mutat. Res. 94:1982;421-434.
20. Watanabe M., Maher V.M., McCormick J.J. Excision repair of UV- or benzo[a]pyrene diol epoxide-induced lesions in xeroderma pigmentosum variant cells is 'error free'. Mutat. Res. 146:1985;285-294.
21. Kaufmann W.K. Cell cycle checkpoints and DNA repair preserve the stability of the human genome. Cancer Metastasis Rev. 14:1995;31-41.
22. Cleaver J.E. Common pathways for ultraviolet skin carcinogenesis in the repair and replication defective groups of xeroderma pigmentosum. J. Dermatol. Sci. 23:2000;1-11.
23. Cordeiro-Stone M., Frank A., Bryant M., Oguejiofor I., Hatch S.B., McDaniel L.D., Kaufmann W.K. DNA damage responses protect xeroderma pigmentosum variant from UVC-induced clastogenesis. Carcinogenesis. 23:2002;959-965.
24. Lehmann A.R., Kirk-Bell S., Arlett C.F., Harcourt S.A., de Weerd-Kastelein E.A., Keijzer W., Hall-Smith P. Repair of ultraviolet light damage in a variety of human fibroblast cell strains. Cancer Res. 37:1977;904-910.
25. Heffernan T.P., Simpson D.A., Frank A.R., Heinloth A.N., Paules R.S., Cordeiro-Stone M., Kaufmann W.K. An ATR- and Chk1-dependent S checkpoint inhibits replicon initiation following UVC-induced DNA damage. Mol. Cell Biol. 22:2002;8552-8561.
26. Brown E.J., Baltimore D. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 17:2003;615-628.
27. Casper A.M., Nghiem P., Arlt M.F., Glover T.W. ATR regulates fragile site stability. Cell. 111:2002;779-789.
28. Boyer J.C., Kaufmann W.K., Cordeiro-Stone M. Role of postreplication repair in transformation of human fibroblasts to anchorage independence. Cancer Res. 51:1991;2960-2964.
29. Cistulli C.A., Kaufmann W.K. p53-dependent signaling sustains DNA replication and enhances clonogenic survival in 254 nm ultraviolet-irradiated human fibroblasts. Cancer Res. 58:1998;1993-2002.
30. Kannouche P., Broughton B.C., Volker M., Hanaoka F., Mullenders L.H., Lehmann A.R. Domain structure, localization, and function of DNA polymerase eta, defective in xeroderma pigmentosum variant cells. Genes Dev. 15:2001;158-172.
31. Kaufmann W.K., Levedakou E.N., Grady H.L., Paules R.S., Stein G.H. Attenuation of G2 checkpoint function precedes human cell immortalization. Cancer Res. 55:1995;7-11.
32. Juan G., Traganos F., James W.M., Ray J.M., Roberge M., Sauve D.M., Anderson H., Darzynkiewicz Z. Histone H3 phosphorylation and expression of cyclins A and B1 measured in individual cells during their progression through G2 and mitosis. Cytometry. 32:1998;71-77.
33. Xu B., Kim S.T., Lim D.S., Kastan M.B. Two molecularly distinct G(2)/M checkpoints are induced by ionizing irradiation. Mol. Cell Biol. 22:2002;1049-1059.
34. Yamada A., Masutani C., Iwai S., Hanaoka F. Complementation of defective translesion synthesis and UV light sensitivity in xeroderma pigmentosum variant cells by human and mouse DNA polymerase eta. Nucleic Acids Res. 28:2000;2473-2480.
35. Arlett C.F., Harcourt S.A., Broughton B.C. The influence of caffeine on cell survival in excision-deficient xeroderma pigmentosum and normal human cell strains following ultraviolet-light irradiation. Mutat. Res. 33:1975;341-346.
36. Boyer J.C., Kaufmann W.K., Brylawski B.P., Cordeiro-Stone M. Defective postreplication repair in xeroderma pigmentosum variant fibroblasts. Cancer Res. 50:1990;2593-2598.
37. Busse P.M., Bose S.K., Jones R.W., Tolmach L.J. The action of caffeine on X-irradiated HeLa cells. III. Enhancement of X-ray-induced killing during G2 arrest. Radiat. Res. 76:1978;292-307.
38. Deming P.B., Cistulli C.A., Zhao H., Graves P.R., Piwnica-Worms H., Paules R.S., Downes C.S., Kaufmann W.K. The human decatenation checkpoint. Proc. Natl. Acad. Sci. U.S.A. 98:2001;12044-12049.
39. Zampetti-Bosseler F., Scott D. Cell death, chromosome damage and mitotic delay in normal human, ataxia telangiectasia and retinoblastoma fibroblasts after X-irradiation. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 39:1981;547-558.
40. Paules R.S., Levedakou E.N., Wilson S.J., Innes C.L., Rhodes N., Tlsty T.D., Galloway D.A., Donehower L.A., Tainsky M.A., Kaufmann W.K. Defective G2 checkpoint function in cells from individuals with familial cancer syndromes. Cancer Res. 55:1995;1763-1773.
