PARP inhibitors as p-glyoprotein substrates

Journal of Pharmaceutical Sciences

Volumn 103, Issue 6, 2014, Pages 1913-1920

  Lawlor, Denise ^a   Martin, Patricia ^a   Busschots, Steven ^a   Thery, Julien ^a   O'Leary, John J ^a   Hennessy, Bryan T ^b   Stordal, Britta ^a  

^a ST JAMES S HOSPITAL   (Ireland)

^b BEAUMONT HOSPITAL   (Ireland)

Author keywords

cancer chemotherapy; cell lines; CEP 8983; drug Resistance; olaparib; P glycoprotein; PARP inhibitor; toxicity; veliparib

Indexed keywords

CEP 8983; ELACRIDAR; MULTIDRUG RESISTANCE PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB; UNCLASSIFIED DRUG; VALSPODAR; VELIPARIB; ZOSUQUIDAR; ENZYME INHIBITOR;

ARTICLE; BIOTECHNOLOGY; CONTROLLED STUDY; CYTOTOXICITY ASSAY; DRUG CYTOTOXICITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IC 50; MTT ASSAY; PROTEIN EXPRESSION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; METABOLISM; TUMOR CELL LINE;

CELL LINE, TUMOR; ENZYME INHIBITORS; HUMANS; P-GLYCOPROTEIN; POLY(ADP-RIBOSE) POLYMERASES;

EID: 84901277295     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.23952     Document Type: Article

References (53)

