Base excision repair-mediated resistance to cisplatin in KRAS(G12C) mutant NSCLC cells

Oncotarget

Volumn 6, Issue 30, 2015, Pages 30072-30087

  Caiola, Elisa ^a   Salles, Daniela ^b   Frapolli, Roberta ^a   Lupi, Monica ^a   Rotella, Giuseppe ^a   Ronchi, Anna ^c   Garassino, Marina Chiara ^d   Mattschas, Nikola ^b   Colavecchio, Stefano ^a   Broggini, Massimo ^a   Wiesmüller, Lisa ^b   Marabese, Mirko ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b UNIVERSITY OF ULM   (Germany)

^c IRCCS   (Italy)

^d NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Base excision repair; Cisplatin; KRAS; NSCLC; Resistance

Indexed keywords

CASPASE 3; CASPASE 7; CISPLATIN; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; ANTINEOPLASTIC AGENT; CATION TRANSPORT PROTEIN; KRAS PROTEIN, HUMAN; PROTEIN P21; SLC31A1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER RESISTANCE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DNA ADDUCT; DNA CROSS LINKING; DNA DAMAGE; DRUG CYTOTOXICITY; DRUG RESPONSE; DRUG UPTAKE; EXCISION REPAIR; FEMALE; GENE EXPRESSION; GENETIC VARIABILITY; GROWTH RATE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; ONCOGENE K RAS; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR VOLUME; 3T3 CELL LINE; ANIMAL; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE; CELL SURVIVAL; DNA REPAIR; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; FLUORESCENCE MICROSCOPY; GENETICS; HUMAN; LUNG NEOPLASMS; METABOLISM; MUTATION; NUDE MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CATION TRANSPORT PROTEINS; CELL CYCLE; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; DNA REPAIR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; HUMANS; LUNG NEOPLASMS; MICE; MICE, NUDE; MICROSCOPY, FLUORESCENCE; MUTATION; NIH 3T3 CELLS; PROTO-ONCOGENE PROTEINS P21(RAS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84945116838     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5019     Document Type: Article

