Synergistic interaction between cisplatin and PARP inhibitors in non-small cell lung cancer

Cell Cycle

Volumn 12, Issue 6, 2013, Pages 877-883

  Michels, Judith ^a,b,c   Vitale, Ilio ^a,b,c   Senovilla, Laura ^a,b,c   Enot, David P ^a,b,c   Garcia, Pauline ^a,b,c   Lissa, Delphine ^a,b,c   Olaussen, Ken A ^a,b,c   Brenner, Catherine ^a,c   Soria, Jean Charles ^a,b,c   Castedo, Maria ^a,b,c   Kroemer, Guido ^a,b,d,e,f  

^a INSERM   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e CENTRE DE RECHERCHE DES CORDELIERS   (France)

^f HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

Author keywords

A549 cells; Apoptosis; CEP 8983; DNA damage response; PJ34 hydrochloride; Small interfering RNAd

Indexed keywords

CASPASE; CEP 8983; CISPLATIN; CYTOCHROME C; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PROTEIN P53; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CELL; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MEMBRANE RUPTURE; MITOCHONDRIAL MEMBRANE; PROTEIN DEPLETION; PROTEIN SECRETION; REVIEW;

EID: 84875132525     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.24034     Document Type: Review

References (46)

1. Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 2007; 8:729-40; PMID:17667954; http://dx.doi.org/10.1038/nrm2233
2. Carrassa L, Broggini M, Erba E, Damia G. Chk1, but not Chk2, is involved in the cellular response to DNA damaging agents: differential activity in cells expressing or not p53. Cell Cycle 2004; 3:1177-81; PMID:15326376; http://dx.doi.org/10.4161/cc.3.9.1080
3. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012; 19:107-20; PMID:21760595; http://dx.doi.org/10.1038/cdd.2011.96
4. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87:99-163; PMID:17237344; http://dx.doi.org/ 10.1152/physrev.00013.2006
5. Nardella C, Clohessy JG, Alimonti A, Pandolfi PP. Pro-senescence therapy for cancer treatment. Nat Rev Cancer 2011; 11:503-11; PMID:21701512; http://dx.doi.org/10.1038/nrc3057
6. Mandic A, Hansson J, Linder S, Shoshan MC. Cisplatin induces endoplasmic reticulum stress and nucleus-independent apoptotic signaling. J Biol Chem 2003; 278:9100-6; PMID:12509415; http://dx.doi.org/10.1074/jbc.M210284200
7. Berndtsson M, Hägg M, Panaretakis T, Havelka AM, Shoshan MC, Linder S. Acute apoptosis by cisplatin requires induction of reactive oxygen species but is not associated with damage to nuclear DNA. Int J Cancer 2007; 120:175-80; PMID:17044026; http://dx.doi.org/10.1002/ijc.22132
8. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 2010; 11:700-14; PMID:20823910; http://dx.doi.org/10.1038/nrm2970
9. Kelland L. The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer 2007; 7:573-84; PMID:17625587; http://dx.doi.org/10.1038/nrc2167
10. Winter C, Albers P. Testicular germ cell tumors: pathogenesis, diagnosis and treatment. Nat Rev Endocrinol 2011; 7:43-53; PMID:21116298; http://dx.doi.org/10.1038/nrendo.2010.196
11. Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, et al. Molecular mechanisms of cisplatin resistance. Oncogene 2012; 31:1869-83; PMID:21892204; http://dx.doi.org/10.1038/onc.2011.384
12. Köberle B, Tomicic MT, Usanova S, Kaina B. Cisplatin resistance: preclinical findings and clinical implications. Biochim Biophys Acta 2010; 1806:172-82; PMID:20647037
13. Siddik ZH. Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene 2003; 22:7265-79; PMID:14576837; http://dx.doi.org/10.1038/ sj.onc.1206933