1. Audeh MW, Carmichael J, Penson RT, Friedlander M, Powell B, Bell-McGuinn KM, Scott C, Weitzel JN, Oaknin A, Loman N, Lu K, Schmutzler RK, Matulonis U, Wickens M, Tutt A,. 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.
2. 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,. 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.
3. Materna V, Pleger J, Hoffmann U, Lage H,. 2004. RNA expression of MDR1/P-glycoprotein, DNA-topoisomerase I, and MRP2 in ovarian carcinoma patients: Correlation with chemotherapeutic response. Gynecol Oncol 94: 152-160.
4. Penson RT, Oliva E, Skates SJ, Glyptis T, Fuller AF, Jr. AF Jr., Goodman A, Seiden MV,. 2004. Expression of multidrug resistance-1 protein inversely correlates with paclitaxel response and survival in ovarian cancer patients: A study in serial samples. Gynecol Oncol 93: 98-106.
5. Arts HJG, Katsaros D, de Vries EGE, Massobrio M, Genta F, Danese S, Arisio R, Scheper RJ, Kool M, Scheffer GL, Willemse PHB, van der Zee AGJ, Suurmeijer AJH,. 1999. Drug resistance-associated markers P-glycoprotein, multidrug resistance-associated protein 1, multidrug resistance-associated protein 2, and lung resistance protein as prognostic factors in ovarian carcinoma. Clin Cancer Res 5: 2798-2805.
6. Ozalp SS, Yalcin OT, Tanir M, Kabukcuoglu S, Etiz E,. 2002. Multidrug resistance gene-1 (Pgp) expression in epithelial ovarian malignancies. Eur J Gynaecol Oncol 23: 337-340.
7. Gregorcyk S, Kang Y, Brandt D, Kolm P, Singer G, Perry RR,. 1996. p-Glycoprotein expression as a predictor of breast cancer recurrence. Ann Surg Oncol 3 (1): 8-14.
8. Larkin A, O'Driscoll L, Kennedy S, Purcell R, Moran E, Crown J, Parkinson M, Clynes M,. 2004. Investigation of MRP-1 protein and MDR-1 P-glycoprotein expression in invasive breast cancer: A prognostic study. Int J Cancer 112 (2): 286-294.
9. Atalay C, Demirkazik A, Gunduz U,. 2008. Role of ABCB1 and ABCC1 gene induction on survival in locally advanced breast cancer. J Chemother 20 (6): 734-739.
10. Jazaeri AA, Yee CJ, Sotiriou C, Brantley KR, Boyd J, Liu ET,. 2002. Gene expression profiles of BRCA1-linked, BRCA2-linked, and sporadic ovarian cancers. J Natl Cancer Inst 94: 990-1000.
11. Rottenberg S, Jaspers JE, Kersbergen A, van der BE, 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,. 2008. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc Natl Acad Sci USA 105: 17079-17084.
12. Li X, Delzer J, Voorman R, de Morais SM, Lao Y,. 2011. Disposition and drug-drug interaction potential of veliparib (ABT-888), a novel and potent inhibitor of poly(ADP-ribose) polymerase. Drug Metab Dispos 39: 1161-1169.
13. Stordal B, Hamon M, McEneaney V, Roche S, Gillet JP, O'Leary JJ, Gottesman M, Clynes M,. 2012. Resistance to paclitaxel in a cisplatin-resistant ovarian cancer cell line is mediated by P-glycoprotein. PLoS One 7: e40717.
14. Richert N, Akiyama S, Shen D, Gottesman MM, Pastan I,. 1985. Multiply drug-resistant human KB carcinoma cells have decreased amounts of a 75-kDa and a 72-kDa glycoprotein. Proc Natl Acad Sci USA 82: 2330-2333.
15. Richert ND, Aldwin L, Nitecki D, Gottesman MM, Pastan I,. 1988. Stability and covalent modification of P-glycoprotein in multidrug-resistant KB cells. Biochemistry 27: 7607-7613.
16. Ma J, Maliepaard M, Kolker HJ, Verweij J, Schellens JH,. 1998. Abrogated energy-dependent uptake of cisplatin in a cisplatin-resistant subline of the human ovarian cancer cell line IGROV-1. Cancer Chemother Pharmacol 41: 186-192.
17. Ma J, Maliepaard M, Nooter K, Boersma AW, Verweij J, Stoter G, Schellens JH,. 1998. Synergistic cytotoxicity of cisplatin and topotecan or SN-38 in a panel of eight solid-tumor cell lines in vitro. Cancer Chemother Pharmacol 41: 307-316.
18. Martin A, Clynes M,. 1993. Comparison of 5 microplate colorimetric assays for in vitro cytotoxicity testing and cell proliferation assays. Cytotechnology 11: 49-58.
