Assessing the function of homologous recombination DNA repair in malignant pleural effusion (MPE) samples

British Journal of Cancer

Volumn 111, Issue 1, 2014, Pages 94-100

  Patterson, M J ^a   Sutton, R E ^a   Forrest, I ^b   Sharrock, R ^b   Lane, M ^b   Kaufmann, A ^a,c   O'Donnell, R ^a,c   Edmondson, R J ^a   Wilson, B T ^a   Curtin, N J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b ROYAL VICTORIA INFIRMARY   (United Kingdom)

^c QUEEN ELIZABETH HOSPITAL   (United Kingdom)

Author keywords

DNA repair; homologous recombination; pleural effusion; RAD51

Indexed keywords

CARBOPLATIN; HISTONE H2AX; PACLITAXEL; PEMETREXED; RAD51 PROTEIN; RUCAPARIB; TOPOTECAN;

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CLINICAL ARTICLE; CONTROLLED STUDY; DNA REPAIR; FANCG GENE; FEASIBILITY STUDY; FEMALE; GENE; GENE SEQUENCE; HETEROZYGOSITY LOSS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; LUNG CARCINOMA; LUNG NON SMALL CELL CANCER; MALE; MALIGNANT PLEURA EFFUSION; MESOTHELIOMA; MULTIPLE CYCLE TREATMENT; OVARY CARCINOMA; PARP1 GENE; PRIORITY JOURNAL; RECOMBINATION REPAIR; RPA1 GENE; SARCOMATOID CARCINOMA; VERY ELDERLY;

AGED; AGED, 80 AND OVER; CARCINOMA, NON-SMALL-CELL LUNG; FEASIBILITY STUDIES; FEMALE; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; PLEURAL EFFUSION, MALIGNANT; RECOMBINATIONAL DNA REPAIR;

EID: 84904130556     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2014.261     Document Type: Article

References (45)