41. Zhou B.B., Chaturvedi P., Spring K., Scott S.P., Johanson R.A., Mishra R., Mattern M.R., Winkler J.D., Khanna K.K. Caffeine abolishes the mammalian G(2)/M DNA damage checkpoint by inhibiting ataxia-telangiectasia-mutated kinase activity. J. Biol. Chem. 275:2000;10342-10348.
42. Cortez D. Caffeine inhibits checkpoint responses without inhibiting ATM and ATR. J. Biol. Chem. 278:2003;37139-37145.
43. Maher V.M., Ouellette L.M., Curren R.D., McCormick J.J. Frequency of ultraviolet light-induced mutations is higher in xeroderma pigmentosum variant cells than in normal human cells. Nature. 261:1976;593-595.
44. Myhr B.C., Turnbull D., DiPaolo J.A. Ultraviolet mutagenesis of normal and xeroderma pigmentosum variant human fibroblasts. Mutat. Res. 62:1979;341-353.
45. Lehmann A.R. Postreplication repair of DNA in UV-irradiated mammalian cells. Basic Life Sci. 5B:1975;617-623.
46. Lehmann A.R. The relationship between pyrimidine dimers and replicating DNA in UV-irradiated human fibroblasts. Nucleic Acids Res. 7:1979;1901-1912.
47. Lehmann A.R., Kirk-Bell S., Arlett C.F., Paterson M.C., Lohman P.H., de Weerd-Kastelein E.A., Bootsma D. Xeroderma pigmentosum cells with normal levels of excision repair have a defect in DNA synthesis after UV-irradiation. Proc. Natl. Acad. Sci. U.S.A. 72:1975;219-223.
48. Fujiwara Y., Tatsumi M. Replicative bypass repair of ultraviolet damage to DNA of mammalian cells: caffeine sensitive and caffeine resistant mechanisms. Mutat. Res. 37:1976;91-110.
49. Laposa R.R., Feeney L., Cleaver J.E. Recapitulation of the cellular xeroderma pigmentosum-variant phenotypes using short interfering RNA for DNA polymerase H. Cancer Res. 63:2003;3909-3912.
50. 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.
51. Kastan M.B., Onyekwere O., Sidransky D., Volgelstein B., Craig R. Participation of p53 protein in the cellular responses to DNA damage. Cancer Res. 51:1991;6304-6311.
52. Falck J., Mailand N., Syljuasen R.G., Bartek J., Lukas J. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature. 410:2001;842-847.
53. Peng C.Y., Graves P.R., Thoma R.S., Wu Z., Shaw A.S., Piwnica-Worms H. Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science. 277:1997;1501-1505.
54. Donzelli M., Draetta G.F. Regulating mammalian checkpoints through Cdc25 inactivation. EMBO Rep. 4:2003;671-677.
55. Blasina A., de Weyer I.V., Laus M.C., Luyten W.H., Parker A.E., McGowan C.H. A human homologue of the checkpoint kinase Cds1 directly inhibits Cdc25 phosphatase. Curr. Biol. 9:1999;1-10.
56. Jin P., Hardy S., Morgan D.O. Nuclear localization of cyclin B1 controls mitotic entry after DNA damage. J. Cell Biol. 141:1998;875-885.
57. Toyoshima F., Moriguchi T., Wada A., Fukuda M., Nishida E. Nuclear export of cyclin B1 and its possible role in the DNA damage-induced G2 checkpoint. Embo J. 17:1998;2728-2735.
58. Hagting A., Karlsson C., Clute P., Jackman M., Pines J. MPF localization is controlled by nuclear export. Embo. J. 17:1998;4127-4138.
59. Toyoshima-Morimoto F., Taniguchi E., Shinya N., Iwamatsu A., Nishida E. Polo-like kinase 1 phosphorylates cyclin B1 and targets it to the nucleus during prophase. Nature. 410:2001;215-220.
60. Smits V.A., Klompmaker R., Arnaud L., Rijksen G., Nigg E.A., Medema R.H. Polo-like kinase-1 is a target of the DNA damage checkpoint. Nat. Cell Biol. 2:2000;672-676.
61. van Vugt M.A., Smits V.A., Klompmaker R., Medema R.H. Inhibition of Polo-like kinase-1 by DNA damage occurs in an ATM- or ATR-dependent fashion. J. Biol. Chem. 276:2001;41656-41660.
62. Deming P.B., Flores K.G., Downes C.S., Paules R.S., Kaufmann W.K. ATR enforces the topoisomerase II-dependent G2 checkpoint through inhibition of Plk1 kinase. J. Biol. Chem. 277:2002;36832-36838.
63. Tercero J.A., Diffley J.F. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature. 412:2001;553-557.
64. Beetham K.L., Busse P.M., Tolmach L.J. Synergistic killing of HeLa cells by hydroxyurea and caffeine. J. Cell Physiol. 115:1983;283-290.
65. Pardee A.B., James L.J. Selective killing of transformed baby hamster kidney (BHK) cells. Proc. Natl. Acad. Sci. U.S.A. 72:1975;4994-4998.
66. O'Neill F.J. Differential effects of cytochalasin B and caffeine on control of DNA synthesis in normal and transformed cells. J. Cell Physiol. 101:1979;201-217.
67. Beetham K.L., Tolmach L.J. Growth and death of HeLa cells in the presence of caffeine. J. Cell Physiol. 113:1982;385-397.