Hedamycin, a DNA alkylator, induces γH2AX and chromosome aberrations: Involvement of phosphatidylinositol 3-kinase-related kinases and DNA replication fork movement

Molecular Cancer Therapeutics

Volumn 4, Issue 8, 2005, Pages 1175-1185

  Tu, Lan Chun ^a   Matsui, Sei Ichi ^a   Beerman, Terry A ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 [5 (4 METHYL 1 PIPERAZINYL)[2,5' BI 1H BENZIMIDAZOL] 2' YL]PHENOL; ADOZELESIN; APHIDICOLIN; ATR PROTEIN; CAFFEINE; CAMPTOTHECIN; CELL NUCLEUS DNA; DEMECOLCINE; HEDAMYCIN; HISTONE H2A; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR;

ARTICLE; CARCINOMA CELL; CELL STRAIN HCT116; CONTROLLED STUDY; DNA ALKYLATION; DNA DAMAGE; DNA REPLICATION; DNA STRAND BREAKAGE; DRUG MECHANISM; GENOTOXICITY; HUMAN; HUMAN CELL; INTERPHASE; METAPHASE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; ULTRAVIOLET RADIATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANTHRAQUINONES; ANTIGENS, NUCLEAR; ANTINEOPLASTIC AGENTS, ALKYLATING; CAFFEINE; CELL CYCLE PROTEINS; CELL NUCLEUS; CHROMOSOME ABERRATIONS; DNA DAMAGE; DNA REPLICATION; DNA-BINDING PROTEINS; HISTONES; HUMANS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; TUMOR CELLS, CULTURED;

EID: 23844490743     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-05-0054     Document Type: Article

References (49)

