Downregulation of XPF-ERCC1 enhances cisplatin efficacy in cancer cells

DNA Repair

Volumn 9, Issue 7, 2010, Pages 745-753

  Arora, Sanjeevani ^a   Kothandapani, Anbarasi ^a   Tillison, Kristin ^a   Kalman Maltese, Vivian ^a   Patrick, Steve M ^a  

^a Department of Biochemistry and Cancer Biology ^*  (United States)

Author keywords

Cisplatin; DNA repair and cancer; XPF ERCC1

Indexed keywords

CISPLATIN; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; HISTONE H2AX; NUCLEIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP F PROTEIN;

ARTICLE; CANCER CELL; CELL VIABILITY; CONTROLLED STUDY; CROSS LINKING; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG EFFICACY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN STABILITY; RNA INTERFERENCE;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CISPLATIN; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; ENDONUCLEASES; GENE KNOCKDOWN TECHNIQUES; HISTONES; HUMANS; NEOPLASMS; RNA, SMALL INTERFERING;

EID: 77953321799     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2010.03.010     Document Type: Article

References (55)

1. Reed E. Platinum-DNA adduct, nucleotide excision repair and platinum based anti-cancer chemotherapy. Cancer Treat. Rev. 24 (1998) 331-344
2. Zamble D.B., and Lippard S.J. Cisplatin and DNA-repair in cancer-chemotherapy. Trends Biochem. Sci. 20 (1995) 435-439
3. Le Chevalier T., Arriagada R., Le Pechoux C., Grunenwald D., Dunant A., Pignon J.P., Tarayre M., Abratt R., Arriagada R., Bergman B., Gralla R., Grunenwald D., Le Chevalier T., Orlowski T., Papadakis E., Pinel M.I.S., Araujo C., la Torre H., de Solchaga M.M., Abdi E., Blum R., Ball D., Basser R., De Boer R., Bishop J., Brigham B., Davis S., Fox D., Richardson G., Wyld D., Pirker R., Humblet Y., Delaunois L., Van Meerbeeck J.P., Germonpre P., Vansteenkiste J., Nackaerts K., Pinel M.I.S., Vauthier G., Younes R.N., Arriagada R., Baeza R., Carvajal P., Kleinman S., Orlandi L., Castro C., Godoy J., Kosatova K., Gaafar R., Azarian R., Benichou M., Boudoux L., Boyer G., Chirat E., Chomy F., Coetmeur D., Couderc L.J., Coudert B., Crequit J., David P., Delaval P., Dohollou N., Foucher P., Gonzalez G., Jeanfaivre T., Joveniaux A., Kanoui A.A., Le Chevalier T., Le Pechoux C., Baldeyrou P., Debrosse D., Girard P., Grunenwald D., Ruffie P., Leclerc P., Milleron B., Monnet I., Monnot H., Morere J.F., Naman H., Dides S., Noel J.P., Otto J., Ozanne F., Ozenne G., Parent F., Peureux M., Picon B., Pujol J.L., Quoix E., Rabut H., Riviere A., Gervais R., Icard P., Rixe O., Deplanque G., Sevin D., Spaeth D., Tourani J.M., Toussaint C., Tuchais C., Vannetzel J.M., VArflet F., Virally J., Zaegel M., Zalcman G., Livatorwski A., Eberhardt W., Alexopoulos C., Apostolopoulou F., Bachlitzanakis N., Bellenis I., Christaki P., Dosios T., Georgoulias V., Iliadis K., Kardamakis D., Konstantinou M., Kotsovoulou V., Pouliou M., Michalopoulou P., Papadakis E., Agelidou A., Zarogoulidis K., Gottfried M., Kovner F., Agostara B., Ascoli M., Brigandi A., Cigolari S., Colucci G., De Braud F., Dirosa T., Giglio A., Maiorino A., Masotti A., Rusca M., Ogawara M., Osada H., Park K., Jackevicius A., Smickoska S., El Gueddari B.E., Aaesebo U., Desales R., Furman M., Kozlowski M., Laudansk J., Grodzki T., Orlowski T., Chabowski M., Pluzanska A., Gaspar L., Ciuleanu T., Baumohl J., Cerna M., Bitenc M., Abratt R., Chasen M., Alberola V., Azagra P., Garcia P.B., Cardenal F., Curto C.P., Salinas J., Serrate R.S., Bergman B., Andersson L., Hero U., Mansson T., Martinsson J.E., Hillerdal G., Agrenius V., Sederholm C., Arvidsson I., Ydreborg S.O., Thaning L., Sjogren A., Jonsson P., Grip H., Singer J., Lundgren R., Brodin O., Andejani D., Branden E., Lamberg K., Riska H., Egli E., Joss R., Martinelli G., Roth A., Stahel R., Stupp R., El Kamel A., Gralla R., Cole J.T., Jahanzeb M., Wiznitzer I., Masters G.A., Radosavljevic G., Babiker A., Green M., Osterlind K., Taube A., and Wedel H. Cisplatin-based adjuvant chemotherapy in patients with completely resected non-small-cell lung cancer. N. Engl. J. Med. 350 (2004) 351-360
