Poly (ADP) ribose polymerase enzyme inhibitor, veliparib, potentiates chemotherapy and radiation in vitro and in vivo in small cell lung cancer

Cancer Medicine

Volumn 3, Issue 6, 2014, Pages 1579-1594

  Owonikoko, Taofeek K ^a,b   Zhang, Guojing ^a   Deng, Xingming ^a,b   Rossi, Michael R ^a   Switchenko, Jeffrey M ^b,c   Doho, Gregory H ^a   Chen, Zhengjia ^b,c   Kim, Sungjin ^b   Strychor, Sandy ^d   Christner, Susan M ^d   Beumer, Jan ^d   Li, Chunyang ^b   Yue, Ping ^a   Chen, Alice ^e   Sica, Gabriel L ^a   Ramalingam, Suresh S ^a,b   Kowalski, Jeanne ^b,c   Khuri, Fadlo R ^a,b   Sun, Shi Yong ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c EMORY UNIVERSITY   (United States)

^d UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Carboplatin; Cisplatin; Etoposide; PARP; SCLC; Veliparib (ABT 888)

Indexed keywords

ANTINEOPLASTIC AGENT; BENZIMIDAZOLE DERIVATIVE; CARBOPLATIN; CISPLATIN; ETOPOSIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; VELIPARIB;

ANIMAL; CHEMORADIOTHERAPY; DRUG POTENTIATION; DRUG SCREENING; HUMAN; IN VITRO STUDY; LUNG NEOPLASMS; MOUSE; NUDE MOUSE; PATHOLOGY; RANDOMIZATION; SMALL CELL LUNG CARCINOMA; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BENZIMIDAZOLES; CARBOPLATIN; CELL LINE, TUMOR; CHEMORADIOTHERAPY; CISPLATIN; DRUG SYNERGISM; ETOPOSIDE; HUMANS; IN VITRO TECHNIQUES; LUNG NEOPLASMS; MICE; MICE, NUDE; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; RANDOM ALLOCATION; SMALL CELL LUNG CARCINOMA; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84990944566     PISSN: None     EISSN: 20457634     Source Type: Journal    
DOI: 10.1002/cam4.317     Document Type: Article

References (52)

