Biophysical aspects of P-glycoprotein-mediated multidrug resistance

International Review of Cytology

Volumn 171, Issue , 1997, Pages 121-165

  Wadkins, Randy M ^a   Roepe, Paul D ^b  

^a CTRC Institute for Drug Development   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENT; DACTINOMYCIN; DOXORUBICIN; GLYCOPROTEIN P; MEMBRANE RECEPTOR; SULFONYLUREA; TETRACYCLINE; TRANSMEMBRANE CONDUCTANCE REGULATOR; VINBLASTINE; VINCRISTINE;

ANTIBIOTIC RESISTANCE; BIOPHYSICS; CANCER CELL CULTURE; CELL MEMBRANE POTENTIAL; CELL PH; DRUG ACCUMULATION; DRUG DIFFUSION; DRUG TRANSPORT; ENZYME ACTIVITY; MEMBRANE TRANSPORT; MOLECULAR CLONING; MULTIDRUG RESISTANCE; NUCLEOTIDE TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; THERMODYNAMICS;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; DRUG RESISTANCE, MULTIPLE; GENES, MDR; HUMANS; HYDROGEN-ION CONCENTRATION; P-GLYCOPROTEIN; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); MURINAE; PLASMODIUM FALCIPARUM;

EID: 0030988015     PISSN: 00747696     EISSN: None     Source Type: Book Series    
DOI: 10.1016/s0074-7696(08)62587-5     Document Type: Article

References (124)

1. Abraham, E. H., Prat, A. G., Gerweck, L., Seneveratne, T., Arceci, R. J., Kramer, R., Guidotti, G., and Cantiello, H. F. (1993). The multidrug resistance (mdr1) gene product functions as an ATP channel. Proc. Natl. Acad. Sei. USA 90, 312-316.
2. Abrams, A., and Baron, C. (1967). The isolation and subunit structure of streptococcal membrane adenosine triphosphatase. Biochemistry 6, 225-229.
3. Abrams, A., Smith, J. B., and Baron, C. (1972). Carbodiimide-resistant membrane adenosine triphosphatase in mutants of Streptococcus faecalis. I. Studies of the mechanism of resistance. J. Biol. Chem. 247, 1484-1488.
4. Aguilar-Bryan, L., Nichols, C. G., Wechsler, S. W., Clement, J. P., Boyd, A. E., Gonzalez, G., Herrera-Sosa, H., Nguy, K., Bryan, J., and Nelson, D. A. (1995). Cloning of the β cell high-affinity sulfonylurea receptor: A regulator of insulin secretion. Science 268, 423-426.
5. Al-Awqati, Q. (1995). Regulation of ion channels by ABC transporters that secrete ATP. Science 269, 805-806.
6. Alloing, G., Trombe, M. C., and Claverys, J. P. (1990). The ami locus of the gram-positive bacterium Streptococcuspneumoniae is similar to binding protein-dependent transport operons of gram-negative bacteria. Mol. Microbiol. 4, 633-644.
7. Al-Shawi, M K., Urbatsch, I. L., and Senior, A. E. (1994). Covalent inhibitors of P-glycoprotein ATPase activity. J. Biol. Client. 269, 8986-8992.
8. Altenberg, G. A., Young, G., Horton, J. K., Glass, D., Belli, J. A., and Reuss, L. (1993). Changes in intra- or extracellular pH do not mediate P-glycoprotein-dependent multidrug resistance. Proc. Natl. Acad. Sei. USA 90, 9735-9738.
9. Altenberg, G. A., Deitmer, J. W., Glass, D. C., and Reuss, L. (1994). P-glycoprotein-associated Cl~ currents are activated by cell swelling but do not contribute to cell volume regulation. Cancer Res. 54, 618-622.
10. 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. Sei. USA 89, 8472-8476.
11. Ames, G. F.-L. (1986). The basis of multidrug resistance in mammalian cells: Homology with bacterial transport. Cell 47, 323-324.
