Molecular dissection of the human multidrug resistance P-glycoprotein

Biochemistry and Cell Biology

Volumn 77, Issue 1, 1999, Pages 11-23

  Loo, Tip W ^a   Clarke, David M ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

ABC transporters; ATPase activity; Dibromobimane; Disulfide crosslinking; Drug transport; Metal chelate chromatography; Mutagenesis; P glycoprotein

Indexed keywords

GLYCOPROTEIN P; PROTEINASE INHIBITOR; ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; AMINO ACID; ANTINEOPLASTIC AGENT; COMPLEMENTARY DNA; TRYPSIN;

CANCER CHEMOTHERAPY; DRUG TRANSPORT; MULTIDRUG RESISTANCE; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; ACQUIRED IMMUNE DEFICIENCY SYNDROME; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; BIOLOGICAL MODEL; CELL DEATH; CELL SURVIVAL; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MOUSE; MUTAGENESIS; NEOPLASM; PHYSIOLOGY; STRUCTURE ACTIVITY RELATION;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BINDING SITES; CELL DEATH; CELL SURVIVAL; CLONING, MOLECULAR; DNA, COMPLEMENTARY; DRUG RESISTANCE, MULTIPLE; HIV PROTEASE INHIBITORS; HUMANS; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS; NEOPLASMS; P-GLYCOPROTEIN; PROTEIN FOLDING; STRUCTURE-ACTIVITY RELATIONSHIP; TRYPSIN;

EID: 0032601621     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o99-014     Document Type: Review

References (102)

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. al-Shawi, M. K., Urbatsch, I. L., and Senior, A. E. 1994. Covalent inhibitors of P-glycoprotein ATPase activity. J. Biol. Chem. 269: 8986-8992.
3. Ambudkar, S. V., Lelong, I. H., Zhang, J., Cardarelli, C. O., Gottesman, M. M., and Pastan, I. 1992. Partial purification and reconstitution of the human multidrug-resistance pump: characterization of the drug-stimulatable ATP hydrolysis. Proc. Natl. Acad. Sci. U.S.A. 89: 8472-8476.
4. Ambudkar, S. V., Cardarelli, C. O., Pashinsky, I., and Stein, W. D. 1997. Relation between the turnover number for vinblastine transport and for vinblastine-stimulated ATP hydrolysis by human P-glycoprotein. J. Biol. Chem. 272: 21 160-21 166.
5. 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.
6. Baas, F., and Borst, P. 1988. The tissue dependent expression of hamster P-glycoprotein genes. FEBS Lett. 229: 329-332.
7. Bell, D. R., Trent, J. M., Willard, H. F., Riordan, J. R., and Ling, V. 1987. Chromosomal location of human P-glycoprotein gene sequences. Cancer Genet. Cytogenet. 25: 141-148.
8. Biedler, J. L., and Riehm, H. 1970. Cellular resistance to actinomycin D in Chinese hamster cells in vitro: cross-resistance, radioautographic, and cytogenetic studies. Cancer Res. 30: 1174-1184.
9. Boesch, D., Muller, K., Pourtier-Manzanedo, A., and Loor, F. 1991. Restoration of daunomycin retention in multidrug-resistant P388 cells by submicromolar concentrations of SDZ PSC 833, a nonimmunosuppressive cyclosporin derivative. Exp. Cell Res. 196: 26-32.
10. Brandl, C. J., and Deber, C. M. 1986. Hypothesis about the function of membrane-buried proline residues in transport proteins. Proc. Natl. Acad. Sci. U.S.A. 83: 917-921.
11. Bruggemann, E. P., Germann, U. A., Gottesman, M. M., and Pastan, I. 1989. Two different regions of P-glycoprotein [corrected] are photoaffinity-labeled by azidopine [published erratum appears in J. Biol. Chem. 1990, 265(7): 4172]. J. Biol. Chem. 264: 15 483-15 488.
12. 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: 21 020-21 026.
13. Chan, H. S., DeBoer, G., Haddad, G., Gallie, B. L., and Ling, V. 1995. Multidrug resistance in pediatric malignancies. Hematol. Oncol. Clin. North Am. 9: 275-318.