1. Norbury CJ, Hickson ID. Cellular responses to DNA damage. Annu Rev Pharmacol Toxicol 2001;41:367-401.
2. Lundin C, Erixon K, Arnaudeau C, et al. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol Cell Biol 2002;22:5869-78.
3. Pourquier P, Pommier Y. Topoisomerase I-mediated DNA damage. Adv Cancer Res 2001;80:189-216.
4. Shiloh Y. ATM and ATR: networking cellular responses to DNA damage. Curr Opin Genet Dev 2001;11:71-7.
5. Michel B, Ehrlich SD, Uzest M. DNA double-strand breaks caused by replication arrest. EMBO J 1997;16:430-8.
6. Weinert T. DNA damage and checkpoint pathways: molecular anatomy and interactions with repair. Cell 1998;94:555-8.
7. Shechter D, Costanzo V, Gautier J. Regulation of DNA replication by ATR: signaling in response to DNA intermediates. DNA Repair (Amst) 2004;3:901-8.
8. Laiho M, Latonen L. Cell cycle control, DNA damage checkpoints and cancer. Ann Med 2003;35:391-7.
9. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998;273:5858-68.
10. Rogakou EP, Boon C, Redon C, Bonner WM. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 1999;146:905-16.
11. D'Amours D, Jackson SP. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat Rev Mol Cell Biol 2002;3: 317-27.
12. Paull TT, Rogakou EP, Yamazaki V, et al. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 2000;10:886-95.
13. Smith R, Kao GD. Pictures, progress, and perplexities: the immediate cell biological effects of ionizing radiation. Cancer Biol Ther 2004;3:602-7. Epub 2004 July 21.
14. Pasero P, Shimada K, Duncker BP. Multiple roles of replication forks in S phase checkpoints: sensors, effectors and targets. Cell Cycle 2003;2:568-72.
15. Larner JM, Lee H, Little RD, et al. Radiation down-regulates replication origin activity throughout the S phase in mammalian cells. Nucleic Acids Res 1999;27:803-9.
16. Tercero JA, Diffley JF. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 2001;412:553-7.
17. Ward IM, Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 2001;276:47759-62.
18. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 2001;276:42462-7.
19. Abraham RT. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 2001;15:2177-96.
20. Giannattasio M, Lazzaro F, Longhese MP, Plevani P, Muzi-Falconi M. Physical and functional interactions between nucleotide excision repair and DNA damage checkpoint. EMBO J 2004;23:429-38.
21. Paulovich AG, Toczyski DP, Hartwell LH. When checkpoints fail. Cell 1997;88:315-21.
22. Strumberg D, Pilon AA, Smith M, et al. Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 5′-phosphorylated DNA double-strand breaks by replication runoff. Mol Cell Biol 2000;20:3977-87.
23. Furuta T, Takemura H, Liao ZY, et al. Phosphorylation of histone H2AX and activation of Mre11, Rad50, and Nbs1 in response to replication-dependent DNA double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J Biol Chem 2003;278: 20303-12.
24. Liu JS, Kuo SR, Melendy T. Comparison of checkpoint responses triggered by DNA polymerase inhibition versus DNA damaging agents. Mutat Res 2003;532:215-26.
25. Tu LC, Melendy T, Beerman TA. DNA damage responses triggered by a highly cytotoxic monofunctional DNA alkylator, hedamycin, a pluramycin antitumor antibiotic. Mol Cancer Ther 2004;3:577-85.
26. Hansen M, Yun S, Hurley L. Hedamycin intercalates the DNA helix and, through carbohydrate-mediated recognition in the minor groove, directs N7-alkylation of guanine in the major groove in a sequence-specific manner. Chem Biol 1995;2:229-40.
27. Casper AM, Nghiem P, Arlt MF, Glover TW. ATR regulates fragile site stability. Cell 2002;111:779-89.
28. Collins AR, Dusinska M, Horska A. Detection of alkylation damage in human lymphocyte DNA with the comet assay. Acta Biochim Pol 2001;48: 611-4.
29. Cortes F, Morgan WF, Wolff S. Effect of exogenous thymidine on sister-chromatid exchange frequency in Chinese hamster ovary cells with bromodeoxyuridine- and chlorodeoxyuridine-substituted chromosomes. Mutat Res 1987;192:277-82.
30. Cleaver JE, Laposa RR, Limoli CL. DNA replication in the face of (in)surmountable odds. Cell Cycle 2003;2:310-5.
31. Pommier Y, Redon C, Rao VA, et al. Repair of and checkpoint response to topoisomerase I-mediated DNA damage. Mutat Res 2003;532:173-203.
32. Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 2000;275:9390-5.
33. Durocher D, Jackson SP. DNA-PK, ATM, ATR. as sensors of DNA damage: variations on a theme? Curr Opin Cell Biol 2001;13:225-31.
34. Cortez D. Caffeine inhibits checkpoint responses without inhibiting the ataxia-telangiectasia-mutated (ATM) and ATM- and Rad3-related (ATR) protein kinases. J Biol Chem 2003;278:37139-45.
35. McGowan CH. Running into problems: how cells cope with replicating damaged DNA. Mutat Res 2003;532:75-84.
36. Iliakis G, Wang H, Perrault AR, et al. Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet Genome Res 2004;104:14-20.
37. Lieber MR, Ma Y, Pannicke U, Schwarz K. Mechanism and regulation of human non-homologous DNA end-joining. Nat Rev Mol Cell Biol 2003;4:712-20.
38. Koike M, Ikuta T, Miyasaka T, Shiomi T. Ku80 can translocate to the nucleus independent of the translocation of Ku70 using its own nuclear localization signal. Oncogene 1999;18:7495-505.
39. Fewell JW, Kuff EL. Intracellular redistribution of Ku immunoreactivity in response to cell-cell contact and growth modulating components in the medium. J Cell Sci 1996;109:1937-46.
40. Nyberg KA, Michelson RJ, Putnam CW, Weinert TA. Toward maintaining the genome: DNA damage and replication checkpoints. Annu Rev Genet 2002;36:617-56.
41. Chen Y, Sanchez Y. Chk1 in the DNA damage response: conserved roles from yeasts to mammals. DNA Repair (Amst) 2004;3:1025-32.
42. Feijoo C, Hall-Jackson C, Wu R, et al. Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J Cell Biol 2001;154:913-23.
43. Modesti M, Kanaar R. DNA repair: spot(light)s on chromatin. Curr Biol 2001;11:R229-32.
44. Heffernan TP, Simpson DA, Frank AR, et al. An ATR- and Chk1-dependent S checkpoint inhibits replicon initiation following UVC-induced DNA damage. Mol Cell Biol 2002;22:8552-61.
45. Huang X, Okafuji M, Traganos F, et al. Assessment of histone H2AX phosphorylation induced by DNA topoisomerase I and II inhibitors topotecan and mitoxantrone and by the DNA cross-linking agent cisplatin. Cytometry A 2004;58A:99-110.
46. Bassing CH, Alt FW. The cellular response to general and programmed DNA double strand breaks. DNA Repair (Amst) 2004;3: 781-96.
47. Matsumoto L, Kurek K, Larocque K, et al. Biological effects of a bifunctional DNA crosslinker. I. Generation of triradial and quadriradial chromosomes. Mutat Res 1999;426:79-87.
48. Downs JA, Jackson SP. A means to a DNA end: the many roles of Ku. Nat Rev Mol Cell Biol 2004;5:367-78.
49. Bree RT, Neary C, Samali A, Lowndes NF. The switch from survival responses to apoptosis after chromosomal breaks. DNA Repair (Amst) 2004;3:989-95.