Multidrug resistance modulators and doxorubicin synergize to elevate ceramide levels and elicit apoptosis in drug-resistant cancer cells

Cancer

Volumn 86, Issue 2, 1999, Pages 300-311

  Lucci, Anthony ^a,b   Han, Tie Yan ^a   Liu, Yong Yu ^a   Giuliano, Armando E ^a   Cabot, Myles C ^a  

^a JOHN WAYNE CANCER INSTITUTE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Breast carcinoma; Ceramide; Multidrug resistance; SDZ PSC 833; Tamoxifen

Indexed keywords

CERAMIDE; CYCLOSPORIN A; DOXORUBICIN; FUMONISIN B1; TAMOXIFEN; VALSPODAR;

APOPTOSIS; ARTICLE; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER INHIBITION; CANCER RESISTANCE; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG MECHANISM; DRUG POTENTIATION; FEMALE; GLYCOSYLATION; HUMAN; HUMAN CELL; MULTIDRUG RESISTANCE; PHOSPHOLIPID BLOOD LEVEL; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC AGENTS, HORMONAL; APOPTOSIS; BREAST NEOPLASMS; CERAMIDES; CYCLOSPORINE; CYCLOSPORINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; DRUG INTERACTIONS; DRUG RESISTANCE, MULTIPLE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; TAMOXIFEN; TUMOR CELLS, CULTURED;

EID: 0033565728     PISSN: 0008543X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0142(19990715)86:2<300::AID-CNCR14>3.0.CO;2-H     Document Type: Article

References (50)

