Influence of MLH1 on colon cancer sensitivity to poly(ADP-ribose) polymerase inhibitor combined with irinotecan

International Journal of Oncology

Volumn 43, Issue 1, 2013, Pages 210-218

  Tentori, Lucio ^a   Leonetti, Carlo ^b   Muzi, Alessia ^a   Dorio, Annalisa Susanna ^a   Porru, Manuela ^b   Dolci, Susanna ^a   Campolo, Federica ^a   Vernole, Patrizia ^a   Lacal, Pedro Miguel ^c   Praz, Françoise ^d,e   Graziani, Grazia ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^d CENTRE DE RECHERCHE SAINT ANTOINE   (France)

^e SORBONNE UNIVERSITÉ   (France)

Author keywords

Chemotherapy; Colon cancer; DNA repair; Drug resistance; Mismatch repair; Poly(ADP ribose) polymerase

Indexed keywords

ANTINEOPLASTIC AGENT; BREAST CANCER RESISTANCE PROTEIN; CHECKPOINT KINASE 1; COMPLEMENTARY DNA; GPI 15427; HISTONE H2AX; IRINOTECAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PROTEIN MLH1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL STRAIN HCT116; CHEMOSENSITIVITY; CHROMOSOME 3; CHROMOSOME ANALYSIS; COLON CANCER; COMPETITIVE INHIBITION; CONTROLLED STUDY; DNA DAMAGE; FLOW CYTOMETRY; G2 PHASE CELL CYCLE CHECKPOINT; GENE SILENCING; HISTONE PHOSPHORYLATION; M PHASE CELL CYCLE CHECKPOINT; MALE; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NONSENSE MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WILD TYPE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS; CAMPTOTHECIN; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN KINASES; TOPOISOMERASE I INHIBITORS;

EID: 84879619017     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2013.1932     Document Type: Article

References (36)