19. Choudhuri S, Klaassen CD,. 2006. Structure, function, expression, genomic organization, and single-nucleotide polymorphisms of human ABCB1 (MDR1), ABCC (MRP), and ABCG2 (BCRP) efflux transporters. Int J Toxicol 25: 231-259.
20. Hyafil F, Vergely C, Du Vignaud P, Grand-Perret T,. 1993. In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxamide derivative. Cancer Res 53: 4595-4602.
21. Thomas H, Coley HM,. 2003. Overcoming multidrug resistance in cancer: An update on the clinical strategy of inhibiting p-glycoprotein. Cancer Control 10: 159-165.
22. Pichler A, Prior JL, Piwnica-Worms D,. 2004. Imaging reversal of multidrug resistance in living mice with bioluminescence: MDR1 P-glycoprotein transports coelenterazine. Proc Natl Acad Sci USA 101: 1702-1707.
23. Abu, Ajaj K, Graeser R, Kratz F,. 2012. Zosuquidar and an albumin-binding prodrug of zosuquidar reverse multidrug resistance in breast cancer cells of doxorubicin and an albumin-binding prodrug of doxorubicin. Breast Cancer Res Treat 134: 117-129.
24. Mease K, Sane R, Podila L, Taub ME,. 2012. Differential selectivity of efflux transporter inhibitors in Caco-2 and MDCK-MDR1 monolayers: A strategy to assess the interaction of a new chemical entity with P-gp, BCRP, and MRP2. J Pharm Sci 101: 1888-1897.
25. Mistry P, Stewart AJ, Dangerfield W, Okiji S, Liddle C, Bootle D, Plumb JA, Templeton D, Charlton P,. 2001. In vitro and in vivo reversal of P-glycoprotein-mediated multidrug resistance by a novel potent modulator, XR9576. Cancer Res 61: 749-758.
26. Crowe A,. 2002. The influence of P-glycoprotein on morphine transport in Caco-2 cells. Comparison with paclitaxel. Eur J Pharmacol 440: 7-16.
27. Westers TM, Houtenbos I, Schuurhuis GJ, Ossenkoppele GJ, van de Loosdrecht AA,. 2005. Quantification of T-cell mediated apoptosis in heterogeneous leukemia populations using four-color multiparameter flow cytometry. Cytometry 66A: 71-77.
28. Wang X, Weaver DT,. 2011. The ups and downs of DNA repair biomarkers for PARP inhibitor therapies. Am J Cancer Res 1: 301-327.
29. Rajan A, Carter CA, Kelly RJ, Gutierrez M, Kummar S, Szabo E, Yancey MA, Ji J, Mannargudi B, Woo S, Spencer S, Figg WD, Giaccone G,. 2012. A phase I combination study of olaparib with cisplatin and gemcitabine in adults with solid tumors. Clin Cancer Res 18: 2344-2351.
30. Kummar S, Ji J, Morgan R, Lenz HJ, Puhalla SL, Belani CP, Gandara DR, Allen D, Kiesel B, Beumer JH, Newman EM, Rubinstein L, Chen A, Zhang Y, Wang L, Kinders RJ, Parchment RE, Tomaszewski JE, Doroshow JH, 2012. A phase I study of veliparib in combination with metronomic cyclophosphamide in adults with refractory solid tumors and lymphomas. Clin Cancer Res 18: 1726-1734.
31. Fojo A, Akiyama Si, Gottesman MM, Pastan I,. 1985. Reduced drug accumulation in multiply drug-resistant human KB carcinoma cell lines. Cancer Res 45: 3002-3007.
32. Kawai H, Kiura K, Tabata M, Yoshino T, Takata I, Hiraki A, Chikamori K, Ueoka H, Tanimoto M, Harada M,. 2002. Characterization of non-small-cell lung cancer cell lines established before and after chemotherapy. Lung Cancer 35: 305-314.
33. Kuroda H, Sugimoto T, Ueda K, Tsuchida S, Horii Y, Inazawa J, Sato K, Sawada T,. 1991. Different drug sensitivity in two neuroblastoma cell lines established from the same patient before and after chemotherapy. Int J Cancer 47: 732-737.
34. Hida T, Ueda R, Takahashi T, Watanabe H, Kato T, Suyama M, Sugiura T, Ariyoshi Y, Takahashi T,. 1989. Chemosensitivity and radiosensitivity of small cell lung cancer cell lines studied by a newly developed 3-(4,5-Dimethylthiazol- 2-yl)-2,5-diphenyltetrazolium bromide (MTT) hybrid assay. Cancer Res 49: 4785-4790.
35. Berendsen HH, de Leij L, de Vries EGE, Mesander G, Mulder NH, de Jong B, Buys CHCM, Postmus PE, Poppema S, Sluiter HJ, The HT, 1988. Characterization of three small cell lung cancer cell lines established from one patient during longitudinal follow-up. Cancer Res 48: 6891-6899.