References (58)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61:69-90.
2. Sato M, Shames DS, Gazdar AF, Minna JD. A translational view of the molecular pathogenesis of lung cancer. J Thorac Oncol. 2007; 2:327-343.
3. Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med. 2008; 359:1367-1380.
4. Pao W, Miller V, Zakowski M, Doherty J, Politi K, Sarkaria I, Singh B, Heelan R, Rusch V, Fulton L, Mardis E, Kupfer D, Wilson R, Kris M, Varmus H. EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci U S A. 2004; 101:13306-13311.
5. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, Fujiwara S, Watanabe H, Kurashina K, Hatanaka H, Bando M, Ohno S, Ishikawa Y, Aburatani H, Niki T, Sohara Y, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature. 2007; 448:561-566.
6. Gerber DE, Minna JD. ALK inhibition for non-small cell lung cancer: from discovery to therapy in record time. Cancer Cell. 2010; 18:548-551.
7. Gridelli C, Ardizzoni A, Douillard JY, Hanna N, Manegold C, Perrone F, Pirker R, Rosell R, Shepherd FA, De Petris L, Di Maio M, de Marinis F. Recent issues in first-line treatment of advanced non-small-cell lung cancer: Results of an International Expert Panel Meeting of the Italian Association of Thoracic Oncology. Lung Cancer. 2010; 68:319-331.
8. Kadota K, Yeh YC, D'Angelo SP, Moreira AL, Kuk D, Sima CS, Riely GJ, Arcila ME, Kris MG, Rusch VW, Adusumilli PS, Travis WD. Associations Between Mutations and Histologic Patterns of Mucin in Lung Adenocarcinoma: Invasive Mucinous Pattern and Extracellular Mucin Are Associated With KRAS Mutation. Am J Surg Pathol. 2014; 38:1118-1127.
9. Riely GJ, Marks J, Pao W. KRAS mutations in non-small cell lung cancer. Proc Am Thorac Soc. 2009; 6:201-205.
10. Schubbert S, Shannon K, Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer. 2007; 7:295-308.
11. Rodenhuis S, Boerrigter L, Top B, Slebos RJ, Mooi WJ, van't Veer L, van Zandwijk N. Mutational activation of the K-ras oncogene and the effect of chemotherapy in advanced adenocarcinoma of the lung: a prospective study. J Clin Oncol. 1997; 15:285-291.
12. Garassino MC, Marabese M, Rusconi P, Rulli E, Martelli O, Farina G, Scanni A, Broggini M. Different types of K-Ras mutations could affect drug sensitivity and tumour behaviour in non-small-cell lung cancer. Ann Oncol. 2011; 22:235-237.
13. Marabese M, Rulli E, Bettini A, Garassino M, Longo F, Moscetti L, Pavese I, Lauricella C, Broggini M, Farina G. KRAS mutational status impact progression free survival of patients treated with platinum based chemotherapy in NSCLC. AACR-NCI-EORTC International Conference: Molecular Targets and Cancer Therapeutics; San Francisco, CA: 2011.
14. Howell SB, Safaei R, Larson CA, Sailor MJ. Copper transporters and the cellular pharmacology of the platinum-containing cancer drugs. Mol Pharmacol. 2010; 77:887-894.
15. Ban N, Takahashi Y, Takayama T, Kura T, Katahira T, Sakamaki S, Niitsu Y. Transfection of glutathione S-transferase (GST)-pi antisense complementary DNA increases the sensitivity of a colon cancer cell line to adriamycin, cisplatin, melphalan, and etoposide. Cancer Res. 1996; 56:3577-3582.
16. Shiloh Y, Ziv Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat Rev Mol Cell Biol. 2013; 14:197-210.
17. Raschle M, Knipscheer P, Enoiu M, Angelov T, Sun J, Griffith JD, Ellenberger TE, Scharer OD, Walter JC. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell. 2008; 134:969-980.
18. Panier S, Boulton SJ. Double-strand break repair: 53BP1 comes into focus. Nat Rev Mol Cell Biol. 2014; 15:7-18.
19. Scharer OD. Nucleotide excision repair in eukaryotes. Cold Spring Harb Perspect Biol. 2013; 5:a012609.
20. Thompson LH, Hinz JM. Cellular and molecular consequences of defective Fanconi anemia proteins in replication-coupled DNA repair: mechanistic insights. Mutat Res. 2009; 668:54-72.
21. Bergink S, Jentsch S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature. 2009; 458:461-467.
22. Sobol RW, Horton JK, Kuhn R, Gu H, Singhal RK, Prasad R, Rajewsky K, Wilson SH. Requirement of mammalian DNA polymerase-beta in base-excision repair. Nature. 1996; 379:183-186.
23. Rosa S, Fortini P, Karran P, Bignami M, Dogliotti E. Processing in vitro of an abasic site reacted with methoxyamine: a new assay for the detection of abasic sites formed in vivo. Nucleic Acids Res. 1991; 19:5569-5574.
24. Masaoka A, Gassman NR, Horton JK, Kedar PS, Witt KL, Hobbs CA, Kissling GE, Tano K, Asagoshi K, Wilson SH. Interaction between DNA Polymerase beta and BRCA1. PLoS One. 2013; 8:e66801.
25. Pirker R, Minar W. Chemotherapy of advanced nonsmall cell lung cancer. Front Radiat Ther Oncol. 2010; 42:157-163.
26. Kallianos A, Rapti A, Zarogoulidis P, Tsakiridis K, Mpakas A, Katsikogiannis N, Kougioumtzi I, Li Q, Huang H, Zaric B, Perin B, Courcoutsakis N, Zarogoulidis K. Therapeutic procedure in small cell lung cancer. J Thorac Dis. 2013; 5:S420-424.
27. Petrosyan F, Daw H, Haddad A, Spiro T. Targeted therapy for lung cancer. Anticancer Drugs. 2012; 23:1016-1021.
28. Suda K, Tomizawa K, Mitsudomi T. Biological and clinical significance of KRAS mutations in lung cancer: an oncogenic driver that contrasts with EGFR mutation. Cancer Metastasis Rev. 2010; 29:49-60.
29. Piva S, Ganzinelli M, Garassino MC, Caiola E, Farina G, Broggini M, Marabese M. Across the universe of K-RAS mutations in non-small-cell-lung cancer. Curr Pharm Des. 2014; 20:3933-3943.
