ATM-depletion in breast cancer cells confers sensitivity to PARP inhibition

Journal of Experimental and Clinical Cancer Research

Volumn 32, Issue 1, 2013, Pages

  Gilardini Montani, Maria Saveria ^a   Prodosmo, Andrea ^b   Stagni, Venturina ^c,d   Merli, Dania ^a   Monteonofrio, Laura ^b   Gatti, Veronica ^b   Gentileschi, Maria Pia ^b   Barilà, Daniela ^c,d   Soddu, Silvia ^b  

^a UNIVERSITY OF TUSCIA   (Italy)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

ATM; Breast cancer; Iniparib; Olaparib; PARP inhibitors

Indexed keywords

2 MORPHOLINO 6 (1 THIANTHRENYL) 4 PYRANONE; ATM PROTEIN; BRCA1 PROTEIN; BRCA2 PROTEIN; DOXORUBICIN; INIPARIB; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB;

ARTICLE; BREAST CANCER; CANCER CELL; CELL CYCLE; COLONY FORMATION; CONTROLLED STUDY; CYTOTOXICITY; DEPLETION; DRUG SENSITIVITY; ENZYME INACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; BENZAMIDES; BREAST NEOPLASMS; CELL LINE, TUMOR; DNA DAMAGE; DNA REPAIR; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MCF-7 CELLS; PHTHALAZINES; PIPERAZINES; POLY(ADP-RIBOSE) POLYMERASES; RISK FACTORS;

EID: 84887792084     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/1756-9966-32-95     Document Type: Article

References (32)

1. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T, Nature 2005 434 7035 913 917 10.1038/nature03443 15829966. (Pubitemid 40559005)
2. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, Santarosa M, Dillon KJ, Hickson I, Knights C, Martin NM, Jackson SP, Smith GC, Ashworth A, Nature 2005 434 7035 917 921 10.1038/nature03445 15829967. (Pubitemid 40559006)
3. Genetics of natural populations. Xiii. Recombination and variability in populations of Drosophila Pseudoobscura. Dobzhansky T, Genetics 1946 31 3 269 290.
4. Synthetic lethality and semi-lethality among functionally related mutants of Drosophila melanogaster. Lucchesi JC, Genetics 1968 59 1 37 44 5683639.
5. Integrating genetic approaches into the discovery of anticancer drugs. Hartwell LH, Szankasi P, Roberts CJ, Murray AW, Friend SH, Science 1997 278 5340 1064 1068 10.1126/science.278.5340.1064 9353181. (Pubitemid 27517876)
6. The concept of synthetic lethality in the context of anticancer therapy. Kaelin WG Jr, Nat Rev Cancer 2005 5 9 689 698 10.1038/nrc1691 16110319. (Pubitemid 41486362)
7. Synthetic lethal approaches to breast cancer therapy. Rehman FL, Lord CJ, Ashworth A, Nat Rev Clin Oncol 2010 7 12 718 724 10.1038/nrclinonc.2010.172 20956981.
8. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M, Mortimer P, Swaisland H, Lau A, O'Connor MJ, Ashworth A, Carmichael J, Kaye SB, Schellens JH, de Bono JS, N Engl J Med 2009 361 2 123 134 10.1056/NEJMoa0900212 19553641.
9. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Tutt A, Robson M, Garber JE, Domchek SM, Audeh MW, Weitzel JN, Friedlander M, Arun B, Loman N, Schmutzler RK, Wardley A, Mitchell G, Earl H, Wickens M, Carmichael J, Lancet 2010 376 9737 235 244 10.1016/S0140-6736(10)60892-6 20609467.
10. Olaparib in patients with recurrent high-grade serous or poorly differentiated ovarian carcinoma or triple-negative breast cancer: a phase 2, multicentre, open-label, non-randomised study. Gelmon KA, Tischkowitz M, Mackay H, Swenerton K, Robidoux A, Tonkin K, Hirte H, Huntsman D, Clemons M, Gilks B, Yerushalmi R, Macpherson E, Carmichael J, Oza A, Lancet Oncol 2011 12 9 852 861 10.1016/S1470-2045(11)70214-5 21862407.
11. Stumbling blocks on the path to personalized medicine in breast cancer: the case of PARP inhibitors for BRCA1/2-associated cancers. Balmaña J, Domchek SM, Tutt A, Garber JE, Cancer Discov 2011 1 1 29 34 10.1158/2159-8274. CD-11-0048 22586318.
12. Role of PARP inhibitors in cancer biology and therapy. Davar D, Beumer JH, Hamieh L, Tawbi H, Curr Med Chem 2012 19 23 3907 3921 10.2174/ 092986712802002464 22788767.
13. The DNA damage response and cancer therapy. Lord CJ, Ashworth A, Nature 2012 481 7381 287 294 10.1038/nature10760 22258607.
14. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. McCabe N, Turner NC, Lord CJ, Kluzek K, Bialkowska A, Swift S, Giavara S, O'Connor MJ, Tutt AN, Zdzienicka MZ, Smith GC, Ashworth A, Cancer Res 2006 66 16 8109 8115 10.1158/0008-5472.CAN-06-0140 16912188. (Pubitemid 44299177)
15. A synthetic lethal siRNA screen identifying genes mediating sensitivity to a PARP inhibitor. Turner NC, Lord CJ, Iorns E, Brough R, Swift S, Elliott R, Rayter S, Tutt AN, Ashworth A, EMBO J 2008 27 9 1368 1377 10.1038/emboj.2008.61 18388863. (Pubitemid 351655175)
16. ATM deficiency sensitizes mantle cell lymphoma cells to poly(ADP-ribose) polymerase-1 inhibitors. Williamson CT, Muzik H, Turhan AG, Zamò A, O'Connor MJ, Bebb DG, Lees-Miller SP, Mol Cancer Ther 2010 9 2 347 357 10.1158/1535-7163.MCT-09-0872 20124459.
17. The PARP inhibitor olaparib induces significant killing of ATM-deficient lymphoid tumor cells in vitro and in vivo. Weston VJ, Oldreive CE, Skowronska A, Oscier DG, Pratt G, Dyer MJ, Smith G, Powell JE, Rudzki Z, Kearns P, Moss PA, Taylor AM, Stankovic T, Blood 2010 116 22 4578 4587 10.1182/blood-2010-01-265769 20739657.
18. Multiple roles of ATM in monitoring and maintaining DNA integrity. Derheimer FA, Kastan MB, FEBS Lett 2010 584 17 3675 3681 10.1016/j.febslet.2010. 05.031 20580718.
19. Beyond ATM: the protein kinase landscape of the DNA damage response. Bensimon A, Aebersold R, Shiloh Y, FEBS Lett 2011 585 11 1625 1639 10.1016/j.febslet.2011.05.013 21570395.
20. Ataxia-telangiectasia and the Nijmegen breakage syndrome: related disorders but genes apart. Shiloh Y, Annu Rev Genet 1997 31 635 662 10.1146/annurev.genet.31.1.635 9442910. (Pubitemid 28023722)
21. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Lavin MF, Nat Rev Mol Cell Biol 2008 9 10 759 769 10.1038/nrm2514 18813293.
22. Inherited mutations in breast cancer genes-risk and response. Shuen AY, Foulkes WD, J Mammary Gland Biol Neoplasia 2011 16 1 3 15 10.1007/s10911-011- 9213-5 21461995.
23. p53 centrosomal localization diagnoses ataxia-telangiectasia homozygotes and heterozygotes. Prodosmo A, De Amicis A, Nisticò C, Gabriele M, Di Rocco G, Monteonofrio L, Piane M, Cundari E, Chessa L, Soddu S, J Clin Invest 2013 123 3 1335 1342 10.1172/JCI67289 23454770.
24. Nuclear ataxia-telangiectasia mutated (ATM) mediates the cellular response to DNA double strand breaks in human neuron-like cells. Biton S, Dar I, Mittelman L, Pereg Y, Barzilai A, Shiloh Y, J Biol Chem 2006 281 25 17482 17491 10.1074/jbc.M601895200 16627474.
25. Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. Kao J, Salari K, Bocanegra M, Choi YL, Girard L, Gandhi J, Kwei KA, Hernandez-Boussard T, Wang P, Gazdar AF, Minna JD, Pollack JR, PLoS One 2009 4 7 6146 10.1371/journal.pone. 0006146 19582160.
26. The ATM-mediated DNA-damage response: taking shape. Shiloh Y, Trends Biochem Sci 2006 31 7 402 410 10.1016/j.tibs.2006.05.004 16774833. (Pubitemid 44038916)
27. The combined status of ATM and p53 link tumor development with therapeutic response. Jiang H, Reinhardt HC, Bartkova J, Tommiska J, Blomqvist C, Nevanlinna H, Bartek J, Yaffe MB, Hemann MT, Genes Dev 2009 23 16 1895 1909 10.1101/gad.1815309 19608766.
28. Low expression levels of ATM may substitute for CHEK2/TP53 mutations predicting resistance towards anthracycline and mitomycin chemotherapy in breast cancer. Knappskog S, Chrisanthar R, Løkkevik E, Anker G, Østenstad B, Lundgren S, Risberg T, Mjaaland I, Leirvaag B, Miletic H, Lønning PE, Breast Cancer Res 2012 14 2 47 10.1186/bcr3147 22420423.
29. Cross-platform pathway-based analysis identifies markers of response to the PARP inhibitor olaparib. Daemen A, Wolf DM, Korkola JE, Griffith OL, Frankum JR, Brough R, Jakkula LR, Wang NJ, Natrajan R, Reis-Filho JS, Lord CJ, Ashworth A, Spellman PT, Gray JW, Van't Veer LJ, Breast Cancer Res Treat 2012 135 2 505 517 doi: 10.1007/s10549-012-2188-0. Epub 2012 Aug 9 10.1007/s10549-012-2188-0 22875744.
30. Potential chemotherapeutic activity of 4-iodo-3-nitrobenzamide. Metabolic reduction to the 3-nitroso derivative and induction of cell death in tumor cells in culture. Mendeleyev J, Kirsten E, Hakam A, Buki KG, Kun E, Biochem Pharmacol 1995 50 5 705 714 10.1016/0006-2952(95)00189-7 7669074.
31. Failure of iniparib to inhibit poly(ADP-Ribose) polymerase in vitro. Patel AG, De Lorenzo SB, Flatten KS, Poirier GG, Kaufmann SH, Clin Cancer Res 2012 18 6 1655 1662 10.1158/1078-0432.CCR-11-2890 22291137.
32. Iniparib nonselectively modifies cysteine-containing proteins in tumor cells and is not a bona fide PARP inhibitor. Liu X, Shi Y, Maag DX, Palma JP, Patterson MJ, Ellis PA, Surber BW, Ready DB, Soni NB, Ladror US, Xu AJ, Iyer R, Harlan JE, Solomon LR, Donawho CK, Penning TD, Johnson EF, Shoemaker AR, Clin Cancer Res 2012 18 2 510 523 10.1158/1078-0432.CCR-11-1973 22128301.