1. Kavallaris M, Kuo DY-S, Burkhart CA, Regl DL, Norris MD, Haber M. Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific β-tubulin isotypes. J Clin Invest 1997;100:1282-93.
2. Ise W, Heuser M, Sanders KH, Beck J, Gekeler V. P-glycoprotein-associated resistance to taxol and taxotere and its reversal by dexniguldipine-HCl, dexverapamil-HCl, or cyclosporin A. Int J Oncol 1996;8:951-6.
3. Fan D, Beltran PJ, O'Brian CA. Reversal of multidrug resistance. In: Kellen JA, editor. Reversal of multidrug resistance in cancer. Toronto, Canada: CRC Press, 1994:93-125.
4. Gottesman M, Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 1993;62:385-427.
5. Bradley G, Ling V. P-glycoprotein, multidrug resistance and tumor progression. Cancer Metabol Rev 1994;13:223-33.
6. Schroder CP, Godwin AK, O'Dwyer PJ, Twe KD, Hamilton TC, Ozols RF. Glutathione and drug resistance. Cancer Invest 1996;14:158-68.
7. Volm M, Kastel M, Mattern J, Efferth T. Expression of resistance factors (P-glycoprotein, glutathione S-transferase-π, and topoisomerase II) and their interrelationship to protooncogene products in renal cell carcinomas. Cancer 1993; 71:3981-7.
8. Yusa K, Tsuruo T. Reversal mechanism of multidrug resistance by verapamil: direct binding of verapamil to P-glycoprotein on specific sites and transport of verapamil outward across the plasma membrane of K562/ADM cells. Cancer Res 1989;49:5002-6.
9. Foxwell BM, Mackie A, Ling V, Ryffel B. Identification of the multidrug resistance-related P-glycoprotein as a cyclosporine binding protein. Mol Pharmacol 1989;8:985-94.
10. Callaghan R, Higgins CF. Interaction of tamoxifen with the multidrug resistance P-glycoprotein. Br J Cancer 1995;71: 294-9.
11. Archinal-Mattheis A, Rzepka RW, Watanabe T, Kokubu N, Itoh Y, Combates NJ, et al. Analysis of the interactions of SDZ PSC 833 ([3′ keto-Bmtl]-Val2]-cyclosporine, a multidrug resistance modulator, with P-glycoprotein. Oncol Res 1995;7:603-10.
12. Gaveriaux C, Boesch D, Jachez B, Bollinger P, Payne T, Loor F. SDZ PSC 833, a nonimmunosuppressive cyclosporine analog, is a very potent multidrug resistance modifier. J Cell Pharmacol 1991;2:225-34.
13. Watanabe T, Tsuge H, Oh-Hara T, Naito M, Tsuruo T. Comparative study on reversal efficacy of SDZ PSC 833, cyclosporine A and verapamil on multidrug resistance in vitro and in vivo. Acta Oncol 1995;34:235-41.
14. Lavie Y, Cao H-T, Bursten SL, Giuliano AE, Cabot MC. Accumulation of glucosylceramides in multidrug-resistant cancer cells. J Biol Chem 1996;271:19530-6.
15. Lavie Y, Cao H-T, Volner A, Lucci A, Han TY, Geffen V, et al. Agents that reverse multidrug resistance, tamoxifen, verapamil, and cyclosporin A, block glycosphingolipid metabolism by inhibiting ceramide glycosylation in human cancer cells. J Biol Chem 1997;272:1682-7.
16. Marsh NL, Elias PM, Holleran WM. Glucosylceramides stimulate murine epidermal hyperproliferation. J Clin Invest 1995;95:2903-9.
17. Shayman JA, Deshmukh GD, Mahdiyoun S, Thomas TP, Wu D, Barcelon FS, et al. Modulation of renal epithelial cell growth by glucosylceramide. J Biol Chem 1991;266:22968-74.
18. Rani CSS, Abe A, Chang Y, Rosenzweig N, Saltiel AR, Radin NS, et al. Cell cycle arrest induced by an inhibitor of glucosylceramide synthase. J Biol Chem 1995;270:2859-67.
19. Smyth MJ, Obeid LM, Hannun YA. Ceramide: a novel lipid mediator of apoptosis. Adv Pharmacol 1997;41:133-54.
20. Liu Y-Y, Han T-Y, Giuliano AE, Cabot MC. Expression of glucosylceramide synthase, converting ceramide to glucosylceramide, confers adriamycin resistance in human breast cancer cells. J Biol Chem 1999;274(21):1140-6.
21. Lutzker SG, Levine A J. Apoptosis and cancer chemotherapy. Cancer Treat Res 1996;87:345-6.
22. Bligh EG, Dyer WT. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959;37:911-7.
23. Cabot MC, Giuliano AE, Volner A, Han T-Y. Tamoxifen retards glycosphingolipid metabolism in human cancer cells. FEBS Lett 1996;394:129-31.
24. Hannun YA, Obeid LM. Ceramide: an intracellular signal for apoptosis. Trends Biochem Sci 1995;20:73-7.
25. Wiesner DA, Kilkus JP, Gottschalk AR, Quintans J, Dawson G. Anti-immunoglobulin-induced apoptosis in WEHI 231 cells involves the slow formation of ceramide from sphingomyelin and is blocked by bcl-XL. J Biol Chem 1997;272: 9868-76.
26. Jaffrezou J-P, Herbert J-M, Levade T, Gau M-N, Chatelain P, Laurent G. Reversal of multidrug resistance by calcium channel blocker SR33557 without photoaffinity labeling of P-glycoprotein. J Biol Chem 1991;266:19858-64.