1. Shrivastav, M., L. P. De Haro, and J. A. Nickoloff. 2008. Regulation of DNA double-strand break repair pathway choice. Cell Res. 18:134-147.
2. Ishizuka, S., K. Martin, C. Booth, C. S. Potten, G. de Murcia, A. Burkle, et al. 2003. Poly (ADP-ribose) polymerase-1 is a survival factor for radiation-exposed intestinal epithelial stem cells in vivo. Nucleic Acids Res. 31:6198-6205.
3. Memisoglu, A., and L. Samson. 2000. Base excision repair in yeast and mammals. Mutat. Res. 451:39-51.
4. D'Amours, D., F. R. Sallmann, V. M. Dixit, and G. G. Poirier. 2001. Gain-of-function of poly (ADP-ribose) polymerase-1 upon cleavage by apoptotic proteases: implications for apoptosis. J. Cell Sci. 114:3771-3778.
5. Schreiber, V., J. C. Ame, P. Dolle, I. Schultz, B. Rinaldi, V. Fraulob, et al. 2002. Poly (ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J. Biol. Chem. 2002(277):23028-23036.
6. Ruscetti, T., B. E. Lehnert, J. Halbrook, H. Le Trong, M. F. Hoekstra, D. J. Chen, et al. 1998. Stimulation of the DNA-dependent protein kinase by poly (ADP-ribose) polymerase. J. Biol. Chem. 273:14461-14467.
7. Farmer, H., N. McCabe, C. J. Lord, A. N. Tutt, D. A. Johnson, T. B. Richardson, et al. 2005. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434:917-921.
8. Audeh, M. W., J. Carmichael, R. T. Penson, M. Friedlander, B. Powell, K. M. Bell-McGuinn, et al. 2010. Oral poly (ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet 376:245-251.
9. Tutt, A., M. Robson, J. E. Garber, S. M. Domchek, M. W. Audeh, J. N. Weitzel, et al. 2010. Oral poly (ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet 376:235-244.
10. Gelmon, K. A., M. Tischkowitz, H. Mackay, K. Swenerton, A. Robidoux, K. Tonkin, et al. 2011. 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. Lancet Oncol. 12:852-861.
11. Banerjee, S., S. B. Kaye, and A. Ashworth. 2010. Making the best of PARP inhibitors in ovarian cancer. Nat. Rev. Clin. Oncol. 7:508-519.
12. Donawho, C. K., Y. Luo, Y. Luo, T. D. Penning, J. L. Bauch, J. J. Bouska, et al. 2007. ABT-888, an orally active poly (ADP-ribose) polymerase inhibitor that potentiates DNA-damaging agents in preclinical tumor models. Clin. Cancer Res. 13:2728-2737.
13. Rouleau, M., A. Patel, M. J. Hendzel, S. H. Kaufmann, and G. G. Poirier. 2010. PARP inhibition: PARP1 and beyond. Nat. Rev. Cancer 10:293-301.
14. Sandhu, S. K., T. A. Yap, and J. S. de Bono. 2010. Poly (ADP-ribose) polymerase inhibitors in cancer treatment: a clinical perspective. Eur. J. Cancer 46:9-20.
15. Kummar, S., R. Kinders, M. E. Gutierrez, L. Rubinstein, R. E. Parchment, L. R. Phillips, et al. 2009. Phase 0 clinical trial of the poly (ADP-ribose) polymerase inhibitor ABT-888 in patients with advanced malignancies. J. Clin. Oncol. 27:2705-2711.
16. O'Shaughnessy, J., C. Osborne, J. E. Pippen, M. Yoffe, D. Patt, C. Rocha, et al. 2011. Iniparib plus chemotherapy in metastatic triple-negative breast cancer. N. Engl. J. Med. 364:205-214.
17. Samol, J., M. Ranson, E. Scott, E. Macpherson, J. Carmichael, A. Thomas, et al. 2012. Safety and tolerability of the poly (ADP-ribose) polymerase (PARP) inhibitor, olaparib (AZD2281) in combination with topotecan for the treatment of patients with advanced solid tumors: a phase I study. Invest. New Drugs 30:1493-1500.
18. Rajan, A., C. A. Carter, R. J. Kelly, M. Gutierrez, S. Kummar, E. Szabo, et al. 2012. A phase I combination study of olaparib with cisplatin and gemcitabine in adults with solid tumors. Clin. Cancer Res. 18:2344-2351.
19. Horn, L., E. L. Castellanos, and D. H. Johnson. 2011. Update on new drugs in small cell lung cancer. Expert Opin. Investig. Drugs 20:441-445.