14. Borst P, Rottenberg S, Jonkers J. How do real tumors become resistant to cisplatin? Cell Cycle 2008; 7:1353-9; PMID:18418074; http://dx.doi.org/10.4161/ cc.7.10.5930
15. Beers MH. Lung carcinoma. In: Porter RS, Jones TV, eds. The Merck manual of diagnosis and therapy. Rahway: Merck & Co., Inc., 2008:2992
16. Jemal A, Thun MJ, Ries LA, Howe HL, Weir HK, Center MM, et al. Annual report to the nation on the status of cancer, 1975-2005, featuring trends in lung cancer, tobacco use, and tobacco control. J Natl Cancer Inst 2008; 100:1672-94; PMID:19033571; http://dx.doi.org/10.1093/jnci/djn389
17. Panaretakis T. Cisplatin-induced apoptosis and development of resistance are transcriptionally distinct processes. Cell Cycle 2012; 11:3723; PMID:22983001; http://dx.doi.org/10.4161/cc.22114
18. Galluzzi L, Vitale I, Senovilla L, Olaussen KA, Pinna G, Eisenberg T, et al. Prognostic impact of vitamin B6 metabolism in lung cancer. Cell Rep 2012; 2:257-69; PMID:22854025; http://dx.doi.org/10.1016/j.celrep.2012.06.017
19. Galluzzi L, Vitale I, Senovilla L, Eisenberg T, Carmona-Gutierrez D, Vacchelli E, et al. Independent transcriptional reprogramming and apoptosis induction by cisplatin. Cell Cycle 2012; 11:3472-80; PMID:22918244; http://dx.doi.org/10.4161/cc.21789
20. Yao Z, Szabadkai G. Transcriptional profiling of apoptosis: cell death classification moves toward the systems era. Cell Cycle 2012; 11:3721-2; PMID:22982998; http://dx.doi.org/10.4161/cc.22116
21. Galluzzi L, Marsili S, Vitale I, Senovilla L, Michels J, Garcia P, et al. Vitamin B6 metabolism influences the intracellular accumulation of cisplatin. Cell Cycle 2013; 12:417-21; PMID:23287530; http://dx.doi.org/10.4161/cc.23275
22. Michels J, Vitale I, Galluzzi L, Adam J, Olaussen KA, Kepp O, et al. Cisplatin resistance associated with PARP hyperactivation. Cancer Res 2013; In press
23. Gibson BA, Kraus WL. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 2012; 13:411-24; PMID:22713970; http://dx.doi.org/10.1038/nrm3376
24. Schreiber V, Dantzer F, Ame JC, de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 2006; 7:517-28; PMID:16829982; http://dx.doi.org/10.1038/nrm1963
25. Jagtap P, Szabó C. Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 2005; 4:421-40; PMID:15864271; http://dx.doi.org/10.1038/nrd1718
26. Villanueva T. Anticancer drugs: Expanding the horizons of PARP inhibitors. Nat Rev Drug Discov 2010; 9:919; PMID:21119729; http://dx.doi.org/ 10.1038/nrd3335
27. Annunziata CM, O'Shaughnessy J. Poly (ADPribose) polymerase as a novel therapeutic target in cancer. Clin Cancer Res 2010; 16:4517-26; PMID:20823142; http://dx.doi.org/10.1158/1078-0432.CCR-10-0526
28. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG. PARP inhibition: PARP1 and beyond. Nat Rev Cancer 2010; 10:293-301; PMID:20200537; http://dx.doi.org/10.1038/nrc2812
29. Audeh MW, Carmichael J, Penson RT, Friedlander M, Powell B, Bell-McGuinn KM, et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet 2010; 376:245-51; PMID:20609468; http://dx.doi.org/10.1016/S0140- 6736(10)60893-8
30. Tutt A, Robson M, Garber JE, Domchek SM, Audeh MW, Weitzel JN, et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet 2010; 376:235-44; PMID:20609467; http://dx.doi.org/10.1016/S0140-6736(10)60892-6
31. McCabe N, Turner NC, Lord CJ, Kluzek K, Bialkowska A, Swift S, et al. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res 2006; 66:8109-15; PMID:16912188; http://dx.doi.org/10.1158/0008-5472.CAN-06-0140