36. Sakai W, Swisher EM, Jacquemont C, Chandramohan KV, Couch FJ, Langdon SP, Wurz K, Higgins J, Villegas E, Taniguchi T,. 2009. Functional restoration of BRCA2 protein by secondary BRCA2 mutations in BRCA2-mutated ovarian carcinoma. Cancer Res 69: 6381-6386.
37. Stronach EA, Chen M, Maginn EN, Agarwal R, Mills GB, Wasan H, Gabra H,. 2011. DNA-PK mediates AKT activation and apoptosis inhibition in clinically acquired platinum resistance. Neoplasia 13: 1069-1080.
38. Langdon SP, Lawrie SS, Hay FG, Hawkes MM, McDonald A, Hayward IP, Schol DJ, Hilgers J, Leonard RCF, Smyth JF,. 1988. Characterization and properties of nine human ovarian adenocarcinoma cell lines. Cancer Res 48: 6166-6172.
39. Didziapetris R, Japertas P, Avdeef A, Petrauskas A,. 2003. Classification analysis of P-glycoprotein substrate specificity. J Drug Target 11: 391-406.
40. Wang Z, Chen Y, Liang H, Bender A, Glen RC, Yan A,. 2011. P-glycoprotein substrate models using support vector machines based on a comprehensive data set. J Chem Inf Model 51: 1447-1456.
41. Bikadi Z, Hazai I, Malik D, Jemnitz K, Veres Z, Hari P, Ni Z, Loo TW, Clarke DM, Hazai E, Mao Q,. 2011. Predicting P-glycoprotein-mediated drug transport based on support vector machine and three-dimensional crystal structure of P-glycoprotein. PLoS One 6: e25815.
42. 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,. 2009. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 361: 123-134.
43. Yamamoto N, Nokihara H, Yamada Y, Goto Y, Tanioka M, Shibata T, Yamada K, Asahina H, Kawata T, Shi X, Tamura T,. 2012. A phase I, dose-finding and pharmacokinetic study of olaparib (AZD2281) in Japanese patients with advanced solid tumors. Cancer Sci 103: 504-509.
44. Kummar S, Kinders R, Gutierrez ME, Rubinstein L, Parchment RE, Phillips LR, Ji J, Monks A, Low JA, Chen A, Murgo AJ, Collins J, Steinberg SM, Eliopoulos H, Giranda VL, Gordon G, Helman L, Wiltrout R, Tomaszewski JE, Doroshow JH,. 2009. Phase 0 clinical trial of the poly (ADP-ribose) polymerase inhibitor ABT-888 in patients with advanced malignancies. J Clin Oncol 27 (16): 2705-2711.
45. Hamidovic A, Hahn K, Kolesar J,. 2010. Clinical significance of ABCB1 genotyping in oncology. J Oncol Pharm Pract 16 (1): 39-44.
46. Kaye SB, Lubinski J, Matulonis U, Ang JE, Gourley C, Karlan BY, Amnon A, Bell-McGuinn KM, Chen LM, Friedlander M, Safra T, Vergote I, Wickens M, Lowe ES, Carmichael J, Kaufman B,. 2012. Phase II, open-label, randomized, multicenter study comparing the efficacy and safety of olaparib, a Poly (ADP-ribose) polymerase inhibitor, and pegylated liposomal doxorubicin in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer. J Clin Oncol 30: 372-379.
47. 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,. 2012. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. New Engl J Med 366: 1382-1392.
48. 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,. 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.
49. 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: 2512-2519.
50. Murphy M, Stordal B,. Erlotinib or gefitinib for the treatment of relapsed platinum pretreated non-small cell lung cancer and ovarian cancer: A systematic review. Drug Resist Updat 14 (3): 177-190.
51. Stordal B, Pavlakis N, Davey R,. 2007. Oxaliplatin for the treatment of cisplatin-resistant cancer: A systematic review. Cancer Treat Rev 33: 347-357.
52. Stordal B, Pavlakis N, Davey R,. 2007. A systematic review of platinum and taxane resistance from bench to clinic: An inverse relationship. Cancer Treat Rev 33: 688-703.
53. Stordal B, Timms K, Farrelly A, Gallagher D, Busschots S, Renaud Ml, Thery J, Williams D, Potter J, Tran T, Korpanty G, Cremona M, Carey M, Li J, Li Y, Aslan O, O'Leary JJ, Mills GB, Hennessy BT,. 2013. BRCA1/2 mutation analysis in 41 ovarian cell lines reveals only one functionally deleterious BRCA1 mutation. Mol Oncol 7: 567-579.