20. Rossi, A., P. Maione, G. Palazzolo, P. C. Sacco, M. L. Ferrara, M. Falanga, et al. 2008. New targeted therapies and small-cell lung cancer. Clin. Lung Cancer 9:271-279.
21. Owonikoko, T. K., M. Behera, Z. Chen, C. Bhimani, W. J. Curran, F. R. Khuri, et al. 2012. A systematic analysis of efficacy of second-line chemotherapy in sensitive and refractory small-cell lung cancer. J. Thorac. Oncol. 7:866-872.
22. Lee, J. H., K. S. Park, A. T. Alberobello, B. Kallakury, M. T. Weng, Y. Wang, et al. 2013. The Janus kinases inhibitor AZD1480 attenuates growth of small cell lung cancers in vitro and in vivo. Clin. Cancer Res. 19:6777-6786.
23. Lara, P. N., Jr., K. Chansky, T. Shibata, H. Fukuda, T. Tamura, J. Crowley, et al. 2010. Common arm comparative outcomes analysis of phase 3 trials of cisplatin + irinotecan versus cisplatin + etoposide in extensive stage small cell lung cancer: final patient-level results from Japan Clinical Oncology Group 9511 and Southwest Oncology Group 0124. Cancer 116:5710-5715.
24. Byers, L. A., J. Wang, M. B. Nilsson, J. Fujimoto, P. Saintigny, J. Yordy, et al. 2012. Proteomic profiling identifies dysregulated pathways in small cell lung cancer and novel therapeutic targets including PARP1. Cancer Dis. 2:798-811.
25. Chou, T. C. 2010. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 70:440-446.
26. Owonikoko, T. K., S. S. Ramalingam, B. Kanterewicz, T. E. Balius, C. P. Belani, and P. A. Hershberger. 2010. Vorinostat increases carboplatin and paclitaxel activity in non-small-cell lung cancer cells. Int. J. Cancer 126:743-755.
27. Parise, R. A., M. Shawaqfeh, M. J. Egorin, and J. H. Beumer. 2008. Liquid chromatography-mass spectrometric assay for the quantitation in human plasma of ABT-888, an orally available, small molecule inhibitor of poly (ADP-ribose) polymerase. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 872:141-147.
28. Colville, H., R. Dzadony, R. Kemp, S. Stewart, H. J. Zeh, III, D. L. Bartlett, et al. 2010. In vitro circuit stability of 5-fluorouracil and oxaliplatin in support of hyperthermic isolated hepatic perfusion. J. Extra Corpor. Technol. 42:75-79.
29. Bolstad, B. M., R. A. Irizarry, M. Astrand, and T. P. Speed. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185-193.
30. Northcott, P. A., D. J. Shih, M. Remke, Y. J. Cho, M. Kool, C. Hawkins, et al. 2012. Rapid, reliable, and reproducible molecular sub-grouping of clinical medulloblastoma samples. Acta Neuropathol. 123:615-626.
31. Geiss, G. K., R. E. Bumgarner, B. Birditt, T. Dahl, N. Dowidar, D. L. Dunaway, et al. 2008. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat. Biotechnol. 26:317-325.
32. Cardnell, R. J., Y. Feng, L. Diao, Y. H. Fan, F. Masrorpour, J. Wang, et al. 2013. Proteomic markers of DNA repair and PI3K pathway activation predict response to the PARP inhibitor BMN 673 in small cell lung cancer. Clin. Cancer Res. 19:6322-6328.
33. Fong, P. C., D. S. Boss, T. A. Yap, A. Tutt, P. Wu, M. Mergui-Roelvink, et al. 2009. Inhibition of poly (ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med. 361:123-134.
34. Collis, S. J., M. J. Swartz, W. G. Nelson, and T. L. DeWeese. 2003. Enhanced radiation and chemotherapy-mediated cell killing of human cancer cells by small inhibitory RNA silencing of DNA repair factors. Cancer Res. 63:1550-1554.
35. Madhusudan, S., and M. R. Middleton. 2005. The emerging role of DNA repair proteins as predictive, prognostic and therapeutic targets in cancer. Cancer Treat. Rev. 31:603-617.
36. Cheng, H., Z. Zhang, A. Borczuk, C. A. Powell, A. S. Balajee, H. B. Lieberman, et al. 2013. PARP inhibition selectively increases sensitivity to cisplatin in ERCC1-low non-small cell lung cancer cells. Carcinogenesis 34:739-749.