14. Chan, H. S., Grogan, T. M., DeBoer, G., Haddad, G., Gallie, B. L., and Ling, V. 1996. Diagnosis and reversal of multidrug resistance in paediatric cancers. Eur. J. Cancer, 6: 1051-1061.
15. Charuk, J. H., and Reithmeier, R. A. 1992. Interaction of P-glycoprotein with a hydrophobic component of rat urine. Biochem. Biophys. Res. Commun. 186: 796-802.
16. Charuk, J. H., Loo, T. W., Clarke, D. M., and Reithmeier, R. A. 1994. Interaction of rat kidney P-glycoprotein with a urinary component and various drugs including cyclosporin A. Am. J. Physiol. 266: F66-F75.
17. Charuk, J. H., Grey, A. A., and Reithmeier, R. A. 1998. Identification of the synthetic surfactant nonylphenol ethoxylate: a P-glycoprotein substrate in human urine. Am. J. Physiol. 274: F1127-F1139.
18. 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.
19. Chen, C. J., Clark, D., Ueda, K., Pastan, I., Gottesman, M. M., and Roninson, I. B. 1990. Genomic organization of the human multidrug resistance (MDR1) gene and origin of P-glycoproteins. J. Biol. Chem. 265: 506-514.
20. Choi, K. H., Chen, C. J., Kriegler, M., and Roninson, I. B. 1988. 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.
21. Cordon-Cardo, C., O'Brien, J. P., Casals, D., Rittman-Grauer, L., Biedler, J. L., Melamed, M. R., and Bertino, J. R. 1989. Multidrug-resistance gene (P-glycoprotein) is expressed by endothelial cells at blood-brain barrier sites. Proc. Natl. Acad. Sci. U.S.A. 86: 695-698.
22. Croop, J. M., Raymond, M., Haber, D., Devault, A., Arceci, R. J., Gros, P., and Housman, D. E. 1989. The three mouse multidrug resistance (mdr) genes are expressed in a tissue-specific manner in normal mouse tissues. Mol. Cell Biol. 9: 1346-1350.
23. de Bruijn, M. H., Van der Bliek, A. M., Biedler, J. L., and Borst, P. 1986. Differential amplification and disproportionate expression of five genes in three multidrug-resistant Chinese hamster lung cell lines. Mol. Cell Biol. 6: 4717-4722.
24. Dong, Y., Chen, G., Duran, G. E., Kouyama, K., Chao, A. C., Sikic, B. I., Gollapudi, S. V., Gupta, S., and Gardner, P. 1994. Volume-activated chloride current is not related to P-glycoprotein overexpression. Cancer Res. 54: 5029-5032.
25. Fisher, G. A., Lum, B. L., Hausdorff, J., and Sikic, B. I. 1996. Pharmacological considerations in the modulation of multidrug resistance. Eur. J. Cancer, 6: 1082-1088.
26. Fojo, A. T., Shen, D. W., Mickley, L. A., Pastan, I., and Gottesman, M. M. 1987. Intrinsic drug resistance in human kidney cancer is associated with expression of a human multidrug-resistance gene. J. Clin. Oncol. 5: 1922-1927.
27. Gerlach, J. H., Endicott, J. A., Juranka, P. F., Henderson, G., Sarangi, F., Deuchars, K. L., and Ling, V. 1986. Homology between P-glycoprotein and a bacterial haemolysin transport protein suggests a model for multidrug resistance. Nature (London), 324: 485-489.
28. Gill, D. R., Hyde, S. C., Higgins, C. F., Valverde, M. A., Mintenig, G. M., and Sepulveda, F. V. 1992. Separation of drug transport and chloride channel functions of the human multidrug resistance P-glycoprotein. Cell, 71: 23-32.
29. Goldstein, L. J. 1996. MDR1 gene expression in solid tumours. Eur. J. Cancer, 6: 1039-1050.
30. Gottesman, M. M., Pastan, I., and Ambudkar, S. V. 1996. P-glycoprotein and multidrug resistance. Curr. Opin. Genet. Dev. 6: 610-617.
