Differential contributory roles of nucleotide excision and homologous recombination repair for enhancing cisplatin sensitivity in human ovarian cancer cells

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Wang, Qi En ^a   Milum, Keisha ^a   Han, Chunhua ^a   Huang, Yi Wen ^b   Wani, Gulzar ^a   Thomale, Jürgen ^c   Wani, Altaf A ^a,b,d  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

^d KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA2 PROTEIN; CISPLATIN; DNA; MESSENGER RNA; TUMOR PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL; DNA CROSS LINKING; DNA REPAIR; DOWN REGULATION; DRUG ACTIVITY; DRUG SENSITIVITY; EXCISION REPAIR; GENE EXPRESSION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; OVARY CANCER; DOSE RESPONSE; DRUG EFFECT; DRUG RESISTANCE; DRUG SCREENING; FEMALE; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; GENETICS; METABOLISM; OVARY TUMOR; PATHOLOGY; TUMOR CELL LINE;

BRCA2 PROTEIN; CELL LINE, TUMOR; CISPLATIN; DNA REPAIR; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM PROTEINS; OVARIAN NEOPLASMS; RECOMBINATION, GENETIC; RNA, MESSENGER;

EID: 79952355824     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-24     Document Type: Article

References (43)

1. Cohen SM, Lippard SJ. Cisplatin: from DNA damage to cancer chemotherapy. Prog Nucleic Acid Res Mol Biol 2001, 67:93-130. full_text, 11525387.
2. Jung Y, Lippard SJ. Direct cellular responses to platinum-induced DNA damage. Chem Rev 2007, 107:1387-1407. 10.1021/cr068207j, 17455916.
3. Kartalou M, Essigmann JM. Recognition of cisplatin adducts by cellular proteins. Mutat Res 2001, 478:1-21. 10.1016/S0027-5107(01)00142-7, 11406166.
4. Huang JC, Zamble DB, Reardon JT, Lippard SJ, Sancar A. HMG-domain proteins specifically inhibit the repair of the major DNA adduct of the anticancer drug cisplatin by human excision nuclease. pnas 1994, 91:10394-10398. 10.1073/pnas.91.22.10394, 45026, 7937961.
5. Zamble DB, Mu D, Reardon JT, Sancar A, Lippard SJ. Repair of cisplatin-DNA adducts by the mammalian excision nuclease. Biochemistry 1996, 35:10004-10013. 10.1021/bi960453+, 8756462.
6. McHugh PJ, Spanswick VJ, Hartley JA. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol 2001, 2:483-490. 10.1016/S1470-2045(01)00454-5, 11905724.
7. Petit C, Sancar A. Nucleotide excision repair: From E.coli to man. Biochimie 1999, 81:15-25. 10.1016/S0300-9084(99)80034-0, 10214906.
8. Araujo SJ, Tirode F, Coin F, Pospiech H, Syvaoja JE, Stucki M, Hubscher U, Egly JM, Wood RD. Nucleotide excision repair of DNA with recombinant human proteins: definition of the minimal set of factors, active forms of TFIIH, and modulation by CAK. Genes Dev 2000, 14:349-359. 316364, 10673506.
9. Araujo SJ, Nigg EA, Wood RD. Strong functional interactions of TFIIH with XPC and XPG in human DNA nucleotide excision repair, without a preassembled repairosome. Mol Cell Biol 2001, 21:2281-2291. 10.1128/MCB.21.7.2281-2291.2001, 86862, 11259578.
10. Volker M, Mone MJ, Karmakar P, Van Hoffen A, Schul W, Vermeulen W, Hoeijmakers JH, van Driel R, van Zeeland AA, Mullenders LH. Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell 2001, 8:213-224. 10.1016/S1097-2765(01)00281-7, 11511374.
11. Sugasawa K, Ng JMY, Masutani C, Iwai S, Van der Spek P, Eker A, Hanaoka F, Bootsma D, Hoeijmakers JH. Xeroderma pigmentosum group C complex is the initiator of global genome nucleotide excision repair. Mol Cell 1998, 2:223-232. 10.1016/S1097-2765(00)80132-X, 9734359.
12. Moynahan ME, Pierce AJ, Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol Cell 2001, 7:263-272. 10.1016/S1097-2765(01)00174-5, 11239455.
