Chemoprotection of hematopoietic cells by a mutant P-glycoprotein resistant to a potent chemosensitizer of multidrug-resistant cancers

Human Gene Therapy

Volumn 11, Issue 4, 2000, Pages 555-565

  Hafkemeyer, Peter ^a,b   Licht, Thomas ^a,c   Pastan, Ira ^a   Gottesman, Michael M ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DAUNORUBICIN; FLUPENTIXOL; GLYCOPROTEIN P; VINBLASTINE; VIRUS VECTOR;

ARTICLE; BONE MARROW; CANCER; CANCER THERAPY; CELL SURVIVAL; COLONY FORMATION; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG SENSITIVITY; GENE EXPRESSION; GENE TRANSFER; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; LEUKOPENIA; MULTIDRUG RESISTANCE; RETROVIRUS;

MURINAE; UNIDENTIFIED RETROVIRUS;

EID: 0034096096     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/10430340050015743     Document Type: Article

References (54)

1. Akiyama, S., Fojo, A., Hanover, J.A., Pastan, I., and Gottesman, M.M. (1985). Isolation and genetic characterization of human KB cell lines resistant to multiple drugs. Somat. Cell. Mol. Genet. 11, 117-126.
2. Ambudkar, S.V., Dey, S., Hrycyna, C.A., Ramachandra, M., Pastan, I., and Gottesman, M.M. (1999). Biochemical, cellular and pharmacological aspects of the multidrug transporter. Annu. Rev. Pharmacol. Toxicol. 39, 361-397.
3. Baldini, N., Scotlandi, K., Barbanti-Brúdano, G., Manara, M.C., Maurici, D., Bacci, G., Bertoni, F., Picci, P., Sottili, S., Campanacci, M., and Serra, M. (1995). Expression of P-glycoprotein in high-grade osteosarcomas in relation to clinical outcome. N. Engl. J. Med. 333, 1380-1385.
4. Banerjee, D., Zhao, S.C., Li, M.X., Schweitzer, B.I., Mineishi, S., and Bertino, J.R. (1994). Gene therapy utilizing drug resistance genes: A review. Stem Cells 12, 378-385.
5. Bodine, D.M., Seidel, N.E., Gale, M.S., Nienhuis, A.W., and Orlic, D. (1994). Efficient retrovirus transduction of mouse pluripotent hematopoietic stem cells mobilized into the peripheral blood by treatment with granulocyte colony-stimulating factor and stem cell factor. Blood 84, 1482-1491.
6. Bunting, K.D., Galipeau, J., Topham, D., Benaim, E., and Sorrentino, B.P. (1998). Transduction of murine bone marrow cells with an MDR1 vector enables ex vivo stem cell expansion, but these expanded grafts cause a myeloproliferative syndrome in transplanted mice. Blood 92, 2269-2279.
7. Cardarelli, C.O., Aksentijevich, I., Pastan, I., and Gottesman, M.M. (1995). Differential effects of P-glycoprotein inhibitors on NIH3T3 cells transfected with wild-type (G185) or mutant (V185) multidrug transporters. Cancer Res. 55, 1086-1091.
8. Chan, H.S.L., Thorner, P.S., Haddad, G., and Ling, V. (1990). Immunohistochemical detection of P-glycoprotein: Prognostic correlation in soft tissue sarcoma of childhood. J. Clin. Oncol. 8, 689-704.
9. Chaudhary, P.M., and Roninson, I.B. (1991). Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells. Cell 66, 85-94.
10. Chaudhary, P.M., and Roninson, I.B. (1993). Induction of multidrug resistance in human cells by transient exposure to different chemotherapeutic drugs. J. Natl. Cancer Inst. 85, 632-639.
11. Chaudhary, P.M., Mechetner, E.B., and Roninson, I.B. (1992). Expression and activity of the multidrug resistance P-glycoprotein in human peripheral blood lymphocytes. Blood 80, 2729-2934.
12. Chin, K.-V., Chauhan, S., Pastan, I., and Gottesman, M.M. (1990). Regulation of mdr RNA levels in response to cytotoxic drugs in rodent cells. Cell Growth Differ. 1, 361-365.