31. Greenberger, L. M. 1993. Major photoaffinity drug labeling sites for iodoaryl azidoprazosin in P-glycoprotein are within, or immediately C-terminal to, transmembrane domains 6 and 12. J. Biol. Chem. 268: 11 417-11 425.
32. Greenberger, L. M., Yang, C. P., Gindin, E., and Horwitz, S. B. 1990. Photoaffinity probes for the alpha 1-adrenergic receptor and the calcium channel bind to a common domain in P-glycoprotein. J. Biol. Chem. 265: 4394-4401.
33. Gros, P., Ben Neriah, Y. B., Croop, J. M., and Housman, D. E. 1986a. Isolation and expression of a complementary DNA that confers multidrug resistance. Nature (London), 323: 728-731.
34. Gros, P., Croop, J., and Housman, D. 1986b. Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell, 47: 371-380.
35. Gruber, A., Peterson, C., and Reizenstein, P. 1988. D-verapamil and L-verapamil are equally effective in increasing vincristine accumulation in leukemic cells in vitro. Int. J. Cancer, 41: 224-226.
36. Higgins, C. F. 1995. The ABC of channel regulation. Cell, 82: 693-696.
37. Hollstein, M., Sidransky, D., Vogelstein, B., and Harris, C. C. 1991. p53 mutations in human cancers. Science (Washington, D.C.), 253: 49-53.
38. Homolya, L., Hollo, Z., Germann, U. A., Pastan, I., Gottesman, M. M., and Sarkadi, B. 1993. Fluorescent cellular indicators are extruded by the multidrug resistance protein. J. Biol. Chem. 268: 21 493-21 496.
39. Juliano, R. L., and Ling, V. 1976. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta, 455: 152-162.
40. Kast, C., Canfield, V., Levenson, R., and Gros, P. 1995. Membrane topology of P-glycoprotein as determined by epitope insertion: transmembrane organization of the N-terminal domain of mdr3. Biochemistry, 34: 4402-4411.
41. Kast, C., Canfield, V., Levenson, R., and Gros, P. 1996. Transmembrane organization of mouse P-glycoprotein determined by epitope insertion and immunofluorescence. J. Biol. Chem. 271: 9240-9248.
42. Kim, R. B., Fromm, M. F., Wandel, C., Leake, B., Wood, A. J., Roden, D. M., and Wilkinson, G. R. 1998. The drug transporter P-glycoprotein limits oral absorption and brain entry of HIV-1 protease inhibitors. J. Clin. Invest. 101: 289-294.
43. Lee, C. G., and Gottesman, M. M. 1998. HIV-1 protease inhibitors and the MDR1 multidrug transporter [editorial]. J. Clin. Invest. 101: 287-288.
44. Lee, C. G., Gottesman, M. M., Cardarelli, C. O., Ramachandra, M., Jeang, K. T., Ambudkar, S. V., Pastan, I., and Dey, S. 1998. HIV-1 protease inhibitors are substrates for the MDR1 multidrug transporter. Biochemistry, 37: 3594-3601.
45. Lehnert, M. 1996. Clinical multidrug resistance in cancer: a multifactorial problem. Eur. J. Cancer, 6: 912-920.
46. Leighton, J., Jr., and Goldstein, L. J. 1995. P-glycoprotein in adult solid tumors. Expression and prognostic significance. Hematol. Oncol. Clin. North Am. 9: 251-273.
47. Levine, A. J., Momand, J., and Finlay, C. A. 1991. The p53 tumour suppressor gene. Nature (London), 351: 453-456.
48. Liu, R., and Sharom, F. J. 1998. Proximity of the nucleotide binding domains of the P-glycoprotein multidrug transporter to the membrane surface: a resonance energy transfer study. Biochemistry, 37: 6503-6512.
49. Loo, T. W., and Clarke, D. M. 1993a. Functional consequences of phenylalanine mutations in the predicted transmembrane domain of P-glycoprotein. J. Biol. Chem. 268: 19 965-19 972.