27. Ramu A, Glaubiger D, Fuks Z. Reversal of acquired resistance to doxorubicin in P388 murine leukemia cells by tamoxifen and other triparanol analogues. Cancer Res 1984; 44:4392-5.
28. DeGregorio MW, Ford JM, Benz CC, Wiebe VJ. Toremifene: pharmacologic and pharmacokinetic basis of reversing multidrug resistance. J Clin Oncol 1989;7:1359-64.
29. Ford JM, Prozialeck WC, Hait WN. Structural features determining activity of phenothiazines and related drugs for inhibition of cell growth and reversal of multidrug resistance. Mol Pharmacol 1989;35:105-15.
30. Solary E, Velay I, Chauffert B, Caillot D, Bidan JM, Dumas M, et al. Sufficient levels of quinine in the serum circumvent the multidrug resistance of the human leukemic cell line K562/ADM. Cancer 1991;68:1714.
31. Van der Graaf WTA, Mulder NH, Timmer-Bosscha H, Meijer C, Meersma GJ, De Vries EG. Different effects of amiodarone, cyclosporin A, and PSC 833 on mitoxantrone sensitivity in human tumor cell lines with various resistance mechanisms. Proc Am Assoc Cancer Res 1993;34:A1899.
32. Slater LM, Sweet P, Stupecky M, Gupta S. Cyclosporine A reverses vincristine and daunorubicin resistance in acute lymphatic leukemia in vitro. J Clin Invest 1986;77:1405-8.
33. Hyafil F, Vergely C, Duvignaud P, Grandperret T. In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxamide derivative. Cancer Res 1993;53:4595-602.
34. Germann U, Shlyakhter D, Mason V, Zelle R, Duffy J, Galullo V, et al. Cellular and biochemical characterization of VX-710 as a chemosensitizer: reversal of P-glycoprotein-mediated multidrug resistance in vitro. Anticancer Drugs 1997;8:125-40.
35. Bose R, Verheij M, Haimovitz-Friedman A, Scotto K, Fuks Z, Kolesnick R. Ceramide synthase mediates daunorubicin-induced apoptosis: an alternative mechanism for generating death signals. Cell 1995;82:405-14.
36. Haimovitz-Friedman A, Kan CC, Ehleiter D, Persaud RS, McLoughlin M, Fuks Z, et al. Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J Exp Med 1994;180:525-35.
37. Cifone MG, DeMaria R, Roncaioli P, Rippo MR, Axuma M, Lanier LL, et al. Apoptotic signaling through CD95 Fas/ Apo-1 activates an acidic sphingomyelinase. J Exp Med 1994; 177:1547-52.
38. Jarvis WD, Kolesnick RN, Fornari FA, Traylor RS, Gewirtz DA, Grant S. Induction of apoptotic DNA damage and cell death by activation of the sphingomyelin pathway. Proc Natl Acad Sci USA 1994;91:73-7.
39. Jaffrezou JP, Levade T, Bettaieb A, Andrieu N, Bezombes C, Maestre N, et al. Daunorbicin-induced apoptosis: triggering of ceramide generation through sphingomyelin hydrolysis. EMBO J 1996;125:2417-24.
40. van Helvoort A, Smith A, Sprong H, Fritzsche I, Schinkel A, Borst P, et al. MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell 1996;87:507-17.
41. Cabot MC, Han TY, Giuliano A. The multidrug resistance modulator SDZ PSC 833 is a potent activator of cellular ceramide formation. FEBS Lett 1998;431:185-8.
42. 6-NBD-sphingomyelin is translocated across the plasma memebrane by a multidrug transporter activity. J Cell Sci 1997;110:75-83.
43. Twentyman PR, Bleehen NM. Resistance modification by PSC 833, a novel nonimmunosupportive cyclosporine A. Eur J Cancer 1991;27:1639-42.
44. Slater LM, Sweet P, Stupecky M, Osann K. Superiority of cyclosporin A over PSC-833 in enhancement of VP-16 efficacy in murine tumors in vivo. Cancer Chemother Pharmacol 1997;39:452-4.
45. Sonneveld P, Marie J-P, Huisman C, Vekhoff A, Schoester M, Faussat AM, et al. Reversal of multidrug resistance by SDZ PSC 833, combined with VAD (vincristine, doxorubicin, dexamethasone) in refractory multiple myeloma. A Phase I study. Leukemia 1996;10:1741-50.
46. Raderer M, Scheithauer W. Clinical trials of agents that reverse multidrug resistance. A literature review. Cancer 1993;72:3553-63.
47. DelPrete SA, Maurer LH, O'Donnel J, Forcier JR, LeMarbre P. Combination chemotherapy with cisplatin, carmustine, dacarbazine and tamoxifen in metastatic melanoma. Cancer Treat Rep 1984;68:1403-5.
48. Gelmann EP. Tamoxifen for the treatment of malignancies other than breast and endometrial carcinoma. Semin Oncol 1997;24:S1-65,170.
49. Couldwell WT, Weiss MH, DeGiorgio CM, Weiner LP, Hinton DR, Ehresmann GR, et al. Clinical and radiographic response in a minority of patients with recurrent malignant gliomas treated with high-dose tamoxifen. Neurosurgery 1993;32:485-9.
50. Lucci A, Cho WI, Han T-Y, Volner A, Giuliano AE, Morton DL, et al. Glucosylceramide: a marker for multiple drug resistant cancers. Anticancer Res 1998;18:475-80.