32. Delaney CA, Wang LZ, Kyle S, White AW, Calvert AH, Curtin NJ, et al. Potentiation of temozolomide and topotecan growth inhibition and cytotoxicity by novel poly(adenosine diphosphoribose) polymerase inhibitors in a panel of human tumor cell lines. Clin Cancer Res 2000; 6:2860-7; PMID:10914735
33. Clark CC, Weitzel JN, O'Connor TR. Enhancement of synthetic lethality via combinations of ABT-888, a PARP inhibitor, and carboplatin in vitro and in vivo using BRCA1 and BRCA2 isogenic models. Mol Cancer Ther 2012; 11:1948-58; PMID:22778154; http://dx.doi.org/10.1158/1535-7163.MCT-11-0597
34. Postel-Vinay S, Vanhecke E, Olaussen KA, Lord CJ, Ashworth A, Soria JC. The potential of exploiting DNA-repair defects for optimizing lung cancer treatment. Nat Rev Clin Oncol 2012; 9:144-55; PMID:22330686; http://dx.doi.org/10.1038/nrclinonc.2012.3
35. Ledermann J, Harter P, Gourley C, Friedlander M, Vergote I, Rustin G, et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med 2012; 366:1382-92; PMID:22452356; http://dx.doi.org/10.1056/ NEJMoa1105535
36. Galluzzi L, Aaronson SA, Abrams J, Alnemri ES, Andrews DW, Baehrecke EH, et al. Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 2009; 16:1093-107; PMID:19373242; http://dx.doi.org/10.1038/cdd.2009.44
37. Kepp O, Galluzzi L, Lipinski M, Yuan J, Kroemer G. Cell death assays for drug discovery. Nat Rev Drug Discov 2011; 10:221-37; PMID:21358741; http://dx.doi.org/10.1038/nrd3373
38. Harbron C. A flexible unified approach to the analysis of pre-clinical combination studies. Stat Med 2010; 29:1746-56; PMID:20572122; http://dx.doi.org/10.1002/sim.3916
39. Banáth JP, Olive PL. Expression of phosphorylated histone H2AX as a surrogate of cell killing by drugs that create DNA double-strand breaks. Cancer Res 2003; 63:4347-50; PMID:12907603
40. Zhang P, Castedo M, Tao Y, Violot D, Métivier D, Deutsch E, et al. Caspase independence of radioinduced cell death. Oncogene 2006; 25:7758-70; PMID:16862186; http://dx.doi.org/10.1038/sj.onc.1209744
41. Galluzzi L, Zamzami N, de La Motte Rouge T, Lemaire C, Brenner C, Kroemer G. Methods for the assessment of mitochondrial membrane permeabilization in apoptosis. Apoptosis 2007; 12:803-13; PMID:17294081; http://dx.doi.org/10.1007/ s10495-007-0720-1
42. Berglind H, Pawitan Y, Kato S, Ishioka C, Soussi T. Analysis of p53 mutation status in human cancer cell lines: a paradigm for cell line cross-contamination. Cancer Biol Ther 2008; 7:699-708; PMID:18277095; http://dx.doi.org/10.4161/cbt.7.5.5712
43. Hainaut P, Hernandez T, Robinson A, Rodriguez-Tome P, Flores T, Hollstein M, et al. IARC Database of p53 gene mutations in human tumors and cell lines: updated compilation, revised formats and new visualisation tools. Nucleic Acids Res 1998; 26:205-13; PMID:9399837; http://dx.doi.org/10.1093/nar/26.1.205
44. Petitjean A, Mathe E, Kato S, Ishioka C, Tavtigian SV, Hainaut P, et al. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum Mutat 2007; 28:622-9; PMID:17311302; http://dx.doi.org/10.1002/humu.20495
45. Vitale I, Senovilla L, Jemaà M, Michaud M, Galluzzi L, Kepp O, et al. Multipolar mitosis of tetraploid cells: inhibition by p53 and dependency on Mos. EMBO J 2010; 29:1272-84; PMID:20186124; http://dx.doi.org/10.1038/emboj. 2010.11
46. Mullen P. PARP cleavage as a means of assessing apoptosis. Methods Mol Med 2004; 88:171-81; PMID:14634228