50. Loo, T. W., and Clarke, D. M. 1993b. Functional consequences of proline mutations in the predicted transmembrane domain of P-glycoprotein. J. Biol. Chem. 268: 3143-3149.
51. Loo, T. W., and Clarke, D. M. 1994a. Functional consequences of glycine mutations in the predicted cytoplasmic loops of P-glycoprotein. J. Biol. Chem. 269: 7243-7248.
52. Loo, T. W., and Clarke, D. M. 1994b. Prolonged association of temperature-sensitive mutants of human P-glycoprotein with calnexin during biogenesis. J. Biol. Chem. 269: 28 683-28 689.
53. Loo, T. W., and Clarke, D. M. 1994c. 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.
54. Loo, T. W., and Clarke, D. M. 1995a. Covalent modification of human P-glycoprotein mutants containing a single cysteine in either nucleotide-binding fold abolishes drug-stimulated ATPase activity. J. Biol. Chem. 270: 22 957-22 961.
55. Loo, T. W., and Clarke, D. M. 1995b. Membrane topology of a cysteine-less mutant of human P-glycoprotein. J. Biol. Chem. 270: 843-848.
56. Loo, T. W., and Clarke, D. M. 1995c. P-glycoprotein. Associations between domains and between domains and molecular chaperones. J. Biol. Chem. 270: 21 839-21 844.
57. Loo, T. W., and Clarke, D. M. 1995d. Rapid purification of human P-glycoprotein mutants expressed transiently in HEK 293 cells by nickel-chelate chromatography and characterization of their drug-stimulated ATPase activities. J. Biol. Chem. 270: 21 449-21 452.
58. Loo, T. W., and Clarke, D. M. 1996a. Inhibition of oxidative cross-linking between engineered cysteine residues at positions 332 in predicted transmembrane segments (TM) 6 and 975 in predicted TM12 of human P-glycoprotein by drug substrates. J. Biol. Chem. 271: 27 482-27 487.
59. Loo, T. W., and Clarke, D. M. 1996b. The minimum functional unit of human P-glycoprotein appears to be a monomer. J. Biol. Chem. 271: 27 488-27 492.
60. Loo, T. W., and Clarke, D. M. 1996c. Mutational analysis of the predicted first transmembrane segment of each homologous half of human P-glycoprotein suggests that they are symmetrically arranged in the membrane. J. Biol. Chem. 271: 15 414-15 419.
61. Loo, T. W., and Clarke, D. M. 1997a. Correction of defective protein kinesis of human P-glycoprotein mutants by substrates and modulators. J. Biol. Chem. 272: 709-712.
62. Loo, T. W., and Clarke, D. M. 1997b. Drug-stimulated ATPase activity of human P-glycoprotein requires movement between transmembrane segments 6 and 12. J. Biol. Chem. 272: 20 986-20 989.
63. Loo, T. W., and Clarke, D. M. 1997c. Identification of residues in the drug-binding site of human P- glycoprotein using a thiol-reactive substrate. J. Biol. Chem. 272: 31 945-31 948.
64. Marie, J. P. 1995. P-glycoprotein in adult hematologic malignancies. Hematol. Oncol. Clin. North Am. 9: 239-249.
65. Morin, X. K., Bond, T. D., Loo, T. W., Clarke, D. M., and Bear, C. E. 1995. Failure of P-glycoprotein (MDR1) expressed in Xenopus oocytes to produce swelling-activated chloride channel activity. J. Physiol. 486: 707-714.
66. Morris, D. I., Greenberger, L. M., Bruggemann, E. P., Cardarelli, C., Gottesman, M. M., Pastan, I., and Seamon, K. B. 1994. Localization of the forskolin labeling sites to both halves of Pglycoprotein: similarity of the sites labeled by forskolin and prazosin. Mol. Pharmacol. 46: 329-337.
67. Ng, W. F., Sarangi, F., Zastawny, R. L., Veinot-Drebot, L., and Ling, V. 1989. Identification of members of the P-glycoprotein multigene family. Mol. Cell Biol. 9: 1224-1232.