13. Sakai W, Swisher EM, Jacquemont C, Chandramohan KV, Couch FJ, Langdon SP, Wurz K, Higgins J, Villegas E, Taniguchi T. Functional restoration of BRCA2 protein by secondary BRCA2 mutations in BRCA2-mutated ovarian carcinoma. Cancer Res 2009, 69:6381-6386. 10.1158/0008-5472.CAN-09-1178, 2754824, 19654294.
14. Chetrit A, Hirsh-Yechezkel G, Ben-David Y, Lubin F, Friedman E, Sadetzki S. Effect of BRCA1/2 mutations on long-term survival of patients with invasive ovarian cancer: the national Israeli study of ovarian cancer. J Clin Oncol 2008, 26:20-25. 10.1200/JCO.2007.11.6905, 18165636.
15. Saldivar JS, Wu X, Follen M, Gershenson D. Nucleotide excision repair pathway review I: implications in ovarian cancer and platinum sensitivity. Gynecol Oncol 2007, 107:S56-S71. 10.1016/j.ygyno.2007.07.043, 17884153.
16. Johnson SW, Perez RP, Godwin AK, Yeung AT, Handel LM, Ozols RF, Hamilton TC. Role of platinum-DNA adduct formation and removal in cisplatin resistance in human ovarian cancer cell lines. Biochem Pharmacol 1994, 47:689-697. 10.1016/0006-2952(94)90132-5, 8129746.
17. Masuda H, Tanaka T, Matsuda H, Kusaba I. Increased removal of DNA-bound platinum in a human ovarian cancer cell line resistant to cis-diamminedichloroplatinum(II). Cancer Res 1990, 50:1863-1866.
18. Parker RJ, Eastman A, Bostick-Bruton F, Reed E. Acquired cisplatin resistance in human ovarian cancer cells is associated with enhanced repair of cisplatin-DNA lesions and reduced drug accumulation. J Clin Invest 1991, 87:772-777. 10.1172/JCI115080, 329864, 1999494.
19. Masuda H, Ozols RF, Lai GM, Fojo A, Rothenberg M, Hamilton TC. Increased DNA repair as a mechanism of acquired resistance to cis-diamminedichloroplatinum(II) in human ovarian cancer cell lines. Cancer Res 1988, 48:5713-5716.
20. Barakat BM, Wang QE, Han C, Milum K, Yin DT, Zhao Q, Wani G, Arafa E, El-Mahdy MA, Wani AA. Overexpression of DDB2 enhances the sensitivity of human ovarian cancer cells to cisplatin by augmenting cellular apoptosis. Int J Cancer 2010, 127:977-988.
21. Koc A, Wheeler LJ, Mathews CK, Merrill GF. Hydroxyurea arrests DNA replication by a mechanism that preserves basal dNTP pools. J Biol Chem 2004, 279:223-230. 10.1074/jbc.M303952200, 14573610.
22. Lehmann AR, Stevens S. A rapid procedure for measurement of DNA repair in human fibroblasts and for complementation analysis of xeroderma pigmentosum cells. Mutat Res 1980, 69:177-190. 10.1016/0027-5107(80)90187-6, 6987495.
23. Liedert B, Pluim D, Schellens J, Thomale J. Adduct-specific monoclonal antibodies for the measurement of cisplatin-induced DNA lesions in individual cell nuclei. Nucleic Acids Res 2006, 34:e47. 10.1093/nar/gkl051, 1420801, 16571898.
24. Wang QE, Zhu Q, Wani G, El-Mahdy MA, Li J, Wani AA. DNA repair factor XPC is modified by SUMO-1 and ubiquitin following UV irradiation. Nucleic Acids Res 2005, 33:4023-4034. 10.1093/nar/gki684, 1178000, 16030353.
25. Sakai W, Swisher EM, Karlan BY, Agarwal MK, Higgins J, Friedman C, Villegas E, Jacquemont C, Farrugia DJ, Couch FJ, Urban H, Taniguchi T. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature 2008, 451:1116-1120. 10.1038/nature06633, 2577037, 18264087.
26. Stewart DJ. Mechanisms of resistance to cisplatin and carboplatin. Crit Rev Oncol Hematol 2007, 63:12-31. 10.1016/j.critrevonc.2007.02.001, 17336087.
27. Arora S, Kothandapani A, Tillison K, Kalman-Maltese V, Patrick SM. Downregulation of XPF-ERCC1 enhances cisplatin efficacy in cancer cells. DNA Repair (Amst) 2010, 9:745-753. 10.1016/j.dnarep.2010.03.010, 20418188.
28. Martin LP, Hamilton TC, Schilder RJ. Platinum resistance: the role of DNA repair pathways. Clin Cancer Res 2008, 14:1291-1295. 10.1158/1078-0432.CCR-07-2238, 18316546.