12. Aszalos, A., Damjanovich, S., and Gottesman, M. M. (1986). Depolymerization of microtubules alters membrane potential and affects the motional freedom of membrane proteins. Biochemistry 25, 5804-5809.
13. Bakker, E. P., Rottenberg, H., and Caplan, S. R. (1976). An estimation of the light-induced electrochemical potential difference of protons across the membrane of Halobacterium halobium. Biochim. Biophys. Ada 440, 557-564.
14. Ballarin-Denti, A., Den Hollander, J. A., Sanders, D., Slayman, C. W., and Slayman, C. L. (1984). Kinetics and pH-dependence of glycine-proton symport in Saccharomyces cerevisiae. Biochim. Biophys. Acta 778,1-16.
15. Bally, M. B., Hope, M. J., Van Echteld, C. J. A., and Cullis, P. R. (1985). Uptake of safranine and other lipophillic cations into model membrane systems in response to membrane potential. Biochim. Biophys. Ada 812, 66-76.
16. Balzi, E., and Goffeau, A. (1991). Multiple or pleiotropic drug resistance in yeast. Biochim. Biophys. Ada 1073, 241-252.
17. Barry, M. A., Reynolds, J. E., and Eastman, A. (1993). Etoposide-induced apoptosis in human HL-60 cells is associated with intracellular acidification. Cancer Res. S3, 2349-2357.
18. Bear, C. E., Li, C., Kartner, N., Bridges, R. J., Jensen, T. J., Ramjeesingh, M., and Riordan, J. R. (1992). Purification and functional reconstitution of the cystic fibrosis transmembrane conductance regulator (CFTR). Cell 68, 809-818.
19. Beck, W. T. (1987). The cell biology of multiple drug resistance. Biochem. Pharmacol. 36,2879-2887.
20. Bertl, A., Slayman, C. L., and Gradmann, D. (1993). Gating and conductance in an outwardly-rectifying K+ channel from the plasma membrane oiSaccharomyces cerevisiae. J. Membrane Biol. 132, 183-199.
21. 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.
22. Bornmann, W., and Roepe, P. D. (1994). Analysis of drug transport kinetics in multidrug-resistant cells using a novel coumarin-vinblastine compound. Biochemistry 33,12665-12675.
23. Burchenal, J. H., Robinson, E., Johnston, S. F., and Kushida, M. M. (1950). Induction of resistance to aminopterin in a strain of transmitted mouse leukemia. Science 111, 116-121.
24. Cafiso, D. S., and Hubbell, W. L. (1979). Estimation of transmembrane potentials from the phase equilibria of hydrophobic paramagnetic ions. Biochemistry 17, 187-195.
25. Cafiso, D. S., and Hubbell, W. L. (1982). Transmembrane electrical curents of spin-labeled hydrophobic ions. Biophys. J. 39, 263-272.
26. Callaghan, R., van Gorkom, L. C. M., and Epand, R. M. (1992). A comparison of membrane properties and composition between cell lines selected and transfected for multi-drug resistance. Br. J. Cancer 66, 781-786.
27. Cantiello, H. F., Prat, A. G., Reisin, I. L., Ercole, L. B., Abraham, E. H., Amara, J. F., Gregory, R. J., and Ausiello, D. A. (1994). External ATP and its analogs activate the cystic fibrosis transmembrane conductance regulator by a cyclic AMP-independent mechanism. J. Biol. Chem. 269. 11224-11232.
28. 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.
29. + antiporter that is physiologically important at elevated pH. J. Biol. Chem. 269, 27365-27371.
30. Choi, K., Frommel, T. O., Stern, R. K., Ferez, C. F., Kriegler, M., Tsuruo, T., and Roninson, I. B. (1991). Multidrug resistance after retroviral transfer of the human MDR1 gene correlates with P-glycoprotein density in the plasma membrane and is not affected by cytotoxic selection. Proc. Nail. Acad. Sei. USA 88, 7386-7390.