1. Birkelbach M, Ferraiolo N, Gheorghiu L, Pfaffle HN, Daly B, Ebright MI, Spencer C, O'Hara C, Whetstine JR, Benes CH, Sequist LV, Zou L, Dahm-Daphi J, Kachnic LA, Willers H (2013) Detection of impaired homologous recombination repair in NSCLC cells and tissues. J Thorac Oncol 8(3): 279-286.
2. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434(7035): 913-917.
3. CGRN (2011) Integrated genomic analyses of ovarian carcinoma. Nature 474(7353): 609-615.
4. CRUK (2013) Cancer Statistics Report: Cancer Mortality in the UK in 2010.
5. Curtin NJ (2012) DNA repair dysregulation from cancer driver to therapeutic target. Nat Rev Cancer 12(12): 801-817.
6. De Bono JS, Mina LA, Gonzalez M, Curtin NJ, Want E, Henshaw JW, Chadha M, Sachdev JC, Matei D, Jameson GS, Ong M, Basu B, Wainberg ZA, Byers LA, Chugh R, Dorr A, Kaye SB, Ramanathan RK (2013) First-in-human trial of novel oral PARP inhibitor BMN 673 in patients with solid tumours. J Clin Oncol 31(suppl): Abstr 2580.
7. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, Sougnez C, Greulich H, Muzny DM, Morgan MB, Fulton L, Fulton RS, Zhang Q, Wendl MC, Lawrence MS, Larson DE, Chen K, Dooling DJ, Sabo A, Hawes AC, Shen H, Jhangiani SN, Lewis LR, Hall O, Zhu Y, Mathew T, Ren Y, Yao J, Scherer SE, Clerc K, Metcalf GA, Ng B, Milosavljevic A, Gonzalez-Garay ML, Osborne JR, Meyer R, Shi X, Tang Y, Koboldt DC, Lin L, Abbott R, Miner TL, Pohl C, Fewell G, Haipek C, Schmidt H, Dunford-Shore BH, Kraja A, Crosby SD, Sawyer CS, Vickery T, Sander S, Robinson J, Winckler W, Baldwin J, Chirieac LR, Dutt A, Fennell T, Hanna M, Johnson BE, Onofrio RC, Thomas RK, Tonon G, Weir BA, Zhao X, Ziaugra L, Zody MC, Giordano T, Orringer MB, Roth JA, Spitz MR, Wistuba II, Ozenberger B, Good PJ, Chang AC, Beer DG, Watson MA, Ladanyi M, Broderick S, Yoshizawa A, Travis WD, Pao W, Province MA, Weinstock GM, Varmus HE, Gabriel SB, Lander ES, Gibbs RA, Meyerson M, Wilson RK (2008) Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455(7216): 1069-1075.
8. Drew Y, Ledermann JA, Jones A, Hall G, Jayson GC, Highley M, Rea D, Glasspool RM, Halford SER, Crosswell G, Colebrook S, Boddy AV, Curtin NJ, Plummer ER (2011a) Phase II trial of the poly(ADP-ribose) polymerase (PARP) inhibitor AG-014699 in BRCA 1 and 2-mutated, advanced ovarian and/or locally advanced or metastatic breast cancer. J Clin Oncol 29(15-suppl): 3104.
9. Drew Y, Mulligan EA, Vong WT, Thomas HD, Kahn S, Kyle S, Mukhopadhyay A, Los G, Hostomsky Z, Plummer ER, Edmondson RJ, Curtin NJ (2011b) Therapeutic potential of poly(ADP-ribose) polymerase inhibitor AG014699 in human cancers with mutated or methylated BRCA1 or BRCA2. J Natl Cancer Inst 103(4): 334-346.
10. Esteller M, Corn PG, Baylin SB, Herman JG (2001) A gene hypermethylation profile of human cancer. Cancer Res 61(8): 3225-3229.
11. 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 (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434(7035): 917-921.
12. Fong PC, Boss DS, Yap TA, Tutt A, Wu PJ, Mergui-Roelvink M, Mortimer P, Swaisland H, Lau A, O'Connor MJ, Ashworth A, Carmichael J, Kaye SB, Schellens JHM, de Bono JS (2009) Inhibition of poly(ADP-Ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 361(2): 123-134.
13. Fong PC, Yap TA, Boss DS, Carden CP, Mergui-Roelvink M, Gourley C, De Greve J, Lubinski J, Shanley S, Messiou C, A'Hern R, Tutt A, Ashworth A, Stone J, Carmichael J, Schellens JHM, de Bono JS, Kaye SB (2010) Poly(ADP)-ribose polymerase inhibition: Frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J Clin Oncol 28(15): 2512-2519.
14. Gaymes TJ, Mohamedali AM, Patterson M, Matto N, Smith A, Kulasekararaj A, Chelliah R, Curtin N, Farzaneh F, Shall S, Mufti GJ (2013) Microsatellite instability induced mutations in DNA repair genes CtIP and MRE11 confer hypersensitivity to poly (ADP-ribose) polymerase inhibitors in myeloid malignancies. Haematologica 98(9): 1397-1406.