4. McGurk C.J., Cummings M., Koberle B., Hartley J.A., Oliver R.T., and Masters J.R. Regulation of DNA repair gene expression in human cancer cell lines. J. Cell. Biochem. 97 (2006) 1121-1136
5. Selvakumaran M., Pisarcik D.A., Bao R., Yeung A.T., and Hamilton T.C. Enhanced cisplatin cytotoxicity by disturbing the nucleotide excision repair pathway in ovarian cancer cell lines. Cancer Res. 63 (2003) 1311-1316
6. Chu G. Cellular responses to cisplatin. The roles of DNA-binding proteins and DNA Repair [Review] [74 Refs.]. J. Biol. Chem. 269 (1994) 787-790
7. Gillet L.C.J., and Scharer O.D. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem. Rev. 106 (2006) 253-276
8. Bessho T., Sancar A., Thompson L.H., and Thelen M.P. Reconstitution of human excision nuclease with recombinant XPF-ERCC1 complex. J. Biol. Chem. 272 (1997) 3833-3837
9. Rosell R., Lord R.V.N., Taron M., and Reguart N. DNA repair and cisplatin resistance in non-small-cell lung cancer. Lung Cancer 38 (2002) 217-227
10. Li Q.D., Yu J.J., Mu C.J., Yunmbam M.K., Slavsky D., Cross C.L., Bostickbruton F., and Reed E. Association between the level of ERCC-1 expression and the repair of cisplatin-induced DNA damage in human ovarian cancer cells. Anticancer Res. (2000) 645-652
11. Park S.Y., Hong Y.C., Kim J.H., Kwak S.M., Cho J.H., Lee H.L., and Ryu J.S. Effect of ERCC1 polymorphisms and the modification by smoking on the survival of non-small cell lung cancer patients. Med. Oncol. 23 (2006) 489-498
12. Olaussen K.A., Dunant A., Fouret P., Brambilla E., Andre F., Haddad V., Taranchon E., Filipits M., Pirker R., Popper H.H., Stahel R., Sabatier L., Pignon J., Tursz T., Le Chevalier T., and Soria J. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy. N. Engl. J. Med. 355 (2006) 983-991
13. Welsh C., Day R., McGurk C., Masters J.R.W., Wood R.D., and Koberle B. Reduced levels of XPA, ERCC1 and XPF DNA repair proteins in testis tumor cell lines. Int. J. Cancer 110 (2004) 352-361
14. Niedernhofer L.J., Odijk H., Budzowska M., van Drunen E., Maas A., Theil A.F., de Wit J., Jaspers N.G.J., Beverloo H.B., Hoeijmakers J.H.J., and Kanaar R. The structure-specific endonuclease ERCC1-XPF is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol. Cell. Biol. 24 (2004) 5776-5787
15. Kuraoka I., Kobertz W.R., Ariza R.R., Biggerstaff M., Essigmann J.M., and Wood R.D. Repair of an interstrand DNA cross-link initiated by ERCC1-XPF repair/recombination nuclease. J. Biol. Chem. 275 (2000) 26632-26636
16. Schiestl R.H., and Prakash S. RAD10, an excision repair gene of Saccharomyces cerevisiae, is involved in the RAD1 pathway of mitotic recombination. Mol. Cell. Biol. 10 (1990) 2485-2491
17. Niedernhofer L.J., Essers J., Weeda G., Beverloo B., de Wit J., Muijtjens M., Odijk H., Hoeijmakers J.H.J., and Kanaar R. The structure-specific endonuclease ERCC1-XPF is required for targeted gene replacement in embryonic stem cells. EMBO J. 20 (2001) 6540-6549
18. Zhu X.D., Niedernhofer L., Kuster B., Mann M., Hoeijmakers J.H.J., and de Lange T. ERCC1/XPF removes the 3′ overhang from uncapped telomeres and represses formation of telomeric DNA-containing double minute chromosomes. Mol. Cell 12 (2003) 1489-1498
19. Munoz P., Blanco R., Flores J.M., and Blasco M.A. XPF nuclease-dependent telomere loss and increased DNA damage in mice overexpressing TRF2 result in premature aging and cancer. Nat. Genet. 37 (2005) 1063-1071
20. Al-Minawi A.Z., Lee Y.F., Hakansson D., Johansson F., Lundin C., Saleh-Gohari N., Schultz N., Jenssen D., Bryant H.E., Meuth M., Hinz J.M., and Helleday T. The ERCC1/XPF endonuclease is required for completion of homologous recombination at DNA replication forks stalled by inter-strand cross-links. Nucleic Acids Res. 37 (2009) 6400-6413
