An unusual DNA binding compound, S23906, induces mitotic catastrophe in cultured human cells

Cancer Letters

Volumn 289, Issue 2, 2010, Pages 178-187

  Cahuzac, Nathalie ^a   Studény, Aurélie ^a   Marshall, Kris ^b   Versteege, Isabella ^a   Wetenhall, Kate ^a   Pfeiffer, Bruno ^a   Léonce, Stéphane ^a   Hickman, John A ^a   Pierré, Alain ^a   Golsteyn, Roy M ^a,b  

^a INSTITUT DE RECHERCHES SERVIER   (France)

^b UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Cdk1; Checkpoint adaptation; Checkpoint kinase 1; Cyclin dependent kinases; Cytotoxic drug; DNA damage response; Histone H2AX

Indexed keywords

ALKYLATING AGENT; BLEOMYCIN; CAFFEINE; CAMPTOTHECIN; CELL ANTIGEN; CHECKPOINT KINASE 1; CISPLATIN; CYCLIN B1; CYCLIN DEPENDENT KINASE; CYCLIN E1; GAMMA HISTONE H2AX; HISTONE H2AX; S 23906; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN HT29; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DNA BINDING; DNA DAMAGE; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MICROSCOPY; MITOSIS INHIBITION; PRIORITY JOURNAL; RNA INTERFERENCE; WESTERN BLOTTING;

ACRONINE; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, NORTHERN; CAFFEINE; CDC2 PROTEIN KINASE; CYCLIN B1; CYCLIN E; DNA; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HT29 CELLS; HUMANS; MITOSIS; ONCOGENE PROTEINS; RNA, SMALL INTERFERING;

EID: 76849088397     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2009.08.014     Document Type: Article

References (39)