15. Graeser M, McCarthy A, Lord CJ, Savage K, Hills M, Salter J, Orr N, Parton M, Smith IE, Reis-Filho JS, Dowsett M, Ashworth A, Turner NC (2010) A marker of homologous recombination predicts pathologic complete response to neoadjuvant chemotherapy in primary breast cancer. Clin Cancer Res 16(24): 6159-6168.
16. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: The next generation. Cell 144(5): 646-674.
17. Hass CS, Lam K, Wold MS (2012) Repair-specific functions of replication protein A. J Biol Chem 287(6): 3908-3918.
18. Hung MS, Lin CK, Leu SW, Wu MY, Tsai YH, Yang CT (2006) Epidermal growth factor receptor mutations in cells from non-small cell lung cancer malignant pleural effusions. Chang Gung Med J 29(4): 373-379.
19. Jin G, Kim MJ, Jeon HS, Choi JE, Kim DS, Lee EB, Cha SI, Yoon GS, Kim CH, Jung TH, Park JY (2010) PTEN mutations and relationship to EGFR, ERBB2, KRAS, and TP53 mutations in non-small cell lung cancers. Lung Cancer 69(3): 279-283.
20. Kastelik JA (2013) Management of malignant pleural effusion. Lung 191(2): 165-175.
21. Kaufman B, Shapira-Frommer R, Schmulzler RK, Audeh MW, Friedlander M, Balmana J, Mitchel G, Fried G, Bowman K, Fielding A, Domchek SM, Sheba C (2013) Olaparib monotherapy in patienrs with advanced cancer and a germ-line BRCA1/2 mutation: An open-label phase II study. J Clin Oncol 31(suppl): Abst 11024.
22. Kennedy RD, D'Andrea AD (2006) DNA repair pathways in clinical practice: Lessons from pediatric cancer susceptibility syndromes. J Clin Oncol 24(23): 3799-3808.
23. Kommajosyula K, Cao Y, Moreau L, D'Andrea A, Shapiro GI (2013) Identification of factors governing sensitivity of NSCLC cell lines to inhibition of poly (ADP-ribose) polymerase (PARP). In Proceedings of the 104th Annual Meeting of the American Association for Cancer Research; 2013 April, pp 6-10.
24. Washington, DC, PA, USA, Cancer Res, 73(8 Suppl): Abstract nr 1781.
25. Ledermann JA, Harter P, Gourley C, Friedlander M, Vergote I, Rustin GJS, Meier W, Shapira-Frommer R, Safra T, Matei D, Fielding A, Macpherson E, Dougherty B, Jurgensmeier JM, Orr M, Matulonis U (2013) Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer (SOC) and a BRCA mutation (BRCAm). J Clin Oncol 31(suppl): Abstr 5505.
26. Marsit CJ, Liu M, Nelson HH, Posner M, Suzuki M, Kelsey KT (2004) Inactivation of the Fanconi anemia/BRCA pathway in lung and oral cancers: Implications for treatment and survival. Oncogene 23(4): 1000-1004.
27. 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 (2006) Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res 66(16): 8109-8115.
28. Michie CO, Sandhu SK, Schelman WR, Molife LR, Wilding G, Omlin AG, Kansra V, Brooks DG, Martel RE, Kaye SB, De Bono JS, Wenham RM (2013) Final results of the pahse I trial of niraparib (MK4827), a poly(ADP)ribose polymerase (PARP) inhibitor incorporating proof of concept biomarker studies and expansion cohorts involving BRCA1/2 mutation carriers, sporadic ovarian, and castration resistant prostate cancer (CRPC). J Clin Oncol 31(suppl): Abstr 2513.
29. Minami D, Takigawa N, Takeda H, Takata M, Ochi N, Ichihara E, Hisamoto A, Hotta K, Tanimoto M, Kiura K (2013) Synergistic effect of olaparib with combination of cisplatin on PTEN-deficient lung cancer cells. Mol Cancer Res 11(2): 140-148.
30. Mukhopadhyay A, Elattar A, Cerbinskaite A, Wilkinson SJ, Drew Y, Kyle S, Los G, Hostomsky Z, Edmondson RJ, Curtin NJ (2010) Development of a functional assay for homologous recombination status in primary cultures of epithelial ovarian tumor and correlation with sensitivity to poly (ADP-ribose) polymerase inhibitors. Clin Cancer Res 16(8): 2344-2351.
31. Mukhopadhyay A, Plummer ER, Elattar A, Soohoo S, Uzir B, Quinn JE, McCluggage WG, Maxwell P, Aneke H, Curtin NJ, Edmondson RJ (2012) Clinicopathological features of homologous recombination-deficient epithelial ovarian cancers: Sensitivity to PARP inhibitors, platinum, and survival. Cancer Res 72(22): 5675-5682.