31. Cole, S. P. C, Bhardwaj, G., Gerlach, J. H., Mackie, J. E., Grant, C. E., Almquist, K. C, Stewart, A. J., Kurz, E. U., Duncan, A. M. V., and Deeley, R. G. (1992). Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258,1650-1654.
32. Coley, H. M., Twentyman, P. R., and Workman, P. (1993). The efflux of anthracyclines in multidrug-resistant cell lines. Biochem. Pharmacol. 46, 1317-1326.
33. Danø, K. (1973). Active outward transport of daunomycin in resistant Ehrlich ascites tumor cells. Biochim. Biophys. Acta 323,466-483.
34. de Kroon, A. I. P. M., Vogt, B., van't Hof, R., de Kruijff, B., and de Gier, J. (1991). Ion gradient-induced membrane translocation of model peptides. Biophys. J. 60, 525-537.
35. Descoteaux, S., Shen, P. S., Ayala, P., Orozco, E., and Samuelson, J. (1992). P-glycoprotein genes of Entamoeba Histolytica. Arch. Med. Res. 23, 23-25.
36. Deuticke, B. (1977). Properties and structural basis of simple diffusion pathways in the erythrocyte membrane. Rev. Physiol. Biochem. Pharmacol. 78, 1-97.
37. Devault, A., and Gros, P. (1990). Two members of the Mouse mdr gene family confer multidrug resistance with overlapping but distinct drug specificities. Mol. Cell. Biol. 10, 1652-1663.
38. Dordal, M. S., Winter, J. N., and Atkinson, A. J., Jr. (1992). Kinetic analysis of p-glycoprotein-mediated doxorubicin efflux. J. Pharmacol. Exp. Ther. 263, 762-766.
39. - channels by protein kinase A corrected by insertion of CFTR. Nature 358, 581-584.
40. Elgavish, A. (1991). High intracellular pH in CFPAC: A pancreas cell line from a patient with cystic fibrosis is lowered by retrovirus-mediated CFTR gene transfer. Biochem. Biophys. Res. Commun. 180, 342-348.
41. El-Moatassim, C., Dornand, J., and Mani, J.-C. (1992). Extracellular ATP and cell signalling. Blochim. Biophys. Acta 1134, 31-45.
42. Gadsby, D. C., and Nairn, A. C. (1994). Regulation of CFTR channel gating. Trends Biochem. Sei. 19, 513-518.
43. 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.
44. Gill, D. R., Hyde, S., Higgins, C. F., Valverde M. A., Mintenig, G. M., and Sepúlveda, F. V. (1992). Seperation of drug transport and chloride channel functions of the human multidrug resistance P-glycoprotein. Cell 71, 23-32.
45. Gottesman, M. M., and Pastan, I. (1993). Biochemistry of multidrug resistance mediated by the multidrug transporter. Anna. Rev. Biochem. 62, 385-427.
46. Grant, C. E., Valdimarsson, G., Hipfner, D. R., Almquist, K. C., Cole, S. P. C., and Deeley, R. G. (1994). Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res. 54, 357-361.
47. Gros, P., Croop, J., and Housman, D. (1986a). Mammalian multidrug-resistance gene: Complete cDNA sequence indicates a strong homology to bacterial transport proteins. Cell 47, 371-380.
48. Gros, P., Neriah, Y. B., Croop, J. M., and Housman, D. E. (1986b). Isolation and expression of a complementary DNA that confers multidrug resistance. Nature (London) 323,728-731.
49. Gros, P., Talbot, F., Tang-Wai, D., Bibi, E., and Kaback, H. R. (1992). Lipophillic cations: A group of model substrates for the multidrug-resistance transporter. Biochemistry 31,1992-1998.
50. Guild, B. C, Mulligan, R. C, Gros, P., and Housman, D. E. (1988). Retroviral transfer of a murine cDNA for multidrug resistance confers pleitropic drug resistance to cells without prior drug selection. Proc. Natl. Acad. Sei. USA 85,1595-1599.
