NF-κB signaling mediates acquired resistance after PARP inhibition

Oncotarget

Volumn 6, Issue 6, 2015, Pages 3825-3839

  Nakagawa, Yuko ^a   Sedukhina, Anna S ^a   Okamoto, Naoki ^a   Nagasawa, Satoi ^a   Suzuki, Nao ^a   Ohta, Tomohiko ^a   Hattori, Hiroyoshi ^b   Roche Molina, Marta ^c   Narváez, Ana J ^d   Jeyasekharan, Anand D ^e   Bernal, Juan A ^c   Sato, Ko ^a  

^a ST MARIANNA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL HOSPITAL ORGANIZATION NAGOYA MEDICAL CENTER   (Japan)

^c CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; BORTEZOMIB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; OLAPARIB; RNA; RUCAPARIB; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR;

ARTICLE; CELL DEATH; CONTROLLED STUDY; DRUG SENSITIVITY; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; OVARY CELL; RNA SEQUENCE; SIGNAL TRANSDUCTION; UPREGULATION; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BREAST NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; OVARIAN NEOPLASMS; PATHOLOGY; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

APOPTOSIS; BASE SEQUENCE; BORTEZOMIB; BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FEMALE; GENES, BRCA1; HUMANS; NF-KAPPA B; OVARIAN NEOPLASMS; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84924271972     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2868     Document Type: Article

References (31)