29. Ferry KV, Hamilton TC, Johnson SW. Increased nucleotide excision repair in cisplatin-resistant ovarian cancer cells: role of ERCC1-XPF. Biochem Pharmacol 2000, 60:1305-1313. 10.1016/S0006-2952(00)00441-X, 11008124.
30. Selvakumaran M, Pisarcik DA, Bao R, Yeung AT, Hamilton TC. Enhanced cisplatin cytotoxicity by disturbing the nucleotide excision repair pathway in ovarian cancer cell lines. Cancer Res 2003, 63:1311-1316.
31. Wu X, Fan W, Xu S, Zhou Y. Sensitization to the cytotoxicity of cisplatin by transfection with nucleotide excision repair gene xeroderma pigmentosun group A antisense RNA in human lung adenocarcinoma cells. Clin Cancer Res 2003, 9:5874-5879.
32. Orelli B, McClendon TB, Tsodikov OV, Ellenberger T, Niedernhofer LJ, Scharer OD. The XPA-binding domain of ERCC1 is required for nucleotide excision repair but not other DNA repair pathways. J Biol Chem 2010, 285:3705-3712. 10.1074/jbc.M109.067538, 2823511, 19940136.
33. Usanova S, Piee-Staffa A, Sied U, Thomale J, Schneider A, Kaina B, et al. Cisplatin sensitivity of testis tumour cells is due to deficiency in interstrand-crosslink repair and low ERCC1-XPF expression. Mol Cancer 2010, 9:248. 10.1186/1476-4598-9-248, 20846399.
34. Johnson SW, Swiggard PA, Handel LM, Brennan JM, Godwin AK, Ozols RF, Hamilton TC. Relationship between platinum-DNA adduct formation and removal and cisplatin cytotoxicity in cisplatin-sensitive and -resistant human ovarian cancer cells. Cancer Res 1994, 54:5911-5916.
35. McGurk CJ, Cummings M, Koberle B, Hartley JA, Oliver RT, Masters JR. Regulation of DNA repair gene expression in human cancer cell lines. J Cell Biochem 2006, 97:1121-1136. 10.1002/jcb.20711, 16315315.
36. Muotri AR, Marchetto MC, Suzuki MF, Okazaki K, Lotfi CF, Brumatti G, Amarante-Mendes GP, Menck C. Low amounts of the DNA repair XPA protein are sufficient to recover UV-resistance. Carcinogenesis 2002, 23:1039-1046. 10.1093/carcin/23.6.1039, 12082027.
37. Koberle B, Roginskaya V, Wood RD. XPA protein as a limiting factor for nucleotide excision repair and UV sensitivity in human cells. DNA Repair (Amst) 2006, 5:641-648. 10.1016/j.dnarep.2005.12.001, 16413230.
38. Altaha R, Liang X, Yu JJ, Reed E. Excision repair cross complementing-group 1: gene expression and platinum resistance. Int J Mol Med 2004, 14:959-970.
39. Olaussen KA, Dunant A, Fouret P, Brambilla E, Andre F, Haddad V, Taranchon E, Filipits M, Pirker R, Popper HH, Stahel R, Sabatier L, Pignon JP, Tursz T, Le Chevalier T, Soria JC. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy. N Engl J Med 2006, 355:983-991. 10.1056/NEJMoa060570, 16957145.
40. Ahmad A, Robinson AR, Duensing A, van Drunen E, Beverloo HB, Weisberg DB, Hasty P, Hoeijmkers JH, Niedernhofer LJ. ERCC1-XPF endonuclease facilitates DNA double-strand break repair. Mol Cell Biol 2008, 28:5082-5092. 10.1128/MCB.00293-08, 2519706, 18541667.
41. Niedernhofer LJ, Odijk H, Budzowska M, van Drunen E, Maas A, Theil AF, de Wit J, Jaspers NG, Beverloo HB, Hoeijmakers JH, Kanaar R. 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. 10.1128/MCB.24.13.5776-5787.2004, 480908, 15199134.
42. Cummings M, Higginbottom K, McGurk CJ, Wong OG, Koberle B, Oliver RT, Masters JR. XPA versus ERCC1 as chemosensitising agents to cisplatin and mitomycin C in prostate cancer cells: role of ERCC1 in homologous recombination repair. Biochem Pharmacol 2006, 72:166-175. 10.1016/j.bcp.2006.04.025, 16756962.
43. Koberle B, Roginskaya V, Zima KS, Masters JR, Wood RD. Elevation of XPA protein level in testis tumor cells without increasing resistance to cisplatin or UV radiation. Mol Carcinog 2008, 47:580-586. 10.1002/mc.20418, 18240296.