51. Hardy, S. P., Goodfellow, H. R., Valverde, M. A., Gill, D. R., Sépulveda, F. 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.
52. Harold, F. M., Baarda, J. R., Baron, C., and Abrams, A. (1969). Inhibition of membrane-bound adenosine triphosphatase and of cation transport in Streptococcus faecalis by N,N′-dicyclohexylcarbodiimide. J. Biol. Chem. 244, 2261.
53. Hasselbach, W. (1978). The reversibility of the SR pump. Biochim. Biophys. Acta 515,23-53.
54. Higgins, C. F., and Gottesman, M. M. (1992). Is the multidrug transporter a flippase? Trends Biochem. Sei. 17, 18-19.
55. Higgins, C. F., Gallagher, M. P., Hyde, S. C, Mimmack, M. L., and Pearce, S. R. (1990). ABC transporters: From micro-organisms to man. Phil. Trans. K. Soc. London 326,353-365.
56. i and membrane potential in hu MDR1 transfectants sufficient to cause MDR protein-mediated multidrug resistance? J. Gen. Physiol. 108, 295-313.
57. Hope, M. J., and Cullis, P. R. (1987). Lipid asymmetry induced by transmembrane pH gradients in large unilamellar vesicles. J. Biol. Chem. 262, 4360-4366.
58. Horichi, N., Tapiero, H., Sugimoto, Y., Bungo, M., Nishiyama, M., Fourcade, A., Lampidis, T.,J., Kasahara, K., Sasaki, Y., Takahashi, T., and Saijo, N. (1990). 3′-Deamino-3′-morpholino-13-deoxo-10-hydroxycarminomycin conquers multidrug resistance by rapid influx following higher frequency of formation of DNA single- and double-strand breaks. Cancer Res. 50, 4698-4701.
59. Huang, N.-N., Ahmed, A. H., Wang, D.-J., and Heppel, L. A. (1992). Extracellular ATP stimulates increases in Na+/K+ pump activity, intracellular pH and uridine uptake in cultures of mammalian cells. Biochem. Biophys. Res. Commun. 182, 836-843.
60. Inagaki, N., Gonoi, T., Clement, J. P., Namba, N., Inazawa, J., Gonzalez, G., Aguilar-Bryan, L., Seino, S., and Bryan, J. (1995). Reconstitution of IKATP: An inward rectifier subunit plus the sulfonyl urea receptor. Science 270, 1166-1170.
61. Karcz, S., and Cowman, A. F. (1991). Similarities and differences between the multidrug resistance phenotype of mammalian tumor cells and chloroquine resistance in Plasmodium falciparum. Exp. Parasitol. 73, 233-240.
62. Knowles, M. R., Clarke, L. L., and Boucher, R. C. (1991). Activation by extracellular nucleotides of chloride secretion in the airway epithelia of patients with cystic fibrosis. N. Engl. J. Meet. 325, 533-538.
63. Koefoed, P., and Brahm, J. (1994). The permeability of the human red cell membrane to steroid sex hormones. Biochim. Biophys. Acta 1195, 55-62.
64. Leveille-Webster, C. R., and Arias, I. M. (1995). The biology of the P-glycoproteins. J. Membrane Biol. 143, 89-102.
65. Lewis, K. (1994). Multidrug resistance pumps in bacteria: Variations on a theme. Trends Biol. Sei. 19, 119-123.
66. Lothstein, L., Rodrigues, P. J., Sweatman, T. W., and Israel, M. (1994). Effects of 14-acyl congeners of N-benzyIadriamycin-14-valerate (AD 198) on cytotoxicity and subcellular drug distribution in AD 198-resistant mouse J774.2 cells. Proc. Am. Assoc. Cancer Res. 35,342. [Abstract No. 2037]
67. Luckie, D. B., Krouse, M. E., Harper, K. L., Law, T. C, and Wine, J. J. (1994). Selection for MDR1/P-glycoprotein enhances swelling-activated K+ and Cl-currents in NIH/3T3 cells. Am. J. Physiol. C 267, 650-658.