37. Patel, A. G., J. N. Sarkaria, and S. H. Kaufmann. 2011. Nonhomologous end joining drives poly (ADP-ribose) polymerase (PARP) inhibitor lethality in homologous recombination-deficient cells. Proc. Natl Acad. Sci. USA 108:3406-3411.
38. Murai, J., S. Y. Huang, B. B. Das, A. Renaud, Y. Zhang, J. H. Doroshow, et al. 2012. Trapping of PARP1 and PARP2 by Clinical PARP Inhibitors. Cancer Res. 72:5588-5599.
39. Murai, J., S. Y. Huang, A. Renaud, Y. Zhang, J. Ji, S. Takeda, et al. 2014. Stereospecific PARP trapping by BMN 673 and comparison with olaparib and rucaparib. Mol. Cancer Ther. 13:433-443.
40. Kovacs, K., A. Toth, P. Deres, T. Kalai, K. Hideg, and B. Sumegi. 2004. Myocardial protection by selective poly (ADP-ribose) polymerase inhibitors. Exp. Clin. Cardiol. 9:17-20.
41. Miknyoczki, S., H. Chang, J. Grobelny, S. Pritchard, C. Worrell, N. McGann, et al. 2007. The selective poly (ADP-ribose) polymerase-1(2) inhibitor, CEP-8983, increases the sensitivity of chemoresistant tumor cells to temozolomide and irinotecan but does not potentiate myelotoxicity. Mol. Cancer Ther. 6:2290-2302.
42. Nguyen, D., M. Zajac-Kaye, L. Rubinstein, D. Voeller, J. E. Tomaszewski, S. Kummar, et al. 2011. Poly (ADP-ribose) polymerase inhibition enhances p53-dependent and -independent DNA damage responses induced by DNA damaging agent. Cell Cycle 10:4074-4082.
43. Huntoon, C. J., K. S. Flatten, A. E. Wahner Hendrickson, A. M. Huehls, S. L. Sutor, S. H. Kaufmann, et al. 2013. ATR inhibition broadly sensitizes ovarian cancer cells to chemotherapy independent of BRCA status. Cancer Res. 73:3683-3691.
44. Fong, P. C., T. A. Yap, D. S. Boss, C. P. Carden, M. Mergui-Roelvink, C. Gourley, et al. 2010. Poly (ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J. Clin. Oncol. 28:2512-2519.
45. Stronach, E. A., M. Chen, E. N. Maginn, R. Agarwal, G. B. Mills, H. Wasan, et al. 2011. DNA-PK mediates AKT activation and apoptosis inhibition in clinically acquired platinum resistance. Neoplasia 13:1069-1080.
46. Juvekar, A., L. N. Burga, H. Hu, E. P. Lunsford, Y. H. Ibrahim, J. Balmana, et al. 2012. Combining a PI3K inhibitor with a PARP inhibitor provides an effective therapy for BRCA1-related breast cancer. Cancer Dis. 2:1048-1063.
47. Sand-Dejmek, J., G. Adelmant, B. Sobhian, A. S. Calkins, J. Marto, D. J. Iglehart, et al. 2011. Concordant and opposite roles of DNA-PK and the "facilitator of chromatin transcription" (FACT) in DNA repair, apoptosis and necrosis after cisplatin. Mol. Cancer 10:74.
48. Dejmek, J., J. D. Iglehart, and J. B. Lazaro. 2009. DNA-dependent protein kinase (DNA-PK)-dependent cisplatin-induced loss of nucleolar facilitator of chromatin transcription (FACT) and regulation of cisplatin sensitivity by DNA-PK and FACT. Mol. Cancer Res. 7:581-591.
49. Shao, C. J., Y. F. Xia, H. L. Shi, J. Y. Zhang, Y. X. He, and Z. P. Chen. 2006. Correlation of DNA-PK activity with anti-cancer drug-sensitivity in human gliomas. Zhonghua Zhong Liu Za Zhi 28:342-344.
50. Ariumi, Y., M. Masutani, T. D. Copeland, T. Mimori, T. Sugimura, K. Shimotohno, et al. 1999. Suppression of the poly (ADP-ribose) polymerase activity by DNA-dependent protein kinase in vitro. Oncogene 18:4616-4625.
51. Veuger, S. J., N. J. Curtin, C. J. Richardson, G. C. Smith, and B. W. Durkacz. 2003. Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly (ADP-ribose) polymerase-1. Cancer Res. 63:6008-6015.
52. Mitchell, J., G. C. Smith, and N. J. Curtin. 2009. Poly (ADP-Ribose) polymerase-1 and DNA-dependent protein kinase have equivalent roles in double strand break repair following ionizing radiation. Int. J. Radiat. Oncol. Biol. Phys. 75:1520-1527.