The interaction of bortezomib with multidrug transporters: Implications for therapeutic applications in advanced multiple myeloma and other neoplasias

Cancer Chemotherapy and Pharmacology

Volumn 71, Issue 5, 2013, Pages 1357-1368

  O'Connor, Robert ^a   Ooi, Melissa G ^a,b   Meiller, Justine ^a   Jakubikova, Jana ^b   Klippel, Steffen ^b   Delmore, Jake ^b   Richardson, Paul ^b   Anderson, Kenneth ^b   Clynes, Martin ^a   Mitsiades, Constantine S ^b   O'Gorman, Peter ^a,c  

^a DUBLIN CITY UNIVERSITY   (Ireland)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MATER MISERICORDIAE UNIVERSITY HOSPITAL   (Ireland)

Author keywords

Bortezomib; Co culture; Elacridar; MDR protein; P glycoprotein

Indexed keywords

BORTEZOMIB; BREAST CANCER RESISTANCE PROTEIN; ELACRIDAR; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; RHODAMINE 123;

ARTICLE; CANCER CELL CULTURE; CELL VIABILITY; COCULTURE; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG CYTOTOXICITY; DRUG RESISTANCE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MULTIPLE MYELOMA; NEOPLASM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STROMA CELL; TUMOR MICROENVIRONMENT;

ANTINEOPLASTIC AGENTS; BIOLOGICAL TRANSPORT; BORONIC ACIDS; CELL LINE; CELL LINE, TUMOR; CELLULAR MICROENVIRONMENT; COCULTURE TECHNIQUES; DRUG RESISTANCE, NEOPLASM; FLUORESCENT DYES; GENE EXPRESSION REGULATION; HUMANS; MULTIPLE MYELOMA; P-GLYCOPROTEIN; PYRAZINES; RHODAMINE 123; STROMAL CELLS;

EID: 84877927768     PISSN: 03445704     EISSN: 14320843     Source Type: Journal    
DOI: 10.1007/s00280-013-2136-7     Document Type: Article

References (51)