68. - exchange in Chinese hamster ovary cells. Biochemistry 33, 7239-7249.
69. Magin, R. L., Niesman, M. R., and Bacic, G. (1990). Influence of fluidity on membrane permeability: Correspondence between studies of membrane models and simple biological systems. Adv. Membrane Fluidity 4, 221-237.
70. Mayer, L. D., Bally, M. B., Hope, M. J., and Cullis, P. R. (1985a). Uptake of dibucaine into large unilamellar vesicles in response to a membrane potential. J. Biol. Chem. 260,802-808.
71. Mayer, L. D., Bally, M. B., Hope, M. J., and Cullis, P. R. (1985b). Uptake of antineoplastic agents into large unilamellar vesicles in response to a membrane potential. Biochim. Biophys. Acta 816, 294-302.
72. Minotti, A. M., Barlow, S. B., and Cabrai, F. (1991). Resistance to antimitotic drugs in Chinese hamster ovary cells correlates with changes in the level of polymerized tubulin. J. Biol. Chem. 266, 3987-3994.
73. Mukhopadhyay, K., Parrack, P. K., and Bhattacharyya, B. (1990). The carboxy terminus of the a subunit of tubulin regulates its interaction with colchicine. Biochemistry 29,6845-6850.
74. Noy, N., Donnelly, T. M., and Zakim, D. (1986). Physical-chemical model studies for the entry of water-insoluble compounds into cells. Studies of fatty acid uptake by the liver. Biochemistry 25, 2013-2021.
75. Parra-Lopez, G, Baer, M. T., and Groisman, E. A. (1993). Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimiiriiim. EMBO J. 12, 4053-4062.
76. Pérez-Sala, D.; Collado-Escobar, D., and Mollinedo, F. (1995). Intracellular alkalinization suppresses lovastatin-induced apoptosis in HL-60 cells through the inactivation of a pH-dependent endonuclease. J. Biol Chem. 270, 6235-6242.
77. Praet, M., Defrise-Quertain, F., and Ruysschaert, J. M. (1993). Comparison of adriamycin and derivatives uptake into large unilamellar lipid vesicles in response to a membrane potential. Biochim. Biophys. Acta 1148, 342-350.
78. Qian, X.-D., and Beck, W. T. (1990). Progesterone photoaffinity labels p-glycoprotein in multidrug-resistant human leukemic lymphoblasts. J. Biol. Chem. 265,18753-18756.
79. Ramu, A., Pollard, H. B., and Rosario, L. M. (1989). Doxorubicin resistance in P388 leukemia - Evidence for reduced drug influx. Int. J. Cancer 44, 539-547.
80. Reddy, M. M., Quinton, P. M., Haws, C, Wine, J. J., Grygorczyk, R., Tabcharani, J. A., Hanrahan, J. W., Gunderson, K. L., and Kopito, R. R. (1996). Failure of the cystic fibrosis transmembrane conductance regulator to conduct ATP. Science 271,1876-1879.
81. Reisin, I. L., Prat, A. G., Abraham, E. H., Amara, J. F., Gregory, R. J., Ausiello, D. A., and Cantiello, H. F. (1994). The cystic fibrosis transmembrane conductance regulator is a dual ATP and chloride channel. J. Biol. Chem. 269, 20584-20591.
82. Riordan, J. R., Rommens, J. M., Kerem, B.-S., Alon, N., Rozmahel, R., Grzelczak, Z., Zielenski, J., Lok, S., Plavsic N., Chou, J.-L., Drumm, M. L., lannuzzi, M. C, Collins, F. S., and Tsui, L.-C. (1989). Identification of the cystic fibrosis gene: Cloning and characterization of complementary DNA. Science 245, 1066-1072.