13. Cowan, K.H., Moscow, J.A., Huang, H., Zujewski, J., Oíshaughnessy, J., Sorrentino, B., Hines, K., Carter, C., Schneider, E., Cusack, G., Noone, M., Dunbar, C., Steinberg, S., Wilson, W., Goldspiel, B., Read, R.J., Leitman, S., McDonagh K., Chow, C., Abati, A., Chiang, Y., Weir, S., Gottesman, M.M., Pastan, I., and Nienhuis, A. (1999). Paclitaxel chemotherapy following autologous stem cell transplantation and engraftment of hematopoietic cells transduced with a retrovirus containing the multidrug resistance cDNA (MDR1) in cancer patients. Clin. Cancer Res. 5, 1619-1628.
14. DeLaFlor-Weiss, E., Richardson, C., Ward, M., Himelstein, A., Smith, L., Podda, S., Gottesman, M.M., Pastan, I., and Bank, A. (1992). Transfer and expression of the human multidrug resistance gene in mouse erythroleukemia cells. Blood 80, 3106-3111.
15. Dey, S., Hafkemeyer, P., Pastan, I., and Gottesman, M.M. (1999). A single amino acid residue contributes to distinct mechanisms of inhibition of the human multidrug transporter by stereoisomers of the dopamine receptor antagonist flupentixol. Biochemistry 38, 6630-6639.
16. Drach, D., Zhao, S., Drach, J., Mahadevia, R., Gattringer, C., Huber, H., and Andreeff, M. (1992). Subpopulations of normal and peripheral blood and bone marrow cells express a functional multidrug resistant phenotype. Blood 80, 2735-2739.
17. Fisher, G.A., and Sikic, B.I. (1995). Clinical studies with modulators of multidrug resistance. Hematol. Oncol. Clin. North Am. 9, 363-382.
18. Fojo, A.T., Ueda, K., Slamon, D.J., Poplack, D.G., Gottesman, M.M., and Pastan, I. (1987). Expression of a multidrug-resistance gene in human tumors and tissues. Proc. Natl. Acad. Sci. U.S.A. 84, 265-269.
19. Ford, J.M., Prozialeck, W.C., and Hait, W.N. (1988). Structural features determining activity of phenothiazines and related drugs for inhibition of cell growth and reversal of multidrug resistance. Mol. Pharmacol. 35, 105-115.
20. Ford, J.M., Bruggemann, E.P., Pastan, I., Gottesman, M.M., and Hait, W.N. (1990). Cellular and biochemical characterization of thioxanthenes for reversal of multidrug resistance in human and murine cell lines. Cancer Res. 50, 1748-1756.
21. Ford, J.M., Yang, J.M., and Hait, W.N. (1996). P-glycoprotein-mediated multidrug resistance: Experimental and clinical strategies for its reversal. Cancer Treat. Res. 87, 3-38.
22. Galski, H., Sullivan, M., Willingham, M.C., Chin, K.-V., Gottesman, M.M., Pastan, I., and Merlino, G.T. (1989). Expression of a human multidrug resistance cDNA (MDR1) in the bone marrow of transgenic mice: Resistance to daunomycin induced leukopenia. Mol. Cell. Biol. 9, 4357-4363.
23. Germann, U.A., Gottesman, M.M., and Pastan, I. (1989). Expression of a multidrug resistance-adenosine deaminase fusion gene. J. Biol. Chem. 264, 7418-7424.
24. Goldstein, L., Galski, H., Fojo, A., Willingham, M., Lai, S.-I., Gazdar, A., Pirker, R., Green, A., Crist, W., Brodeur, G.M., Lieber, M., Cossman, J., Gottesman, M.M., and Pastan, I. (1989). Expression of a multidrug resistance gene in human cancers. J. Natl. Cancer Inst. 81, 116-124.
25. Goldstein, L.J., Fojo, A.T., Ueda, K., Crist, W., Green, A., Brodeur, G., Pastan, I., and Gottesman, M.M. (1990). Expression of the multidrug resistance, MDR1, gene in neuroblastom as. J. Clin. Oncol. 1, 128-136.
26. Gottesman, M.M., and Pastan, I. (1991). The multidrug resistance (MDR1) gene as a selectable marker in gene therapy. In Human Gene Transfer, Vol. 219. O. Cohen-Haguenauer and M. Boiron, eds. (Coloque INSERM/John Libbey Eurotext, London) pp. 185-191.