1. Richardson PG, Mitsiades C, Schlossman R, Munshi N, Anderson K (2007) New drugs for myeloma. Oncologist 12:664-689
2. O'Connor R (2007) The pharmacology of cancer resistance. Anticancer Res 27:1267-1272
3. Yang HH, Ma MH, Vescio RA, Berenson JR (2003) Overcoming drug resistance in multiple myeloma: the emergence of therapeutic approaches to induce apoptosis. J Clin Oncol 21:4239-4247
4. Grogan TM, Spier CM, Salmon SE et al (1993) P-glycoprotein expression in human plasma cell myeloma: correlation with prior chemotherapy. Blood 81:490-495
5. Sonneveld P, Suciu S, Weijermans P et al (2001) Cyclosporin A combined with vincristine, doxorubicin and dexamethasone (VAD) compared with VAD alone in patients with advanced refractory multiple myeloma: an EORTC-HOVON randomized phase III study (06914). Br J Haematol 115:895-902
6. Dalton WS, Crowley JJ, Salmon SS et al (1995) A phase III randomized study of oral verapamil as a chemosensitizer to reverse drug resistance in patients with refractory myeloma. A Southwest Oncology Group study. Cancer 75:815-820
7. Friedenberg WR, Rue M, Blood EA et al (2006) Phase III study of PSC-833 (valspodar) in combination with vincristine, doxorubicin, and dexamethasone (valspodar/VAD) versus VAD alone in patients with recurring or refractory multiple myeloma (E1A95): a trial of the Eastern Cooperative Oncology Group. Cancer 106:830-838
8. Sonneveld P, Marie JP, Huisman C et al (1996) Reversal of multidrug resistance by SDZ PSC 833, combined with VAD (vincristine, doxorubicin, dexamethasone) in refractory multiple myeloma. A phase I study. Leukemia 10:1741-1750
9. Rumpold H, Salvador C, Wolf AM, Tilg H, Gastl G, Wolf D (2007) Knockdown of PgP resensitizes leukemic cells to proteasome inhibitors. Biochem Biophys Res Commun 361:549-554
10. Loo TW, Clarke DM (1999) The human multidrug resistance P-glycoprotein is inactive when its maturation is inhibited: potential for a role in cancer chemotherapy. FASEB J 13:1724-1732
11. Duffy CP, Elliott CJ, O'Connor RA et al (1998) Enhancement of chemotherapeutic drug toxicity to human tumour cells in vitro by a subset of non-steroidal anti-inflammatory drugs (NSAIDs). Eur J Cancer 34:1250-1259
12. Clynes M, Redmond A, Moran E, Gilvarry U (1992) Multiple drug-resistance in variant of a human non-small cell lung carcinoma cell line, DLKP-A. Cytotechnology 10:75-89
13. Murphy L, Clynes M, Keenan J (2007) Proteomic analysis to dissect mitoxantrone resistance-associated proteins in a squamous lung carcinoma. Anticancer Res 27:1277-1284
14. Collins DM, Crown J, O'Donovan N et al (2010) Tyrosine kinase inhibitors potentiate the cytotoxicity of MDR-substrate anticancer agents independent of growth factor receptor status in lung cancer cell lines. Invest New Drugs 28(4):433-444
15. Roovers DJ, van Vliet M, Bloem AC, Lokhorst HM (1999) Idarubicin overcomes P-glycoprotein-related multidrug resistance: comparison with doxorubicin and daunorubicin in human multiple myeloma cell lines. Leuk Res 23:539-548
16. Sarver JG, Klis WA, Byers JP, Erhardt PW (2002) Microplate screening of the differential effects of test agents on Hoechst 33342, rhodamine 123, and rhodamine 6G accumulation in breast cancer cells that overexpress P-glycoprotein. J Biomol Screen 7:29-34
17. Martin A, Clynes M (1991) Acid phosphatase: endpoint for in vitro toxicity tests. In Vitro Cell Dev Biol 27A:183-184
18. McMillin DW, Delmore J, Weisberg E et al (2010) Tumor cell-specific bioluminescence platform to identify stroma-induced changes to anticancer drug activity. Nat Med 16:483-489
19. McMillin DW, Ooi M, Delmore J et al (2009) Antimyeloma activity of the orally bioavailable dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor NVP-BEZ235. Cancer Res 69:5835-5842
20. Ooi MG, Hayden PJ, Kotoula V et al (2009) Interactions of the Hdm2/p53 and proteasome pathways may enhance the antitumor activity of bortezomib. Clin Cancer Res 15(23):7153-7160
21. Schmidmaier R, Baumann P, Meinhardt G (2006) Cell-cell contact mediated signalling - no fear of contact. Exp Oncol 28:12-15
22. Chou TC, Talalay P (1983) Analysis of combined drug effects: a new look at a very old problem. Trends Pharmacol Sci 4:450-454
23. Chou TC, Talalay P (1984) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzym Regul 22:27-55
24. Hideshima T, Mitsiades C, Tonon G, Richardson PG, Anderson KC (2007) Understanding multiple myeloma pathogenesis in the bone marrow to identify new therapeutic targets. Nat Rev Cancer 7:585-598
25. Nakamura T, Tanaka K, Matsunobu T et al (2007) The mechanism of cross-resistance to proteasome inhibitor bortezomib and overcoming resistance in Ewing's family tumor cells. Int J Oncol 31:803-811
26. Iijima M, Momose I, Ikeda D (2010) Increased ABCB1 expression in TP-110-resistant RPMI-8226 cells. Biosci Biotechnol Biochem 74:1913-1919
27. Styczynski J, Olszewska-Slonina D, Kolodziej B, Napieraj M, Wysocki M (2006) Activity of bortezomib in glioblastoma. Anticancer Res 26:4499-4503