21. Willey J.C., Crawford E.L., Jackson C.M., Weaver D.A., Hoban J.C., Khuder S.A., and Demuth J.P. Expression measurement of many genes simultaneously by quantitative RT-PCR using standardized mixtures of competitive templates. Am. J. Respir. Cell Mol. Biol. 19 (1998) 6-17
22. Weaver D.A., Crawford E.L., Warner K.A., Elkhairi F., Khuder S.A., and Willey J.C. ABCC5, ERCC2, XPA and XRCC1 transcript abundance levels correlate with cisplatin chemoresistance in non-small cell lung cancer cell lines. Mol. Cancer 4 (2005)
23. Tilby M.J., Johnson C., Knox R.J., Cordell J., Roberts J.J., and Dean C.J. Sensitive detection of DNA modifications induced by cisplatin and carboplatin in vitro and in vivo using a monoclonal-antibody. Cancer Res. 51 (1991) 123-129
24. De Silva I.U., McHugh P.J., Clingen P.H., and Hartley J.A. Defects in interstrand cross-link uncoupling do not account for the extreme sensitivity of ERCC1 and XPF cells to cisplatin. Nucleic Acids Res. 30 (2002) 3848-3856
25. Olive P.L., Banath J.P., and Durand R.E. Heterogeneity in radiation-induced DNA damage and repair in tumor and normal-cells measured using the comet assay. Radiat. Res. 122 (1990) 86-94
26. Singh N.P., Mccoy M.T., Tice R.R., and Schneider E.L. A simple technique for quantitation of low-levels of DNA damage in individual cells. Exp. Cell Res. 175 (1988) 184-191
27. Zamble D.B., Mu D., Reardon J.T., Sancar A., and Lippard S.J. Repair of cisplatin-DNA adducts by the mammalian excision nuclease. Biochemistry 35 (1996) 10004-10013
28. Hartley J.M., Spanswick V.J., Gander M., Giacomini G., Whelan J., Souhami R.L., and Hartley J.A. Measurement of DNA cross-linking in patients on ifosfamide therapy using the single cell gel electrophoresis (comet) assay. Clin. Cancer Res. 5 (1999) 507-512
29. Friedmann B., Caplin M., Hartley J.A., and Hochhauser D. Modulation of DNA repair in vitro after treatment with chemotherapeutic agents by the epidermal growth factor receptor inhibitor gefitinib (ZD1839). Clin. Cancer Res. 10 (2004) 6476-6486
30. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., and Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273 (1998) 5858-5868
31. Olive P.L., and Banath J.P. Kinetics of H2AX Phosphorylation after exposure to cisplatin. Cytometry Part B: Clin. Cytom. 76B (2009) 79-90
32. Paull T.T., Rogakou E.P., Yamazaki V., Kirchgessner C.U., Gellert M., and Bonner W.M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10 (2000) 886-895
33. Yu T., MacPhail S.H., Banath J.P., Klokov D., and Olive P.L. Endogenous expression of phosphorylated histone H2AX in tumors in relation to DNA double-strand breaks and genomic instability. DNA Repair 5 (2006) 935-946
34. Reed E. ERCC1 measurements in clinical oncology. N. Engl. J. Med. 355 (2006) 1054-1055
35. Lord R.V.N., Brabender J., Gandara D., Alberola V., Camps C., Domine M., Cardenal F., Sanchez J.M., Gumerlock P.H., Taron M., Sanchez J.J., Danenberg K.D., Danenberg P.V., and Rosell R. Low ERCC1 expression correlates with prolonged survival after cisplatin plus gemcitabine chemotherapy in non-small cell lung cancer. Clin. Cancer Res. 8 (2002) 2286-2291
36. Azuma K., Komohara Y., Sasada T., Terazaki Y., Ikeda J., Hoshino T., Itoh K., Yamada A., and Aizawa H. Excision repair cross-complementation group 1 predicts progression-free and overall survival in non-small cell lung cancer patients treated with platinum-based chemotherapy. Cancer Sci. 98 (2007) 1336-1343
37. Tripsianes K., Folkers G., Ab E., Das D., Odijk H., Jaspers N.G.J., Hoeijmakers J.H.J., Kaptein R., and Boelens R. The structure of the human ERCC1/XPF interaction domains reveals a complementary role for the two proteins in nucleotide excision repair. Structure 13 (2005) 1849-1858
38. Choi Y.J., Ryu K.S., Ko Y.M., Chae Y.K., Pelton J.G., Wemmer D.E., and Choi B.S. Biophysical characterization of the interaction domains and mapping of the contact residues in the XPF-ERCC1 complex. J. Biol. Chem. 280 (2005) 28644-28652