68. Poruchynsky, M. S., and Ling, V. 1994. Detection of oligomeric and monomeric forms of P-glycoprotein in multidrug resistant cells. Biochemistry, 33: 4163-4174.
69. Rasola, A., Galietta, L. J., Gruenert, D. C., and Romeo, G. 1994. Volume-sensitive chloride currents in four epithelial cell lines are not directly correlated to the expression of the MDR-1 gene. J. Biol. Chem. 269: 1432-1436.
70. Raviv, Y., Pollard, H. B., Bruggemann, E. P., Pastan, I., and Gottesman, M. M. 1990. Photosensitized labeling of a functional multidrug transporter in living drug-resistant tumor cells. J. Biol. Chem. 265: 3975-3980.
71. Raymond, M., Rose, E., Housman, D. E., and Gros, P. 1990. Physical mapping, amplification, and overexpression of the mouse mdr gene family in multidrug-resistant cells. Mol. Cell Biol. 10: 1642-1651.
72. Riordan, J. R., and Ling, V. 1985. Genetic and biochemical characterization of multidrug resistance. Pharmacol. Ther. 28: 51-75.
73. Roepe, P. D. 1995. The role of the MDR protein in altered drug translocation across tumor cell membranes. Biochim. Biophys. Acta, 1241: 385-405.
74. Roepe, P. D., Wei, L. Y., Hoffman, M. M., and Fritz, F. 1996. Altered drug translocation mediated by the MDR protein: direct, indirect, or both? J. Bioenerg. Biomembr. 28: 541-555.
75. Rosenberg, M. F., Callaghan, R., Ford, R. C., and Higgins, C. F. 1997. Structure of the multidrug resistance P-glycoprotein to 2.5 nm resolution determined by electron microscopy and image analysis. J. Biol. Chem. 272: 10 685-10 694.
76. Ruetz, S., and Gros, P. 1994. Phosphatidylcholine translocase: a physiological role for the mdr2 gene. Cell, 77: 1071-1081.
77. Sarkadi, B., and Muller, M. 1997. Search for specific inhibitors of multidrug resistance in cancer. Semin. Cancer Biol. 8: 171-182.
78. 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.
79. Schinkel, A. H. 1997. The physiological function of drug-transporting P-glycoproteins. Semin. Cancer Biol. 8: 161-170.
80. Schinkel, A. H., Smit, J. J., van Tellingen, O., Beijnen, J. H., Wagenaar, E., van Deemter, L., Mol, C. A., van der Valk, M. A., Robanus-Maandag, E. C., te Riele, H. P., and et al. 1994. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell, 77: 491-502.
81. Schuetz, E. G., Schinkel, A. H., Relling, M. V., and Schuetz, J. D. 1996. P-glycoprotein: a major determinant of rifampicin-inducible expression of cytochrome P4503A in mice and humans. Proc. Natl. Acad. Sci. U.S.A. 93: 4001-4005.
82. 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.
83. Sharom, F. J. 1997. The P-glycoprotein efflux pump: how does it transport drugs? J. Membr. Biol. 160: 161-175.
84. 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: 24 197-24 202.
85. 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.
86. Skach, W. R., Calayag, M. C., and Lingappa, V. R. 1993. Evidence for an alternate model of human P-glycoprotein structure and biogenesis. J. Biol. Chem. 268: 6903-6908.
87. Smit, J. J., Schinkel, A. H., Oude Elferink, R. P., Groen, A. K., Wagenaar, E., van Deemter, L., Mol, C. A., Ottenhoff, R., van der Lugt, N. M., van Roon, M. A., and et al. 1993. Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease. Cell, 75: 451-462.
88. Smith, A. J., Timmermans-Hereijgers, J. L., Roelofsen, B., Wirtz, K. W., van Blitterswijk, W. J., Smit, J. J., Schinkel, A. H., and Borst, P. 1994. The human MDR3 P-glycoprotein promotes translocation of phosphatidylcholine through the plasma membrane of fibroblasts from transgenic mice. FEBS Lett. 354: 263-266.