32. O'Shaughnessy J, Osborne C, Pippen JE, Yoffe M, Patt D, Rocha C, Koo IC, Sherman BM, Bradley C (2011) Iniparib plus chemotherapy in metastatic triple-negative breast cancer. N Engl J Med 364(3): 205-214.
33. Orta ML, Calderon-Montano JM, Dominguez I, Pastor N, Burgos-Moron E, Lopez-Lazaro M, Cortes F, Mateos S, Helleday T (2013) 5-Aza-20-deoxycytidine causes replication lesions that require Fanconi anemiadependent homologous recombination for repair. Nucleic Acids Res 41(11): 5827-5836.
34. Patel AG, De Lorenzo SB, Flatten KS, Poirier GG, Kaufmann SH (2012) Failure of iniparib to inhibit poly(ADP-Ribose) polymerase in vitro. Clin Cancer Res 18(6): 1655-1662.
35. Paul I, Savage KI, Blayney JK, Lamers E, Gately K, Kerr K, Sheaff M, Arthur K, Richard DJ, Hamilton PW, James JA, O'Byrne KJ, Harkin DP, Quinn JE, Fennell DA (2011) PARP inhibition induces BAX/BAK-independent synthetic lethality of BRCA1-deficient non-small cell lung cancer. J Pathol 224(4): 564-574.
36. Postel-Vinay S, Bajrami I, Friboulet L, Elliott R, Fontebasso Y, Dorvault N, Olaussen KA, Andre F, Soria JC, Lord CJ, Ashworth A (2013) A high-throughput screen identifies PARP1/2 inhibitors as a potential therapy for ERCC1-deficient non-small cell lung cancer. Oncogene 32(47): 5377-5387.
37. Roberts ME, Neville E, Berrisford RG, Antunes G, Ali NJ (2010) Management of a malignant pleural effusion: British Thoracic Society Pleural Disease Guideline 2010. Thorax 65(Suppl 2): Ii32-ii40.
38. Sandhu SK, Schelman WR, Wilding G, Moreno V, Baird RD, Miranda S, Hylands L, Riisnaes R, Forster M, Omlin A, Kreischer N, Thway K, Gevensleben H, Sun L, Loughney J, Chatterjee M, Toniatti C, Carpenter CL, Iannone R, Kaye SB, de Bono JS, Wenham RM (2013) The poly(ADPribose) polymerase inhibitor niraparib (MK4827) in BRCA mutation carriers and patients with sporadic cancer: A phase 1 dose-escalation trial. Lancet Oncol 14(9): 882-892.
39. Schelman WR, Sandhu SK, Monreno Garcia V, Wilding G, Sun L, Toniatti C, Stroh M, Kreischer N, Carpenter CL, Molife LR, Kaye SB, De Bono JS, Wenham RM (2011) First-in-human trial of a poly(ADP)-ribose polymerase (PARP) inhibitor MK-4827 in advanced cancer patients with antitumor activity in BRCA-deficient tumors and sporadic ovarian cancers (soc). J Clin Oncol 29(suppl): Abstr 3102.
40. Vollebergh MA, Jonkers J, Linn SC (2012) Genomic instability in breast and ovarian cancers: Translation into clinical predictive biomarkers. Cell Mol Life Sci 69(2): 223-245.
41. Vollebergh MA, Lips EH, Nederlof PM, Wessels LF, Schmidt MK, van Beers EH, Cornelissen S, Holtkamp M, Froklage FE, de Vries EG, Schrama JG, Wesseling J, van de Vijver MJ, van Tinteren H, de Bruin M, Hauptmann M, Rodenhuis S, Linn SC (2011) An aCGH classifier derived from BRCA1-mutated breast cancer and benefit of high-dose platinum-based chemotherapy in HER2-negative breast cancer patients. Ann Oncol 22(7): 1561-1570.
42. Willers H, Taghian AG, Luo CM, Treszezamsky A, Sgroi DC, Powell SN (2009) Utility of DNA repair protein foci for the detection of putative BRCA1 pathway defects in breast cancer biopsies. Mol Cancer Res 7(8): 1304-1309.
43. Wilson JB, Yamamoto K, Marriott AS, Hussain S, Sung P, Hoatlin ME, Mathew CG, Takata M, Thompson LH, Kupfer GM, Jones NJ (2008) FANCG promotes formation of a newly identified protein complex containing BRCA2, FANCD2 and XRCC3. Oncogene 27(26): 3641-3652.
44. Yamamoto K, Ishiai M, Matsushita N, Arakawa H, Lamerdin JE, Buerstedde JM, Tanimoto M, Harada M, Thompson LH, Takata M (2003) Fanconi anemia FANCG protein in mitigating radiation-and enzyme-induced DNA double-strand breaks by homologous recombination in vertebrate cells. Mol Cell Biol 23(15): 5421-5430.
45. Zarogoulidis K, Zarogoulidis P, Darwiche K, Tsakiridis K, Machairiotis N, Kougioumtzi I, Courcoutsakis N, Terzi E, Zaric B, Huang H, Freitag L, Spyratos D (2013) Malignant pleural effusion and algorithm management. J Thorac Dis 5(Suppl 4): S413-S419.