Functional characterization of a glycine 185-to-valine substitution in human P-glycoprotein by using a vaccinia-based transient expression system

Molecular Biology of the Cell

Volumn 7, Issue 10, 1996, Pages 1485-1498

  Ramachandra, Muralidhara ^a   Ambudkar, Suresh V ^a   Gottesman, Michael M ^a   Pastan, Ira ^a   Hrycyna, Christine A ^a,b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Jane Coffin Childs Mem Fund Med R

Author keywords

[No Author keywords available]

Indexed keywords

COLCHICINE; CYCLOSPORIN A; GLYCOPROTEIN P; NICARDIPINE; RHODAMINE; TETRAPHENYLPHOSPHONIUM; VERAPAMIL; VINBLASTINE;

AMINO ACID SUBSTITUTION; ARTICLE; CANCER CELL; ENZYME ACTIVITY; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HYDROLYSIS; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; VACCINIA VIRUS;

VACCINIA; VACCINIA VIRUS;

EID: 0029797074     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.7.10.1485     Document Type: Article

References (51)

1. Al-Shawi, M.K., and Senior, A.E. (1993). Characterization of the adenosine triphosphatase activity of Chinese hamster P-glycoprotein. J. Biol. Chem. 268, 4197-4206.
2. Ambudkar, S.V. (1995). Purification and reconstitution of functional human P-glycoprotein. J. Bioenerg. Biomembr. 27, 23-29.
3. Ambudkar, S.V., Lelong, I.H., Zhang, J.P., Cardarelli, C.O., Gottesman, M.M., and Pastan, I. (1992). Partial purification and reconstitution of the human multidrug resistance pump - characterization of the drug-stimulable ATP hydrolysis. Proc. Natl. Acad. Sci. USA 89, 8472-8476.
4. Azzaria, M., Schurr, E., and Gros, P. (1989). Discrete mutations introduced in the predicted nucleotide-binding sites of the mdr1 gene abolish its ability to confer multidrug resistance. Mol. Cell. Biol. 9, 5289-5297.
5. Bailey, J.L. (1967). Techniques in Protein Chemistry, New York: Elsevier Publishing, 340-341.
6. Beck, W.T., and Cirtain, M. (1982). Continued expression of Vinca alkaloid resistance by CCRF-CEM cells after treatment with tunicamycin or pronase. Cancer Res. 42, 184-189.
7. Bruggemann, E.P., Currier, S.J., Gottesman, M.M., and Pastan, I. (1992). Characterization of the azidopine and vinblastine binding site of P-glycoprotein. J. Biol. Chem. 267, 21020-21026.
8. Bruggemann, E.P., Germann, U.A., Gottesman, M.M., and Pastan, I. (1989). Two different regions of P-glycoprotein are photoaffinity labeled by azidopine. J. Biol. Chem. 264, 15483-15488.
9. 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.
10. Chen, C.-J., Chin, J.E., Ueda, K., Clark, D.P., Pastan, I., Gottesman, M.M., and Roninson, I.B. (1986). Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 47, 381-389.
11. Choi, K., Chen, C.-J., Kriegler, M., and Roninson, I.B. (1989). An altered pattern of cross-resistance in multidrug-resistant human cells results from spontaneous mutations in the mdr1 (P-glycoprotein) gene. Cell 53, 519-529.
12. Cornwell, M.M., Tsuruo, T., Gottesman, M.M., and Pastan, I. (1987). ATP-binding properties of P-glycoprotein from multidrug-resistant KB cells. FASEB J. 1, 51-54.
13. Currier, S.J., Kane, S.E., Willingham, M.C., Cardarelli, C.O., Pastan, I., and Gottesman, M.M. (1992). Identification of residues in the first cytoplasmic loop of P-glycoprotein involved in the function of chimeric human MDR1-MDR2 transporters. J. Biol. Chem. 267, 25153-25159.
14. Doige, C.A., Yu, X.H., and Sharom, F.J. (1992). ATPase activity of partially purified P-glycoprotein from multidrug-resistant Chinese hamster ovary cells. Biochim. Biophys. Acta 1109, 149-160.