1. Fernandez-Capetillo O., Chen H.-T., Celeste A., Ward I., Romanienko P.J., Morales J.C., Naka K., Xia Z., Camerini-Otero D., Motoyama N., Carpenter P.B., Bonner W.M., Chen J., and Nussenzweig A. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nature Cell Biol. 4 (2002) 993-997
2. Lukas C., Falck J., Bartkova J., Bartek J., and Lukas J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nature Cell Biol. 5 (2003) 255-260
3. Zhao H., and Piwnica-Worms H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol. Cell. Biol. 21 (2001) 4129-4139
4. Kurz E.U., and Lees-Miller S.P. DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Repair 3 (2004) 889-900
5. Furnari B., Rhind N., and Russell P. Cdc25 mitotic inducer targeted by Chk1 DNA damage checkpoint kinase. Science 277 (1997) 1495-1497
6. Sanchez Y., Wong C., Thoma R.S., Richman R., Wu Z., Piwnica-worms H., and Elledge S.J. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through CDC25. Science 277 (1997) 1497-1501
7. Mailand N., Falck J., Lukas C., Syljuasen R.G., Welcker M., Bartek J., and Lukas J. Rapid destruction of human Cdc25A in response to DNA damage. Science 288 (2000) 1425-1429
8. Ayscough K., Hayles J., MacNeill S.A., and Nurse P. Cold-sensitive mutants of p34cdc2 that suppress a mitotic catastrophe phenotype in fission yeast. Mol. Gen. Genet. 232 (1992) 344-350
9. Ricci M.S., and Zong W.X. Chemotherapeutic approaches for targeting cell death pathways. Oncologist 11 (2006) 342-357
10. Borgne A., and Golsteyn R.M. The role of cyclin-dependent kinases in apoptosis. In: Meijer L., Jézéquel A., and Roberge M. (Eds). Progress in Cell Cycle Research. Life in Progress Editions (2003), Roscoff, France 453-459
11. Castedo M., Perfettini J.-L., Roumier T., Andreau K., Medema R., and Kroemer G. Cell death by mitotic catastrophe: a molecular definition. Oncogene 23 (2004) 2825-2837
12. Vakifahmetoglu H., Olsson M., and Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ. 15 (2008) 1153-1162
13. Léonce S., Perez V., Lambel S., Peyroulan D., Tillequin F., Michel S., Koch M., Pfeiffer B., Atassi G., Hickman J.A., and Pierré A. Induction of cyclin E and inhibition of DNA synthesis by the novel acronycine derivative S 23906-1 precede the irreversible arrest of tumor cells in S-phase leading to apoptosis. Mol. Pharmacol. 60 (2001) 1383-1391
14. Leonce S., Kraus-Berthier L., Golsteyn R.M., David-Cordonnier M.H., Tardy C., Lansiaux A., Poindessous V., Larsen A.K., and Pierre A. Generation of replication-dependent double-strand breaks by the novel N2-G-alkylator S23906-1. Cancer Res. 66 (2006) 7203-7210
15. Guilbaud N., Kraus-Berthier L., Meyer-Losic F., Malivet V., Chacun C., Jan M., Tillequin F., Michel S., Koch M., Pfeiffer B., Atassi G., Hickman J.A., and Pierré A. Marked antitumour activity of a new potent acronycine derivative in orthotopic models of human solid tumors. Clin. Cancer Res. 7 (2001) 2573-2580
16. Syljuasen R.G., Sorensen C.S., Nylandsted J., Lukas C., Lukas J., and Bartek J. Inhibition of Chk1 by CEP-3891 accelerates mitotic nuclear fragmentation in response to ionizing radiation. Cancer Res. 64 (2004) 9035-9040
17. Holgersson A., Heiden T., Castro J., Edgren M.R., Lewensohn R., and Meijer A.E. Different G2/M accumulation in M059J and M059K cells after exposure to DNA double-strand break-inducing agents. Int. J. Radiat. Oncol. Biol. Phys. 61 (2005) 915-921
18. Tse A.N., and Schwartz G.K. Potentiation of cytotoxicity of topoisomerase I poison by concurrent and sequential treatment with the checkpoint inhibitor UCN-01 involves disparate mechanisms resulting in either p53-independent clonogenic suppression or p53-dependent mitotic catastrophe. Cancer Res. 64 (2004) 6635-6644
19. Borgne A., Versteege I., Mahe M., Studeny A., Leonce S., Naime I., Rodriguez M., Hickman J.A., Meijer L., and Golsteyn R.M. Analysis of cyclin B1 and CDK activity during apoptosis induced by camptothecin treatment. Oncogene 25 (2006) 7361-7372
20. Vakifahmetoglu H., Olsson M., Tamm C., Heidari N., Orrenius S., and Zhivotovsky B. DNA damage induces two distinct modes of cell death in ovarian carcinomas. Cell Death Differ. 7 (2007) 7
21. Vakifahmetoglu H., Olsson M., and Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ. 15 (2008) 1153-1162
22. Sarkaria J.N., Busby E.C., Tibbetts R.S., Roos P., Taya Y., Karnitz L.M., and Abraham R.T. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59 (1999) 4375-4382
23. Léonce S., Perez V., Casabianca-Pignède M.R., Anstett M., Bisagni E., and Pierré A.A.G. In vitro cytotoxicity of S16020-2, a new olivacine derivative. Invest. New Drugs (1996) 169-180
24. Elbashir S.M., Harborth J., Weber K., and Tuschl T. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 26 (2002) 199-213
25. David-Cordonnier M.H., Laine W., Lansiaux A., Kouach M., Briand C., Pierré A., Hickman J.A., and Bailly C. Alkylation of guanine in DNA by S 23906-1, a novel potent antitumor compound derived from the plant alkaloid acronycine. Biochemistry 41 (2002) 9911-9920
26. Bosco E.E., Mayhew C.N., Hennigan R.F., Sage J., Jacks T., and Knudsen E.S. RB signaling prevents replication-dependent DNA double-strand breaks following genotoxic insult. Nucleic Acids Res. 32 (2004) 25-34
27. Furuta T., Takemura H., Liao Z.Y., Aune G.J., Redon C., Sedelnikova O.A., Pilch D.R., Rogakou E.P., Celeste A., Chen H.T., Nussenzweig A., Aladjem M.I., Bonner W.M., and Pommier Y. 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. 278 (2003) 20303-20312
28. Tomilin N.V., Solovjeva L.V., Svetlova M.P., Pleskach N.M., Zalenskaya I.A., Yau P.M., and Bradbury E.M. Visualization of focal nuclear sites of DNA repair synthesis induced by bleomycin in human cells. Radiat. Res. 156 (2001) 347-354
29. Wang J., Wiltshire T., Wang Y., Mikell C., Burks J., Cunningham C., Van Laar E.S., Waters S.J., Reed E., and Wang W. ATM-dependent CHK2 activation induced by anticancer agent, irofulven. J. Biol. Chem. 279 (2004) 39584-39592
30. Zhou B.B., Chaturvedi P., Spring K., Scott S.P., Johanson R.A., Mishra R., Mattern M.R., Winkler J.D., and 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
31. Pommier Y., Kohlhagen G., Bailly C., Waring M., Mazumder A., and Kohn K.W. DNA sequence- and structure-selective alkylation of guanine N2 in the DNA minor groove by ecteinascidin 743, a potent antitumor compound from the Caribbean tunicate Ecteinascidia turbinata. Biochemistry 35 (1996) 13303-13309
32. David-Cordonnier M.H., Laine W., Lansiaux A., Rosu F., Colson P., de Pauw E., Michel S., Tillequin F., Koch M., Hickman J.A., Pierre A., and Bailly C. Covalent binding of antitumor benzoacronycines to double-stranded DNA induces helix opening and the formation of single-stranded DNA: unique consequences of a novel DNA-bonding mechanism. Mol. Cancer Ther. 4 (2005) 71-80
33. Lopez-Larraza D., De Luca J.C., and Bianchi N.O. The kinetics of DNA damage by bleomycin in mammalian cells. Mutat. Res. 232 (1990) 57-61
34. Nazarov I.B., Smirnova A.N., Krutilina R.I., Svetlova M.P., Solovjeva L.V., Nikiforov A.A., Oei S.L., Zalenskaya I.A., Yau P.M., Bradbury E.M., and Tomilin N.V. Dephosphorylation of histone gamma-H2AX during repair of DNA double-strand breaks in mammalian cells and its inhibition by calyculin A. Radiat. Res. 160 (2003) 309-317
35. Porter L.A., Singh G., and Lee J.M. Abundance of cyclin B1 regulates γ-radiation-induced apoptosis. Blood 95 (2000) 2645-2650
36. Castedo M., Perfettini J.L., Roumier T., and Kroemer G. Cyclin-dependent kinase-1: linking apoptosis to cell cycle and mitotic catastrophe. Cell Death Differ. 9 (2002) 1287-1293
37. Golsteyn R.M. Cdk1 and Cdk2 complexes (cyclin dependent kinases) in apoptosis: a role beyond the cell cycle. Cancer Lett. 217 (2005) 129-138
38. Chen T., Hevi S., Gay F., Tsujimoto N., He T., Zhang B., Ueda Y., and Li E. Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nat. Genet. 39 (2007) 391-396
39. Ramalingam S., Natarajan G., Schafer C., Subramaniam D., May R., Ramachandran I., Queimado L., Houchen C.W., and Anant S. Novel intestinal splice variants of RNA binding protein CUGBP2: isoform specific effects on mitotic catastrophe. Am. J. Physiol. Gastrointest. Liver Physiol. 7 (2008) 971-981