1. Davies JM and Goldberg RM: Treatment of metastatic colorectal cancer. Semin Oncol 38: 552-560, 2011.
2. Alagoz M, Gilbert DC, El-Khamisy S and Chalmers AJ: DNA repair and resistance to topoisomerase I inhibitors: mechanisms, biomarkers and therapeutic targets. Curr Med Chem 19: 3874-3885, 2012.
3. Miknyoczki SJ, Jones-Bolin S, Pritchard S, Hunter K, Zhao H, Wan W, Ator M, et al: Chemopotentiation of temozolomide, irinotecan and cisplatin activity by CEP-6800, a poly(ADP-ribose) polymerase inhibitor. Mol Cancer Ther 2: 371-382, 2003.
4. Calabrese CR, Almassy R, Barton S, Batey MA, Calvert AH, Canan-Koch S, Durkacz BW, et al: Anticancer chemosensitization and radiosensitization by the novel poly(ADP-ribose) polymerase-1 inhibitor AG14361. J Natl Cancer Inst 96: 56-67, 2004. (Pubitemid 38180960)
5. Smith LM, Willmore E, Austin CA and Curtin NJ: The novel poly(ADP-Ribose) polymerase inhibitor, AG14361, sensitizes cells to topoisomerase I poisons by increasing the persistence of DNA strand breaks. Clin Cancer Res 11: 8449-8457, 2005. (Pubitemid 41746960)
6. Tentori L, Leonetti C, Scarsella M, Muzi A, Mazzon E, Vergati M, Forini O, et al: Inhibition of poly(ADP-ribose) polymerase prevents irinotecan-induced intestinal damage and enhances irinotecan/temozolomide efficacy against colon carcinoma. FASEB J 20: 1709-1711, 2006.
7. Daniel RA, Rozanska AL, Thomas HD, Mulligan EA, Drew Y, Castelbuono DJ, Hostomsky Z, et al: Inhibition of poly(ADP-ribose) polymerase-1 enhances temozolomide and topotecan activity against childhood neuroblastoma. Clin Cancer Res 15: 1241-1249, 2009.
8. Schreiber V, Dantzer F, Ame JC and de Murcia G: Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7: 517-528, 2006. (Pubitemid 44036457)
9. Malanga M and Althaus FR: Poly(ADP-ribose) reactivates stalled DNA topoisomerase I, induces DNA strand break resealing. J Biol Chem 279: 5244-5248, 2004. (Pubitemid 38220543)
10. Leonetti C, Biroccio A, Graziani G and Tentori L: Targeted therapy for brain tumours: role of PARP inhibitors. Curr Cancer Drug Targets 12: 218-236, 2012.
11. Martin SA, Lord CJ and Ashworth A: Therapeutic targeting of the DNA mismatch repair pathway. Clin Cancer Res 16: 5107-5113, 2010.
12. D'Atri S, Tentori L, Lacal PM, Graziani G, Pagani E, Benincasa E, Zambruno G, et al: Involvement of the mismatch repair system in temozolomide-induced apoptosis. Mol Pharmacol 54: 334-341, 1998. (Pubitemid 28368823)
13. Tentori L and Graziani G: Recent approaches to improve the antitumor efficacy of temozolomide. Curr Med Chem 16: 245-257, 2009.
14. Fedier A, Schwarz VA, Walt H, Carpini RD, Haller U and Fink D: Resistance to topoisomerase poisons due to loss of DNA mismatch repair. Int J Cancer 93: 571-576, 2001. (Pubitemid 32701417)
15. Jacob S, Aguado M, Fallik D and Praz F: The role of the DNA mismatch repair system in the cytotoxicity of the topoisomerase inhibitors camptothecin and etoposide to human colorectal cancer cells. Cancer Res 61: 6555-6562, 2001. (Pubitemid 32783264)
16. Magrini R, Bhonde MR, Hanski ML, Notter M, Scherübl H, Boland CR, Zeitz M and Hanski C: Cellular effects of CPT-11 on colon carcinoma cells: dependence on p53 and hMLH1 status. Int J Cancer 101: 23-31, 2002. (Pubitemid 34832993)
17. Fallik D, Borrini F, Boige V, Viguier J, Jacob S, Miquel C, Sabourin JC, et al: Microsatellite instability is a predictive factor of the tumor response to irinotecan in patients with advanced colorectal cancer. Cancer Res 63: 5738-5744, 2003. (Pubitemid 37187470)
18. Papouli E, Cejka P and Jiricny J: Dependence of the cytotoxicity of DNA-damaging agents on the mismatch repair status of human cells. Cancer Res 64: 3391-3394, 2004. (Pubitemid 38657910)
19. Bhonde MR, Hanski ML, Stehr J, Jebautzke B, Peiró-Jordán R, Fechner H, Yokoyama KK, et al: Mismatch repair system decreases cell survival by stabilizing the tetraploid G1 arrest in response to SN-38. Int J Cancer 126: 2813-2825, 2010.