27. Gottesman, M.M., and Pastan, I. (1993). Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62, 385-427.
28. Gottesman, M.M., Hrycyna, C.A., Schoenlein, P.V., Germann, U.A., and Pastan, I. (1995). Genetic analysis of the multidrug transporter. Annu. Rev. Genet. 29, 607-649.
29. Hafkemeyer, P., Dey, S., Ambudkar, S.V., Hrycyna, C.A., Pastan, I., and Gottesman, M.M. (1998). Contribution to substrate specificity and transport of nonconserved residues in transmembrane domain 12 of human P-glycoprotein. Biochemistry 37, 16400-16409.
30. Hanania, E.G., and Deisseroth, A.B. (1994). Serial transplantation shows that early hematopoietic precursor cells are transduced by MDR-1 retroviral vector in a mouse gene therapy model. Cancer Gene Ther. 1, 21-25.
31. Hanania, E.G., Giles, R.E., Kavanagh, J., Fu, S.Q., Ellerson, D., Zu, Z., Wang, T., Su, Y., Kudelka, A., Rahman, Z., Holmes, F., Hortobagyi, G., Claxton, D., Bachier, C., Thall, P., Cheng, S., Hester, J., Ostrove, J.M., Bird, R.E., Chang, A., Korbling, M., Seong, D., Cote, R., Holzmayer, T., Mechetner, E., Heimfeld, S., Berenson, R., Burtness, B., Edwards, C., Bast, R., Andreeff, M., Champlin, R., and Deisseroth, A.B. (1996). Results of MDR-1 vector modification trial indicate that granulocyte/macrophage colony-forming unit cells do not contribute to posttransplant hematopoietic recovery following intensive systemic therapy. Proc. Natl. Acad. Sci. U.S.A. 93, 15346-15351.
32. Hesdorffer, C., Ayello, J., Ward, M., Kaubisch, A., Vahdat, L., Balmaceda, C., Garrett, T., Fetell, M., Reiss, R., Bank, A., and Antman, K. (1998). Phase I trial of retroviral-mediated transfer of the human MDR1 gene as marrow chemo-protection in patients undergoing high-dose chemotherapy and autologous stem-cell transplantation. J. Clin. Oncol. 16, 165-172.
33. Hrycyna, C.A., Ramachandra, M., Pastan, I., and Gottesman, M.M. (1998). Functional expression of human P-glycoprotein from plasmids using vaccinia virus-bacteriophage T7 RNA polymerase system. Methods Enzymol. 292, 456-473.
34. Johnstone, E.C., Crow, T.J., Frith, C.D., Carney, M.W.P., and Price, J.S. (1978). Mechanism of the antipsychotic effect in the treatment of acute schizophrenia. Lancet 1, 848-849.
35. Kinsella, T.M., and Nolan, G.P. (1996). Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7, 1405-1413.
36. Klimecki, W.T., Futscher, B.W., Grogan, T.M., and Dalton, W.S. (1994). P-glycoprotein expression and function in circulating blood cells from normal volunteers. Blood 83, 2451-2458.
37. Licht, T., Fiebig, H.H., Bross, K.J., Herrmann, F., Berger, D.P., Shoemaker, R., and Mertelsmann, R. (1991). Induction of multiple-drug resistance during anti-neoplastic chemotherapy in vitro. Int. J. Cancer 49, 630-637.
38. Licht, T., Aksentijevich, I., Gottesman, M.M., and Pastan, I. (1995). Efficient expression of functional human MDR1 gene in murine bone marrow after retroviral transduction of purified hematopoietic stem cells. Blood 86, 111-121.
39. Licht, T., Aran, J.M., Goldenberg, S.K., Vieira, W.D., Gottesman, M.M., and Pastan, I. (1999). Retroviral transfer of human MDR1 gene to hematopoietic cells: Effects of drug selection and of transcript splicing on expression of encoded P-glycoprotein. Hum. Gene Ther. 10, 2173-2185.
40. Loo, T.W., and Clarke, D.M. (1993). Functional consequence of phenylalanine mutations in the predicted transmembrane domain of P-glycoprotein. J. Biol. Chem. 268, 19965-19972.