1. 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. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. The New England journal of medicine. 2009; 361:123-134.
2. Yap TA, Sandhu SK, Carden CP, de Bono JS. Poly(ADP-ribose) polymerase (PARP) inhibitors: Exploiting a synthetic lethal strategy in the clinic. CA: a cancer journal for clinicians. 2011; 61:31-49.
3. 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. 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. The lancet oncology. 2011; 12:852-861.
4. Ledermann J, Harter P, Gourley C, Friedlander M, Vergote I, Rustin G, Scott C, Meier W, Shapira-Frommer R, Safra T, Matei D, Macpherson E, Watkins C, Carmichael J, Matulonis U. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. The New England journal of medicine. 2012; 366:1382-1392.
5. Edwards SL, Brough R, Lord CJ, Natrajan R, Vatcheva R, Levine DA, Boyd J, Reis-Filho JS, Ashworth A. Resistance to therapy caused by intragenic deletion in BRCA2. Nature. 2008; 451:1111-1115.
6. Norquist B, Wurz KA, Pennil CC, Garcia R, Gross J, Sakai W, Karlan BY, Taniguchi T, Swisher EM. Secondary somatic mutations restoring BRCA1/2 predict chemotherapy resistance in hereditary ovarian carcinomas. J Clin Oncol. 2011; 29:3008-3015.
7. Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, van der Gulden H, Hiddingh S, Thanasoula M, Kulkarni A, Yang Q, Haffty BG, Tommiska J, Blomqvist C, Drapkin R, Adams DJ, Nevanlinna H, et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nature structural & molecular biology. 2010; 17:688-695.
8. Rottenberg S, Jaspers JE, Kersbergen A, van der Burg E, Nygren AO, Zander SA, Derksen PW, de Bruin M, Zevenhoven J, Lau A, Boulter R, Cranston A, O'Connor MJ, Martin NM, Borst P, Jonkers J. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc Natl Acad Sci U S A. 2008; 105:17079-17084.
9. Sun CK, Zhang F, Xiang T, Chen Q, Pandita TK, Huang Y, Hu MC, Yang Q. Phosphorylation of ribosomal protein S6 confers PARP inhibitor resistance in BRCA1-deficient cancers. Oncotarget. 2014; 5:3375-3385.
10. Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell. 2008; 132:344-362.
11. Hayden MS, Ghosh S. Signaling to NF-kappaB. Genes & development. 2004; 18:2195-2224.
12. Sun SC. Non-canonical NF-kappaB signaling pathway. Cell research. 2011; 21:71-85.
13. Wang CY, Cusack JC Jr, Liu R, Baldwin AS Jr. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-kappaB. Nature medicine. 1999; 5:412-417.
14. Mateo J, Ong M, Tan DS, Gonzalez MA, de Bono JS. Appraising iniparib, the PARP inhibitor that never was-what must we learn? Nature reviews Clinical oncology. 2013; 10:688-696.
15. Ali M, Telfer BA, McCrudden C, O'Rourke M, Thomas HD, Kamjoo M, Kyle S, Robson T, Shaw C, Hirst DG, Curtin NJ, Williams KJ. Vasoactivity of AG014699, a clinically active small molecule inhibitor of poly(ADP-ribose) polymerase: a contributory factor to chemopotentiation in vivo? Clinical cancer research: an official journal of the American Association for Cancer Research. 2009; 15:6106-6112.
16. Murai J, Huang SY, Renaud A, Zhang Y, Ji J, Takeda S, Morris J, Teicher B, Doroshow JH, Pommier Y. Stereospecific PARP trapping by BMN 673 and comparison with olaparib and rucaparib. Molecular cancer therapeutics. 2014; 13:433-443.
17. Rappold I, Iwabuchi K, Date T, Chen J. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. The Journal of cell biology. 2001; 153:613-620.
18. Ayoub N, Jeyasekharan AD, Bernal JA, Venkitaraman AR. HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response. Nature. 2008; 453:682-686.
19. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC bioinformatics. 2011; 12:323.
20. Anders S, McCarthy DJ, Chen Y, Okoniewski M, Smyth GK, Huber W, Robinson MD. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nature protocols. 2013; 8:1765-1786.
21. Kramer A, Green J, Pollard J Jr., Tugendreich S. Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics. 2014; 30:523-530.
22. Fernandez-Majada V, Aguilera C, Villanueva A, Vilardell F, Robert-Moreno A, Aytes A, Real FX, Capella G, Mayo MW, Espinosa L, Bigas A. Nuclear IKK activity leads to dysregulated notch-dependent gene expression in colorectal cancer. Proc Natl Acad Sci U S A. 2007; 104:276-281.
23. Hideshima T, Chauhan D, Richardson P, Mitsiades C, Mitsiades N, Hayashi T, Munshi N, Dang L, Castro A, Palombella V, Adams J, Anderson KC. NF-kappa B as a therapeutic target in multiple myeloma. The Journal of biological chemistry. 2002; 277:16639-16647.
24. Hideshima T, Ikeda H, Chauhan D, Okawa Y, Raje N, Podar K, Mitsiades C, Munshi NC, Richardson PG, Carrasco RD, Anderson KC. Bortezomib induces canonical nuclear factor-kappaB activation in multiple myeloma cells. Blood. 2009; 114:1046-1052.
25. Li C, Chen S, Yue P, Deng X, Lonial S, Khuri FR, Sun SY. Proteasome inhibitor PS-341 (bortezomib) induces calpain-dependent IkappaB(alpha) degradation. The Journal of biological chemistry. 2010; 285:16096-16104.
26. Hideshima T, Richardson P, Chauhan D, Palombella VJ, Elliott PJ, Adams J, Anderson KC. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer research. 2001; 61:3071-3076.
27. Baud V, Karin M. Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nature reviews Drug discovery. 2009; 8:33-40.
28. Gilmore TD, Herscovitch M. Inhibitors of NF-kappaB signaling: 785 and counting. Oncogene. 2006; 25:6887-6899.
29. Sato K, Sundaramoorthy E, Rajendra E, Hattori H, Jeyasekharan AD, Ayoub N, Schiess R, Aebersold R, Nishikawa H, Sedukhina AS, Wada H, Ohta T, Venkitaraman AR. A DNA-damage selective role for BRCA1 E3 ligase in claspin ubiquitylation, CHK1 activation, and DNA repair. Current biology: CB. 2012; 22:1659-1666.
30. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols. 2009; 4:44-57.
31. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic acids research. 2009; 37:1-13.