39. Biggerstaff M., Szymkowski D.E., and Wood R.D. Co-correction of the ERCC1, ERCC4 and Xeroderma-Pigmentosum group-F DNA-repair defects in-vitro. EMBO J. 12 (1993) 3685-3692
40. Niedernhofer L.J., Bhagwat N., and Wood R.D. ERCC1 and non-small-cell lung cancer. N. Engl. J. Med. 356 (2007) 2538-2540
41. Jaspers N.G.J., Raams A., Silengo M.C., Wijgers N., Niedernhofer L.J., Robinson A.R., Giglia-Mari G., Hoogstraten D., Kleijer W.J., Hoeijmakers J.H.J., and Vermeulen W. 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. 80 (2007) 457-466
42. Das D., Tripsianes K., Jaspers N.G.J., Hoeijmakers J.H.J., Kaptein R., Boelens R., and Folkers G.E. The HhH domain of the human DNA repair protein XPF forms stable homodimers. Proteins Struct. Funct. Bioinform. 70 (2008) 1551-1563
43. Vanduin M., Vredeveldt G., Mayne L.V., Odijk H., Vermeulen W., Klein B., Weeda G., Hoeijmakers J.H.J., Bootsma D., and Westerveld A. The cloned human DNA excision repair gene Errc-1 fails to correct Xeroderma Pigmentosum complementation group-A through group-I. Mutat. Res. 217 (1989) 83-92
44. Tian M., Shinkura R., Shinkura N., and Alt F.W. Growth retardation, early death, and DNA repair defects in mice deficient for the nucleotide excision repair enzyme XPF. Mol. Cell. Biol. 24 (2004) 1200-1205
45. Weeda G., Donker I., deWit J., Morreau H., Janssens R., Vissers C.J., Nigg A., vanSteeg H., Bootsma D., and Hoeijmakers J.H.J. Disruption of mouse ERCC1 results in a novel repair syndrome with growth failure, nuclear abnormalities and senescence. Curr. Biol. 7 (1997) 427-439
46. Mcwhir J., Selfridge J., Harrison D.J., Squires S., and Melton D.W. Mice with DNA-repair gene (Ercc-1) deficiency have elevated levels of p53, liver nuclear abnormalities and die before weaning. Nat. Genet. 5 (1993) 217-224
47. Zheng H.Y., Wang X., Warren A.J., Legerski R.J., Nairn R.S., Hamilton J.W., and Li L. Nucleotide excision repair- and polymerase eta-mediated error-prone removal of mitomycin C interstrand cross-links. Mol. Cell. Biol. 23 (2003) 754-761
48. Bergstralh D.T., and Sekelsky J. Interstrand crosslink repair: can XPF-ERCC1 be let off the hook?. Trends Genet. 24 (2008) 70-76
49. Wynne P., Newton C., Ledermann J., Olaitan A., Mould T.A., and Hartley J.A. Enhanced repair of DNA interstrand crosslinking in ovarian cancer cells from patients following treatment with platinum-based chemotherapy. Br. J. Cancer 97 (2007) 927-933
50. McHugh P., Spanswick V., and Hartley J. Repair of DNA Interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol. 2 8 (2001) 483-490
51. Andersson B.S., Sadeghi T., Siciliano M.J., Legerski R., and Murray D. Nucleotide excision repair genes as determinants of cellular sensitivity to cyclophosphamide analogs. Cancer Chemother. Pharmacol. 38 (1996) 406-416
52. Carvalho H., Ortolan T.G., Depaula T., Leite R.A., Weinlich R., Marante-Mendes G.P., and Menck C.F.M. Sustained activation of p53 in confluent nucleotide excision repair-deficient cells resistant to ultraviolet-induced apoptosis. DNA Repair 7 (2008) 922-931
53. Fink D., Zheng H., Nebel S., Norris P.S., Aebi S., Lin T.P., Nehme A., Christen R.D., Haas M., MacLeod C.L., and Howell S.B. In vitro and in vivo resistance to cisplatin in cells that have lost DNA mismatch repair. Cancer Res. 57 (1997) 1841-1845
54. Chang I.Y., Kim M.H., Kim H.B., Lee D.Y., Kim S.H., Kim H.Y., and You H.J. Small interfering RNA-induced suppression of ERCC1 enhances sensitivity of human cancer cells to cisplatin. Biochem. Biophys. Res. Commun. 327 (2005) 225-233
55. Cummings M., Higginbottom K., McGurk C.J., Wong O.G.W., Koberle B., Oliver R.T.D., and Masters J.R. XPA versus ERCC1 as chemosensitising agents to cisplatin and mitomycin C in prostate cancer cells: role of ERCC1 in homologous recombination repair. Biochem. Pharmacol. 72 (2006) 166-175