15. Earl, P.E., Cooper, N., and Moss, B. (1991). Propagation of cell cultures and vaccinia virus stocks. In: Current Protocols in Molecular Biology, ed. F.M. Ausubel, R. Brent, R.E. Kinston, D.D. Moore, J.A. Smith, J.C. Seidman, and K. Struhl, New York: John Wiley and Sons, 16.16.1-16.16.7.
16. Elroy-Stein, O., Fuerst, T.R., and Moss, B. (1989). Cap-independent translation of mRNA conferred by encephalomyocarditis virus 5′ sequence improves the performance of the vaccinia virus/bacteriophage T7 hybrid expression system. Proc. Natl. Acad. Sci. USA 86, 6126-6130.
17. Elroy-Stein, O., and Moss, B. (1991). Gene expression using the vaccinia virus/T7 RNA polymerase hybrid system. In: Current Protocols in Molecular Biology, ed. F.M. Ausubel, R. Brent, R.E. Kinston, D.D. Moore, J.A. Smith, J.C. Seidman, and K. Struhl, New York: John Wiley and Sons, 16.19.1-16.19.9.
18. Evans, G.L., Ni, B., Hrycyna, C.A., Chen, D., Ambudkar, S.V., Pastan, I., Germann, U.A., and Gottesman, M.M. (1995). Heterologous expression systems for P-glycoprotein: E. coli, yeast, and baculovirus. J. Bioenerg. Biomembr. 27, 43-52.
19. Fuerst, T.R., Niles, E.G., Studier, F.W., and Moss, B. (1986). Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83, 8122-8126.
20. Georges, E., Bradley, G., Gariepy, J., and Ling, V. (1990). Detection of P-glycoprotein isoforms by gene-specific monoclonal antibodies. Proc. Natl. Acad. Sci. USA 87, 152-156.
21. Germann, U.A., Chambers, T.C., Ambudkar, S.V., Licht, T., Cardarelli, C.O., Pastan, I., and Gottesman, M.M. (1996). Characterization of phosphorylation-defective mutants of human P-glycoprotein expressed in mammalian cells. J. Biol. Chem. 271, 1708-1716.
22. Germann, U.A., Willingham, M.C., Pastan, I., and Gottesman, M.M. (1990). Expression of the human multidrug transporter in insect cells by a recombinant baculovirus. Biochemistry 29, 2295-2303.
23. 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.
24. Gottesman, M.M., and Pastan, I. (1993). Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62, 385-427.
25. Hamada, H., and Tsuruo, T. (1986). Functional role for the 170- to 180-kDa glycoprotein specific to drug-resistant tumor cells as revealed by monoclonal antibodies. Proc. Natl. Acad. Sci. USA 83, 7785-7789.
26. Hardy, S.P., Goodfellow, H.R., Valverde, M.A., Gill, D.R., Sepúlveda, V., and Higgins, C.F. (1995). Protein kinase C-mediated phosphorylation of the human multidrug resistance P-glycoprotein regulates cell volume-activated chloride channels. EMBO J. 14, 68-75.
27. Higgins, C.F. (1992). ABC transporters - from microorganisms to man. Annu. Rev. Cell Biol. 8, 67-113.
28. Horio, M., Gottesman, M.M., and Pastan, I. (1988). ATP-dependent transport of vinblastine in vesicles from human multidrug-resistant cells. Proc. Natl. Acad. Sci. USA 85, 3580-3584.
29. Hrycyna, C.H., Zhang, S., Ramachandra, M., Ni, B., Pastan, I., and Gottesman, M. (1996). Functional and molecular characterization of the human multidrug transporter. In: Multidrug Resistance in Cancer Cells: Cellular, Biochemical, Molecular, and Biological Aspects, ed. S. Gupta and T. Tsuruo, New York: John Wiley and Sons, 29-37.
30. 185 with an altered pattern of multidrug resistance. Biochem. Biophys. Res. Commun. 162, 224-231.
31. Kuchler, K., and Thorner, J. (1992). Functional expression of human mdr1 in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 89, 2302-2306.
32. Ling, V., Kartner, N., Sudo, T., Siminovitch, L., and Riordan, J.R. (1983). The multidrug resistance phenotype in Chinese hamster ovary cells. Cancer Treat. Rep. 67, 869-874.