41. McLachlin, J.R., Eglitis, M.A., Ueda, K., Kantoff, P.W., Pastan, I., Anderson, W.F., and Gottesman, M.M. (1990). Expression of a human complementary DNA for the human multidrug resistance gene in murine hematopoietic precursor cells with the use of retroviral gene transfer. J. Natl. Cancer Inst. 82, 1260-1263.
42. Metz, M.Z., Best, D.M., and Kane, S.E. (1995). Harvey murine sarcoma virus/MDR1 retroviral vectors: Efficient virus production and foreign gene transduction using MDR1 as selectable marker. Virology 208, 634-643.
43. Mickisch, G.H., Licht, T., Merlino, G.T., Gottesman, M.M., and Pastan, I. (1991). Chemotherapy and chemosensitization of transgenic mice which express the human multidrug resistance gene in bone marrow: Efficacy, potency and toxicity. Cancer Res. 51, 5417-5424.
44. Moscow, J.A., Huang, H., Dunbar, C., Sorrentino, B., Zujewski, J., Chiang, Y., Chang, Y.N., Cullen, E., Cusack, G., Carter, C., Hines, K., Goldspiel, B., Leitman, S., Read, E.J., Abati, A., Venzon, D., Sellers, S., Gottesman, M.M., Pastan, I., Nienhuis, A., and Cowan, K.H. (1999). Reconstitution and expansion of hematopoietic cells transduced with retroviruses containing either the multidrug resistance gene (MDR1) or the neomycin resistance gene (neoR) in breast cancer patients treated with paclitaxel, doxorubicin and vinblastine. Blood 94, 52-61.
45. Neyfakh, A.A., Serpinskaya, A.S., Chervonsky, A.V., Apasov, S.G., and Kazarov, A.R. (1989). Multidrug-resistance phenotype of a subpopulation of T-lymphocytes without drug selection. Exp. Cell Res. 185, 496-505.
46. Nolan, G.P., and Shatzman, A.R. (1998). Expression vectors and delivery systems. Curr. Opin. Biotechnol. 9, 447-450.
47. Pastan, I., Gottesman, M.M., Ueda, K., Lovelace, E., Rutherford, A.V., and Willingham, M.C. (1988). A retrovirus carrying an MDR1 cDNA confers multidrug resistance and polarized expression of P-glycoprotein in MDCK cells. Proc. Natl. Acad. Sci. U.S.A. 85, 4486-4490.
48. Podda, S., Ward, M., Himelstein, A., Richardson, C., Delaflor-Weiss, E., Smith, L., Gottesman, M.M., Pastan, I., and Bank, A. (1992). Transfer and expression of the human multiple drug resistance gene into live mice. Proc. Natl. Acad. Sci. U.S.A. 89, 9676-9680.
49. Salmon, S.E., Dalton, W.S., Grogan, T.M., Plezia, P., Lehnert, M., Roe, D.J., and Miller, T.P. (1991). Multidrug-resistant myeloma: Laboratory and clinical effects of verapamil as a chemosensitizer. Blood 78, 44-50.
50. Shen, D.W., Cardarelli, C., Hwang, J., Cornwell, M., Richert, N., Ishii, S., Pastan, I., and Gottesman, M.M. (1986). Multiple drug-resistant human KB carcinoma cells independently selected for high-level resistance to colchicine, Adriamycin, or vinblastine show changes in expression of specific proteins. J. Biol. Chem. 261, 7762-7770.
51. Sonneveld, P., Durie, B.D.M., Lokhorst, H.M., Marie, J.P., Solbu, G., Suciu, S., Zittoun, R., Löwenberg, B., and Nooter, K. for the Leukemia Group of the EORTC and the Hovon. (1992). Modulation of multidrug-resistant multiple myeloma by cyclosporine. Lancet 340, 255-259.
52. Sorrentino, B.P., Brandt, S.J., Bodine, D., Gottesman, M., Pastan, I., Cline, A., and Nienhuis, A.W. (1992). Selection of drug-resistant bone marrow cells in vivo after retroviral transfer of human MDR1. Science 257, 99-103.
53. Yahanda, A.M., Adler, K.M., Fisher, G.A., Brophy, N.A., Halsey, J., Hardy, I., Gosland, M.P., Lum, B.L., and Sikic, B.I. (1992). Phase I trial of etoposide with cyclosporine as a modulator of multidrug resistance. J. Clin. Oncol. 10, 1624-1634.
54. Yuen, A.R., and Sikic, B.I. (1994). Multidrug resistance in lymphomas. J. Clin. Oncol. 12, 2453-2459.