30. Loriot Y, Mordant P, Deutsch E, Olaussen KA, Soria JC. Are RAS mutations predictive markers of resistance to standard chemotherapy? Nat Rev Clin Oncol. 2009; 6:528-534.
31. Karachaliou N, Mayo C, Costa C, Magri I, GimenezCapitan A, Molina-Vila MA, Rosell R. KRAS mutations in lung cancer. Clin Lung Cancer. 2013; 14:205-214.
32. Roberts PJ, Stinchcombe TE. KRAS mutation: should we test for it, and does it matter? J Clin Oncol. 2013; 31:1112-1121.
33. To MD, Rosario RD, Westcott PM, Banta KL, Balmain A. Interactions between wild-type and mutant Ras genes in lung and skin carcinogenesis. Oncogene. 2013; 32:4028-4033.
34. Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M, Kroemer G. Molecular mechanisms of cisplatin resistance. Oncogene. 2012; 31:1869-1883.
35. Koberle B, Tomicic MT, Usanova S, Kaina B. Cisplatin resistance: preclinical findings and clinical implications. Biochim Biophys Acta. 2010; 1806:172-182.
36. Stewart DJ. Mechanisms of resistance to cisplatin and carboplatin. Crit Rev Oncol Hematol. 2007; 63:12-31.
37. Bao Y. Chromatin response to DNA double-strand break damage. Epigenomics. 2011; 3:307-321.
38. Martin LP, Hamilton TC, Schilder RJ. Platinum resistance: the role of DNA repair pathways. Clin Cancer Res. 2008; 14:1291-1295.
39. Kothandapani A, Sawant A, Dangeti VS, Sobol RW, Patrick SM. Epistatic role of base excision repair and mismatch repair pathways in mediating cisplatin cytotoxicity. Nucleic Acids Res. 2013; 41:7332-7343.
40. Wang YC, Lu YP, Tseng RC, Lin RK, Chang JW, Chen JT, Shih CM, Chen CY. Inactivation of hMLH1 and hMSH2 by promoter methylation in primary non-small cell lung tumors and matched sputum samples. J Clin Invest. 2003; 111:887-895.
41. Iwatsuki M, Mimori K, Yokobori T, Tanaka F, Tahara K, Inoue H, Baba H, Mori M. A platinum agent resistance gene, POLB, is a prognostic indicator in colorectal cancer. J Surg Oncol. 2009; 100:261-266.
42. Srivastava DK, Husain I, Arteaga CL, Wilson SH. DNA polymerase beta expression differences in selected human tumors and cell lines. Carcinogenesis. 1999; 20:1049-1054.
43. Albertella MR, Lau A, O'Connor MJ. The overexpression of specialized DNA polymerases in cancer. DNA Repair (Amst). 2005; 4:583-593.
44. Canitrot Y, Laurent G, Astarie-Dequeker C, Bordier C, Cazaux C, Hoffmann JS. Enhanced expression and activity of DNA polymerase beta in chronic myelogenous leukemia. Anticancer Res. 2006; 26:523-525.
45. Bergoglio V, Canitrot Y, Hogarth L, Minto L, Howell SB, Cazaux C, Hoffmann JS. Enhanced expression and activity of DNA polymerase beta in human ovarian tumor cells: impact on sensitivity towards antitumor agents. Oncogene. 2001; 20:6181-6187.
46. Michels J, Obrist F, Castedo M, Vitale I, Kroemer G. PARP and other prospective targets for poisoning cancer cell metabolism. Biochem Pharmacol. 2014.
47. Wang T, Zang W, Ma Y, Li M, Xuan X, Wang N, Wu R, Li Y, Dong Z, Zhao G. DNA polymerase beta promoter mutations affect gene transcription, translation and the sensitivity of esophageal cancer cells to cisplatin treatment. Mol Biol Rep. 2013; 40:1333-1339.
48. Chyan YJ, Rawson TY, Wilson SH. Cloning and characterization of a novel member of the human ATF/CREB family: ATF2 deletion, a potential regulator of the human DNA polymerase beta promoter. Gene. 2003; 312:117-124.
49. Steven A, Heiduk M, Recktenwald CV, Hiebl B, Wickenhauser C, Massa C, Seliger B. Colorectal Carcinogenesis: Connecting K-RAS-induced Transformation and CREB Activity in vitro and in vivo. Mol Cancer Res. 2015;.
50. De Vos M, Schreiber V, Dantzer F. The diverse roles and clinical relevance of PARPs in DNA damage repair: current state of the art. Biochem Pharmacol. 2012; 84:137-146.
51. Michels J, Vitale I, Galluzzi L, Adam J, Olaussen KA, Kepp O, Senovilla L, Talhaoui I, Guegan J, Enot DP, Talbot M, Robin A, Girard P, Orear C, Lissa D, Sukkurwala AQ, et al. Cisplatin resistance associated with PARP hyperactivation. Cancer Res. 2013; 73:2271-2280.
52. Marabese M, Marchini S, Sabatino MA, Polato F, Vikhanskaya F, Marrazzo E, Riccardi E, Scanziani E, Broggini M. Effects of inducible overexpression of DNp73alpha on cancer cell growth and response to treatment in vitro and in vivo. Cell Death Differ. 2005; 12:805-814.
53. Bohringer M, Obermeier K, Griner N, Waldraff D, Dickinson E, Eirich K, Schindler D, Hagen M, Jerry DJ, Wiesmuller L. siRNA screening identifies differences in the Fanconi anemia pathway in BALB/c-Trp53+/-with susceptibility versus C57BL/6-Trp53+/-mice with resistance to mammary tumors. Oncogene. 2013; 32:5458-5470.
54. Marabese M, Mazzoletti M, Vikhanskaya F, Broggini M. HtrA2 enhances the apoptotic functions of p73 on bax. Cell Death Differ. 2008; 15:849-858.
55. Zamai M, VandeVen M, Farao M, Gratton E, Ghiglieri A, Castelli MG, Fontana E, D'Argy R, Fiorino A, Pesenti E, Suarato A, Caiolfa VR. Camptothecin poly [n-(2-hydroxypropyl) methacrylamide] copolymers in antitopoisomerase-I tumor therapy: intratumor release and antitumor efficacy. Mol Cancer Ther. 2003; 2:29-40.
56. Ubezio P. Microcomputer experience in analysis of flow cytometric DNA distributions. Comput Programs Biomed. 1985; 19:159-166.
57. Akyuz N, Boehden GS, Susse S, Rimek A, Preuss U, Scheidtmann KH, Wiesmuller L. DNA substrate dependence of p53-mediated regulation of double-strand break repair. Mol Cell Biol. 2002; 22:6306-6317.
58. Bennardo N, Cheng A, Huang N, Stark JM. AlternativeNHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 2008; 4:e1000110.