The NER proteins XPC and CSB, but not ERCC1, regulate the sensitivity to the novel DNA binder S23906: Implications for recognition and repair of antitumor alkylators

Biochemical Pharmacology

Volumn 80, Issue 3, 2010, Pages 335-343

  Rocca, Céline J ^a,b,c   Poindessous, Virginie ^a,b,c   Soares, Daniele G ^a,b,c,d   Ouadrani, Karima El ^a,b,c   Sarasin, Alain ^e,f   Guérin, Eric ^g,h   de Gramont, Aimery ^a,b,c,i   Henriques, João A P ^d   Escargueil, Alexandre E ^a,b,c   Larsen, Annette K ^a,b,c  

^a CENTRE DE RECHERCHE SAINT ANTOINE   (France)

^b INSERM   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^e CNRS   (France)

^f INSTITUT GUSTAVE ROUSSY   (France)

^g HÔPITAL DE HAUTEPIERRE   (France)

^h UNIVERSITÉ DE STRASBOURG   (France)

ⁱ HÔPITAL SAINT ANTOINE   (France)

Author keywords

ERCC1; Monofunctional alkylators; Nucleotide excision repair; S23906; XPC

Indexed keywords

1,2 DIACETOXY 3,14 DIHYDRO 3,3,14 TRIMETHYL 6 METHOXY 7H BENZ[B]PYRANO[3,2 D]ACRIDIN 7 ONE; ANTINEOPLASTIC AGENT; CISPLATIN; COCKAYNE SYNDROME GROUP B PROTEIN; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; HISTONE H2AX; NUCLEIC ACID BINDING PROTEIN; PLASMID DNA; RNA; S 23906; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP A PROTEIN; XERODERMA PIGMENTOSUM GROUP C PROTEIN; XERODERMA PIGMENTOSUM GROUP F PROTEIN;

ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER RESISTANCE; CONTROLLED STUDY; DNA ADDUCT; DNA DAMAGE; DNA STRAND BREAKAGE; DNA SYNTHESIS; DNA TRANSCRIPTION; DRUG SENSITIVITY; EXCISION REPAIR; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; UPREGULATION;

ACRONINE; ALKYLATING AGENTS; ANTINEOPLASTIC AGENTS, ALKYLATING; BINDING SITES; CELL LINE; CELL LINE, TUMOR; DNA; DNA ADDUCTS; DNA HELICASES; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; ENDONUCLEASES; HUMANS; ORPHAN NUCLEAR RECEPTORS; XERODERMA PIGMENTOSUM;

EID: 77953360610     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.04.012     Document Type: Article

References (37)