28. Wiberg K, Carlson K, Aleskog A, Larsson R, Nygren P, Lindhagen E (2009) In vitro activity of bortezomib in cultures of patient tumour cells - potential utility in haematological malignancies. Med Oncol 26:193-201
29. Fujita T, Washio K, Takabatake D et al (2005) Proteasome inhibitors can alter the signaling pathways and attenuate the P-glycoprotein-mediated multidrug resistance. Int J Cancer 117:670-682
30. Lu S, Chen Z, Yang J et al (2010) The effects of proteasome inhibitor bortezomib on a P-gp positive leukemia cell line K562/A02. Int J Lab Hematol 32(1 pt 1):e123-131
31. Minderman H, Zhou Y, O'Loughlin KL, Baer MR (2007) Bortezomib activity and in vitro interactions with anthracyclines and cytarabine in acute myeloid leukemia cells are independent of multidrug resistance mechanisms and p53 status. Cancer Chemother Pharmacol 60:245-255
32. Mitsiades N, Mitsiades CS, Richardson PG et al (2003) The proteasome inhibitor PS-341 potentiates sensitivity of multiple myeloma cells to conventional chemotherapeutic agents: therapeutic applications. Blood 101:2377-2380
33. Schwarzenbach H (2002) Expression of MDR1/P-glycoprotein, the multidrug resistance protein MRP, and the lung-resistance protein LRP in multiple myeloma. Med Oncol 19:87-104
34. Kuo MT, Liu Z, Wei Y et al (2002) Induction of human MDR1 gene expression by 2-acetylaminofluorene is mediated by effectors of the phosphoinositide 3-kinase pathway that activate NF-kappaB signaling. Oncogene 21:1945-1954
35. Thevenod F, Friedmann JM, Katsen AD, Hauser IA (2000) Up-regulation of multidrug resistance P-glycoprotein via nuclear factor-kappaB activation protects kidney proximal tubule cells from cadmium- and reactive oxygen species-induced apoptosis. J Biol Chem 275:1887-1896
36. Ros JE, Schuetz JD, Geuken M et al (2001) Induction of Mdr1b expression by tumor necrosis factor-alpha in rat liver cells is independent of p53 but requires NF-kappaB signaling. Hepatology 33:1425-1431
37. Zhang Y, Shi Y, Li X et al (2008) Proteasome inhibitor MG132 reverses multidrug resistance of gastric cancer through enhancing apoptosis and inhibiting P-gp. Cancer Biol Ther 7:540-546
38. Bentires-Alj M, Barbu V, Fillet M et al (2003) NF-kappaB transcription factor induces drug resistance through MDR1 expression in cancer cells. Oncogene 22:90-97
39. Werts ED, DeGowin RL, Knapp SK, Gibson DP (1980) Characterization of marrow stromal (fibroblastoid) cells and their association with erythropoiesis. Exp Hematol 8:423-433
40. Chauhan D, Uchiyama H, Akbarali Y et al (1996) Multiple myeloma cell adhesion-induced interleukin-6 expression in bone marrow stromal cells involves activation of NF-kappa B. Blood 87:1104-1112
41. Hideshima T, Chauhan D, Schlossman R, Richardson P, Anderson KC (2001) The role of tumor necrosis factor alpha in the pathophysiology of human multiple myeloma: therapeutic applications. Oncogene 20:4519-4527
42. Urashima M, Ogata A, Chauhan D et al (1996) Transforming growth factor-beta1: differential effects on multiple myeloma versus normal B cells. Blood 87:1928-1938
43. Podar K, Anderson KC (2005) The pathophysiologic role of VEGF in hematologic malignancies: therapeutic implications. Blood 105:1383-1395
44. Jakubikova J, Adamia S, Kost-Alimova M et al (2011) Lenalidomide targets clonogenic side population in multiple myeloma: pathophysiologic and clinical implications. Blood 117:4409-4419
45. McMillin DW, Negri JM, Mitsiades CS (2013) The role of tumour-stromal interactions in modifying drug response: challenges and oppurtunities. Nat Rev Drug Discov 12(3):217-228
46. McMillin DW, Delmore J, Negri J, Ooi M, Klippel S, Miduturu CV, Gray NS, Richardson PG, Anderson KC, Kung AL, Mitsiades CS (2011) Microenvironmental influence on pre-clinical activity of polo-like kinase inhibition in multiple myeloma: implications for clinical translation. PLoS One 6(7):e2022647
47. Pessina A, Piccirillo M, Mineo E et al (1999) Role of SR-4987 stromal cells in the modulation of doxorubicin toxicity to in vitro granulocyte- macrophage progenitors (CFU-GM). Life Sci 65:513-523
48. Perez LE, Parquet N, Meads M, Anasetti C, Dalton W (2010) Bortezomib restores stroma-mediated APO2L/TRAIL apoptosis resistance in multiple myeloma. Eur J Haematol 84(3):212-222
49. Garcia MG, Alaniz LD, Cordo Russo RI, Alvarez E, Hajos SE (2009) PI3K/Akt inhibition modulates multidrug resistance and activates NF-kappaB in murine lymphoma cell lines. Leuk Res 33:288-296
50. Petrylak DP, Scher HI, Reuter V, O'Brien JP, Cordon-Cardo C (1994) P-glycoprotein expression in primary and metastatic transitional cell carcinoma of the bladder. Ann Oncol 5:835-840
51. Mitsiades CS, Davies FE, Laubach JP et al (2011) Future directions of next-generation novel therapies, combination approaches, and the development of personalized medicine in myeloma. J Clin Oncol 29:1916-1923