33. Loo, T.W., and Clarke, D.M. (1994). Reconstitution of drug-stimulated ATPase activity following co-expression of each half of human P-glycoprotein as separate polypeptides. J. Biol. Chem. 269, 7750-7755.
34. Loo, T.W., and Clarke, D.M. (1995). Rapid purification of human P-glycoprotein mutants expressed transiently in HEK 293 cells by nickel-chela te chromatography and characterization of their drug-stimulated ATPase activities. J. Biol. Chem. 270, 21449-21452.
35. McGrath, J.P., and Varshavsky, A. (1989). The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature 340, 400-404.
36. Miller, L.K. (1993). Baculoviruses: high-level expression in insect cells. Curr. Opin. Genet. Dev. 3, 97-101.
37. Moss, B. (1991). Vaccinia virus: a tool for research and vaccine development. Science 252, 1662-1667.
38. 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. USA 85, 4486-4490.
39. Rao, U.S. (1995). Mutation of glycine 185 to valine alters the ATPase function of the human P-glycoprotein expressed in Sf9 cells. J. Biol. Chem. 270, 6686-6690.
40. Riordan, J.R., et al. (1989). Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245, 1066-1073.
41. Safa, A.R., Stern, R.K., Choi, K., Agresti, M., Tamai, I., Mehta, N.D., and Roninson, I.B. (1990). Molecular basis of preferential resistance to colchicine in multidrug-resistant human cells conferred by gly to val 185 substitution in P-glycoprotein. Proc. Natl. Acad. Sci. USA 87, 7225-7229.
42. Sarkadi, B., Muller, M., Homolya, L., Hollo, Z., Seprodi, J., Germann, U.A., Gottesman, M.M., Price, E.M., and Boucher, R.C. (1994). Interaction of bioactive hydrophobic peptides with the human multidrug transporter. FASEB J. 8, 766-770.
43. Sarkadi, B., Price, E.M., Boucher, R.C., Germann, U.A., and Scarborough, G.A. (1992). Expression of the human multidrug resistance cDNA in insect cells generates a high activity drug-stimulated membrane ATPase. J. Biol. Chem. 267, 4854-4858.
44. Schinkel, A.H., Kemp, S., Dolle, M., Rudenko, G., and Wagenaar, E. (1993). N-Glycosylation and deletion mutants of the human MDR1 P-glycoprotein. J. Biol. Chem. 268, 7474-7481.
45. Shapiro, A.B., and Ling, V. (1994). ATPase activity of purified and reconstituted P-glycoprotein from Chinese hamster ovary cells. J. Biol. Chem. 269, 3745-3754.
46. Shapiro, A.B., and Ling, V. (1995). Reconstitution of drug transport by purified P-glycoprotein. J. Biol. Chem. 270, 16167-16175.
47. Sharom, F.J., Yu, X., and Doige, C.A. (1993). Functional reconstitution of drug transport and ATPase activity in proteoliposomes containing partially purified P-glycoprotein. J. Biol. Chem. 268, 24197-24202.
48. Stein, W.D., Cardarelli, C.O., Pastan, I., and Gottesman, M.M. (1994). Kinetic evidence suggesting that the multidrug transporter differentially handles influx and efflux of its substrates. Mol. Pharmacol. 45, 763-772.
49. Ueda, K., Cardarelli, C., Gottesman, M.M., and Pastan, I. (1987). Expression of a full-length cDNA for the human MDR1 (P-glycoprotein) gene confers multidrug resistance to colchicine, doxorubicin, and vinblastine. Proc. Natl. Acad. Sci. USA 84, 3004-3008.
50. Valverde, M.A., Diáz, M., Sepúlveda, F.V., Gill, D.R., Hyde, S.C., and Higgins, C.F. (1992). Volume-regulated chloride channels associated with the human multidrug resistance P-glycoprotein. Nature 355, 830-833.
51. Zhang, L., Sachs, C.W., Fu, H.W., Fine, R.L., and Casey, P.J. (1995). Characterization of prenylcysteines that interact with P-glycoprotein and inhibit drug transport in tumor cells. J. Biol. Chem. 270, 22859-22865.