1. David-Cordonnier M.H., Laine W., Lansiaux A., Rosu F., Colson P., de Pauw E., et al. 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 2005, 4:71-80.
2. David-Cordonnier M.H., Lainé W., Lansiaux A., Kouach M., Briand G., Pierré A., et al. Alkylation of guanine in DNA by S23906-1, a novel potent antitumor compound derived from the plant alkaloid acronycine. Biochemistry 2002, 41:9911-9920.
3. Nguyen Q.C., Nguyen T.T., Yougnia R., Gaslonde T., Dufat H., Michel S., et al. Acronycine derivatives: a promising series of anticancer agents. Anticancer Agents Med Chem 2009, 9:804-815.
4. Léonce S., Kraus-Berthier L., Golsteyn R.M., David-Cordonnier M.H., Tardy C., Lansiaux A., et al. Generation of replication-dependent double-strand breaks by the novel N2-G-alkylator S23906-1. Cancer Res 2006, 66:7203-7210.
5. Soares D.G., Escargueil A.E., Poindessous V., Sarasin A., de Gramont A., Bonatto D., et al. Replication and homologous recombination repair regulate DNA double-strand break formation by the antitumor alkylator ecteinascidin 743. Proc Natl Acad Sci U S A 2007, 104:13062-13067.
6. Cahuzac N., Studény A., Marshall K., Versteege I., Wetenhall K., Pfeiffer B., et al. An unusual DNA binding compound S23906, induces mitotic catastrophe in cultured human cells. Cancer Lett 2009, (September 14). [Epub ahead of print].
7. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 2001, 411:366-374.
8. Volker M., Moné M.J., Karmakar P., van Hoffen A., Schul W., Vermeulen W., et al. Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell 2001, 8:213-224.
9. Riedl T., Hanaoka F., Egly J.M. The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J 2003, 22:5293-5303.
10. Hanawalt P.C., Spivak G. Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol 2008, 9:958-970.
11. Olaussen K.A., Dunant A., Fouret P., Brambilla E., André F., Haddad V., et al. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy. N Engl J Med 2006, 355:983-991.
12. Bhagwat N.R., Roginskaya V.Y., Acquafondata M.B., Dhir R., Wood R.D., Niedernhofer L.J. Immunodetection of DNA repair endonuclease ERCC1-XPF in human tissue. Cancer Res 2009, 69:6831-6838.
13. Jaspers N.G., Raams A., Kelner M.J., Ng J.M., Yamashita Y.M., Takeda S., et al. Anti-tumour compounds illudin S and Irofulven induce DNA lesions ignored by global repair and exclusively processed by transcription- and replication-coupled repair pathways. DNA Repair (Amst) 2002, 1:1027-1038.
14. Koeppel F., Poindessous V., Lazar V., Raymond E., Sarasin A., Larsen A.K. Irofulven cytotoxicity depends on transcription-coupled nucleotide excision repair and is correlated with XPG expression in solid tumor cells. Clin Cancer Res 2004, 10:5604-5613.
15. Escargueil A.E., Poindessous V., Soares D.G., Sarasin A., Cook P.R., Larsen A.K. Influence of irofulven, a transcription-coupled repair-specific antitumor agent, on RNA polymerase activity, stability and dynamics in living mammalian cells. J Cell Sci 2008, 121:1275-1283.
16. Poindessous V., Koeppel F., Raymond E., Comisso M., Waters S.J., Larsen A.K. Marked activity of irofulven toward human carcinoma cells: comparison with cisplatin and ecteinascidin. Clin Cancer Res 2003, 9:2817-2825.
17. Damia G., Silvestri S., Carrassa L., Filiberti L., Faircloth G.T., Liberi G., et al. Unique pattern of ET-743 activity in different cellular systems with defined deficiencies in DNA-repair pathways. Int J Cancer 2001, 92:583-588.
18. Herrero A.B., Martín-Castellanos C., Marco E., Gago F., Moreno S. Cross-talk between nucleotide excision and homologous recombination DNA repair pathways in the mechanism of action of antitumor trabectedin. Cancer Res 2006, 66:8155-8162.
19. Jaspers N.G., Raams A., Silengo M.C., Wijgers N., Niedernhofer L.J., Robinson A.R., et al. First reported patient with human ERCC1 deficiency has cerebro-oculo-facio-skeletal syndrome with a mild defect in nucleotide excision repair and severe developmental failure. Am J Hum Genet 2007, 80:457-466.
20. Olive P.L., Banáth J.P. The comet assay: a method to measure DNA damage in individual cells. Nat Protoc 2006, 1:23-29.
21. Mori T., Nakane M., Hattori T., Matsunaga T., Ihara M., Nikaido O. Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6-4)photoproduct from the same mouse immunized with ultraviolet-irradiated DNA. Photochem Photobiol 1991, 54:225-232.
22. Salles B., Provot C., Calsou P., Hennebelle I., Gosset I., Fournié G.J. A chemiluminescent microplate assay to detect DNA damage induced by genotoxic treatments. Anal Biochem 1995, 232:37-42.
23. Pencreach E., Guérin E., Nicolet C., Lelong-Rebel I., Voegeli A.C., Oudet P., et al. Marked activity of irinotecan and rapamycin combination toward colon cancer cells in vivo and in vitro is mediated through cooperative modulation of the mammalian target of rapamycin/hypoxia-inducible factor-1alpha axis. Clin Cancer Res 2009, 15:1297-1307.
24. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 33:research 0034.1-0034.11.
25. Viguier J., Boige V., Miquel C., Pocard M., Giraudeau B., Sabourin J.C., et al. ERCC1 codon 118 polymorphism is a predictive factor for the tumor response to oxaliplatin/5-fluorouracil combination chemotherapy in patients with advanced colorectal cancer. Clin Cancer Res 2005, 11:6212-6217.
26. Yasuda G., Nishi R., Watanabe E., Mori T., Iwai S., Orioli D., et al. In vivo destabilization and functional defects of the xeroderma pigmentosum C protein caused by a pathogenic missense mutation. Mol Cell Biol 2007, 27:6606-6614.
27. Min J.H., Pavletich N.P. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 2007, 449:570-575.
28. Camenisch U., Träutlein D., Clement F.C., Fei J., Leitenstorfer A., Ferrando-May E., et al. Two-stage dynamic DNA quality check by xeroderma pigmentosum group C protein. EMBO J 2009, 28:2387-2399.
29. Gossage L., Madhusudan S. Current status of excision repair cross complementing-group 1 (ERCC1) in cancer. Cancer Treat Rev 2007, 33:565-577.
30. McHugh P.J., Spanswick V.J., Hartley J.A. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol 2001, 2:483-490.
31. Niedernhofer L.J., Odijk H., Budzowska M., van Drunen E., Maas A., Theil A.F., et al. The structure-specific endonuclease ERCC1-XPF is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol Cell Biol 2004, 24:5776-5787.
32. Al-Minawi A.Z., Saleh-Gohari N., Helleday T. The ERCC1/XPF endonuclease is required for efficient single-strand annealing and gene conversion in mammalian cells. Nucleic Acids Res 2008, 36:1-9.
33. Ahmad A., Robinson A.R., Duensing A., van Drunen E., Beverloo H.B., Weisberg D.B., et al. ERCC1-XPF endonuclease facilitates DNA double-strand break repair. Mol Cell Biol 2008, 28:5082-5092.
34. Bhagwat N., Olsen A.L., Wang A.T., Hanada K., Stuckert P., Kanaar R., et al. XPF-ERCC1 participates in the Fanconi anemia pathway of cross-link repair. Mol Cell Biol 2009, 29:6427-6437.
35. Zhu X.D., Niedernhofer L., Kuster B., Mann M., Hoeijmakers J.H., de Lange T. ERCC1/XPF removes the 3' overhang from uncapped telomeres and represses formation of telomeric DNA-containing double minute chromosomes. Mol Cell 2003, 12:1489-1498.
36. Muñoz P., Blanco R., Flores J.M., Blasco M.A. XPF nuclease-dependent telomere loss and increased DNA damage in mice overexpressing TRF2 result in premature aging and cancer. Nat Genet 2005, 37:1063-1071.
37. Ishibashi T., Lippard S.J. Telomere loss in cells treated with cisplatin. Proc Natl Acad Sci U S A 1998, 95:4219-4223.