89. Tang-Wai, D. F., Kajiji, S., DiCapua, F., de Graaf, D., Roninson, I. B., and Gros, P. 1995. Human (MDR1) and mouse (mdr1, mdr3) P-glycoproteins can be distinguished by their respective drug resistance profiles and sensitivity to modulators. Biochemistry, 34: 32-39.
90. Thiebaut, F., Tsuruo, T., Hamada, H., Gottesman, M. M., Pastan, I., and Willingham, M. C. 1987. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc. Natl. Acad. Sci. U.S.A. 84: 7735-7738.
91. Thottassery, J. V., Zambetti, G. P., Arimori, K., Schuetz, E. G., and Schuetz, J. D. 1997. p53-dependent regulation of MDR1 gene expression causes selective resistance to chemotherapeutic agents. Proc. Natl. Acad. Sci. U.S.A. 94: 11 037-11 042.
92. Tominaga, M., Tominaga, T., Miwa, A., and Okada, Y. 1995. Volume-sensitive chloride channel activity does not depend on endogenous P-glycoprotein. J. Biol. Chem. 270: 27 887-27 893.
93. Trezise, A. E., Romano, P. R., Gill, D. R., Hyde, S. C., Sepulveda, F. V., Buchwald, M., and Higgins, C. F. 1992. The multidrug resistance and cystic fibrosis genes have complementary patterns of epithelial expression. EMBO J. 11: 4291-4303.
94. Tsuruo, T., Iida, H., Tsukagoshi, S., and Sakurai, Y. 1981. Overcoming of vincristine resistance in P388 leukemia in vivo and in vitro through enhanced cytotoxicity of vincristine and vinblastine by verapamil. Cancer Res. 41: 1967-1972.
95. Tsuruo, T., Iida, H., Nojiri, M., Tsukagoshi, S., and Sakurai, Y. 1983. Circumvention of vincristine and Adriamycin resistance in vitro and in vivo by calcium influx blockers. Cancer Res. 43: 2905-2910.
96. Ueda, K., Cardarelli, C., Gottesman, M. M., and Pastan, I. 1987. Expression of a full-length cDNA for the human "MDR1" gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc. Natl. Acad. Sci. U.S.A. 84: 3004-3008.
97. Valverde, M. A., Diaz, M., Sepulveda, 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 (London), 355: 830-833.
98. Valverde, M. A., Bond, T. D., Hardy, S. P., Taylor, J. C., Higgins, C. F., Altamirano, J., and Alvarez-Leefmans, F. J. 1996. The multidrug resistance P-glycoprotein modulates cell regulatory volume decrease. EMBO J. 15: 4460-4468.
99. Van der Bliek, A. M., Baas, F., Ten Houte de Lange, T., Kooiman, P. M., Van der Velde-Koerts, T., and Borst, P. 1987. The human mdr3 gene encodes a novel P-glycoprotein homologue and gives rise to alternatively spliced mRNAs in liver. EMBO J. 6: 3325-3331.
100. Van der Bliek, A. M., Baas, F., Van der Velde-Koerts, T., Biedler, J. L., Meyers, M. B., Ozols, R. F., Hamilton, T. C., Joenje, H., and Borst, P. 1988. Genes amplified and overexpressed in human multidrug-resistant cell lines. Cancer Res. 48: 5927-5932.
101. Weinstein, R. S., Jakate, S. M., Dominguez, J. M., Lebovitz, M. D., Koukoulis, G. K., Kuszak, J. R., Klusens, L. F., Grogan, T. M., Saclarides, T. J., Roninson, I. B., and Coon, J.S. 1991. Relationship of the expression of the multidrug resistance gene product (P-glycoprotein) in human colon carcinoma to local tumor aggressiveness and lymph node metastasis. Cancer Res. 51: 2720-2726.
102. Zhang, M., Wang, G., Shapiro, A., and Zhang, J. T. 1996. Topological folding and proteolysis profile of P-glycoprotein in membranes of multidrug-resistant cells: implications for the drug-transport mechanism. Biochemistry, 35: 9728-9736.