20. Martin LP, Hamilton TC and Schilder RJ: Platinum resistance: the role of DNA repair pathways. Clin Cancer Res 14: 1291-1295, 2008. (Pubitemid 351413906)
21. Papadopoulos N, Nicolaides NC, Wei YF, Ruben SM, Carter KC, Rosen CA, Haseltine WA, et al: Mutation of a mutL homolog in hereditary colon cancer. Science 263: 1625-1629, 1994. (Pubitemid 24128369)
22. Koi M, Umar A, Chauhan DP, Cherian SP, Carethers JM, Kunkel TA and Boland CR: Human chromosome 3 corrects mismatch repair deficiency and microsatellite instability and reduces N-methyl-N′-nitro-N-nitrosoguanidine tolerance in colon tumor cells with homozygous hMLH1 mutation. Cancer Res 54: 4308-4312, 1994.
23. Vernole P, Muzi A, Volpi A, Terrinoni A, Dorio AS, Tentori L, Shah GM and Graziani G: Common fragile sites in colon cancer cell lines: role of mismatch repair, RAD51 and poly(ADP-ribose) polymerase-1. Mutat Res 712: 40-48, 2011.
24. Tentori L, Leonetti C, Scarsella M, D'Amati G, Vergati M, Portarena I, Xu W, et al: Systemic administration of GPI 15427, a novel poly(ADP-ribose) polymerase-1 inhibitor, increases the antitumor activity of temozolomide against intracranial melanoma, glioma, lymphoma. Clin Cancer Res 9: 5370-5379, 2003. (Pubitemid 37413592)
25. Yamane K, Taylor K and Kinsella TJ: Mismatch repair-mediated G2/M arrest by 6-thioguanine involves the ATR-Chk1 pathway. Biochem Biophys Res Commun 318: 297-302, 2004. (Pubitemid 38526279)
26. Yoshioka K, Yoshioka Y and Hsieh P: ATR kinase activation mediated by MutSalpha and MutLalpha in response to cytotoxic O6-methylguanine adducts. Mol Cell 22: 501-510, 2006.
27. Adamson AW, Beardsley DI, Kim WJ, Gao Y, Baskaran R and Brown KD: Methylator-induced, mismatch repair-dependent G2 arrest is activated through Chk1 and Chk2. Mol Biol Cell 16: 1513-1526, 2005. (Pubitemid 40349584)
28. Marra G and Jiricny J: DNA mismatch repair and colon cancer. Adv Exp Med Biol 570: 85-123, 2005. (Pubitemid 47413187)
29. Damia G and D'Incalci M: Genetic instability influences drug response in cancer cells. Curr Drug Targets 11: 1317-1324, 2010.
30. Sinicrope FA, Foster NR, Thibodeau SN, Marsoni S, Monges G, Labianca R, Kim GP, et al: DNA mismatch repair status and colon cancer recurrence and survival in clinical trials of 5-fluorouracilbased adjuvant therapy. J Natl Cancer Inst 103: 863-875, 2011.
31. Garner KM and Eastman A: Variations in Mre11/Rad50/Nbs1 status and DNA damage-induced S-phase arrest in the cell lines of the NCI60 panel. BMC Cancer 206: 1-13, 2011.
32. Takemura H, Rao VA, Sordet O, Furuta T, Miao ZH, Meng L, Zhang H and Pommier Y: Defective Mre11-dependent activation of Chk2 by ataxia telangiectasia mutated in colorectal carcinoma cells in response to replication-dependent DNA double strand breaks. J Biol Chem 281: 30814-30823, 2006. (Pubitemid 44582136)
33. Tentori L, Muzi A, Dorio AS, Scarsella M, Leonetti C, Shah GM, Xu W, et al: Pharmacological inhibition of poly(ADP-ribose) polymerase (PARP) activity in PARP-1 silenced tumour cells increases chemosensitivity to temozolomide and to a N3-adenine selective methylating agent. Curr Cancer Drug Targets 10: 368-383, 2010.
34. D'Onofrio G, Tramontano F, Dorio AS, Muzi A, Maselli V, Fulgione D, Graziani G, et al: Poly(ADP-ribose) polymerase signaling of topoisomerase 1-dependent DNA damage in carcinoma cells. Biochem Pharmacol 81: 194-202, 2011.
35. Patel AG, Flatten KS, Schneider PA, Dai NT, McDonald JS, Poirier GG and Kaufmann SH: Enhanced killing of cancer cells by poly(ADP-ribose) polymerase inhibitors and topoisomerase I inhibitors reflects poisoning of both enzymes. J Biol Chem 287: 4198-4210, 2012.
36. Davidson D, Wang Y, Aloyz R and Panasci L: The PARP inhibitor ABT-888 synergizes irinotecan treatment of colon cancer cell lines. Invest New Drugs 31: 461-468, 2013.