83. i on the cellular retention of doxorubicin analyzed via a comparison between CFTR and MDR transfectants. Biochem. Pharmacol. 52, 1081-1095.
84. Roepe, P. D. (1992). Analysis of the steady-state and initial rate of doxorubicin efflux from a series of multidrug-resistant cells expressing different levels of p-glycoprotein. Biochemistry 31, 12555-12564.
85. Roepe, P. D. (1994). Indirect mechanism of drug transport by P-glycoprotein. Drug transport mediated by P-glycoprotein may be secondary to electrochemical perturbations of the plasma membrane. Trends Pharmacol. Sei. 15, 445-446.
86. Roepe, P. D. (1995). The role of the MDR protein in altered drug translocation across tumor cell membranes. Biochim. Biophys. Acta 1241, 385-406.
87. + symport. Res. Microbiol. (Ann. Pasteur Inst.) 141, 290-308.
88. i homeostasis in multidrug-restant (MDR) cells: Further characterization of a series of MDR cell lines expressing different levels of p-glycoprotein. Biochemistry 32, 11042-11056.
89. Ruetz, S., and Gros, P. (1994a). Functional expression of P-glycoprotein in secretory vesicles. J. Biol. Chem. 269, 12277-12284.
90. Ruetz, S., and Gros, P. (1994b). A mechanism for P-glycoprotein action in multidrug resistance: Are we there yet? Trends Pharmacol. Sei. 15, 260-263.
91. Ruetz, S., Raymond, M., and Gros, P. (1993). Functional expression of P-glycoprotein encoded by the mouse mdr3 gene in yeast cells. Proc. Natl. Acad. Sei. USA 90, 11588-11592.
92. Schlemmer, S. R., and Sirotnak, F. M. (1994). Functional studies of P-glycoprotein in inside-out plasma membrane vesicles derived from murine erythroleukemia cells overexpressing MDR3. J. Biol. Chem. 269, 31059-31066.
93. Schuldiner, S., and Kaback, H. R. (1975). Membrane potentials and active transport in membrane vesicles from Escherichia coll Biochemistry, 14, 5451-5461.
94. Schwiebert, E. M., Egan, M. E., Hwang, T.-H., Fulmer, S. B., Allen, S. S., Cutting, G. R., and Guggino, W. B. (1995). CFTR regulates outwardly rectifying chloride channels through an autocrine mechanism involving ATP. Cell 81, 1063-1073.
95. Scotto, K. W., Biedler, J., and Melera, P. W. (1986). Amplification and expression of genes associated with multidrug resistance in mammalian cells. Science 232, 751-755.
96. Shalinsky, D. R., Jekunen, A. P., Alcaraz, J. E., Christen, R. D., Kim, S., Khatibi, S., and Howell, S. B. (1993). Regulation of initial vinblastine influx by p-glycoprotein. Br. J. Cancer 67, 37-46.
97. 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.
98. Shapiro, A., and Ling, V. (1995a). Reconstitution of drug transport by purified P-glycoprotein. J. Biol Chem. 270,16167-16175.
99. Shapiro, A., and Ling, V. (1995b). Using purified P-glycoprotein to understand multidrug resistance. J. Bioenergetics Biomembranes 27, 7-13.
100. 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.
101. Simon, S. M., and Schindler, M. (1994). Cell biological mechanisms of multidrug resistance in tumors. Proc. Natl. Acad. Sei. USA 91, 3497-3504.
102. Simon, S. M., Roy, D., and Schindler, M. (1994). Intracellular pH and the control of multidrug resistance. Proc. Nail. Acad. Sei. USA 91, 1128-1132.
103. Sims, P. J., Waggoner, A. S., Wang, C.-H., and Hoffman, J. F. (1974). Studies on the mechanism by which cyanine dyes measure membrane potential in red blood cells and phosphatidylcholine vesicles. Biochemistry 13, 3315-3330.
104. Sirotnak, F. M., Yang, C.-H., Mines, L. S., Oribe, E., and Biedler, J. L. (1986). Markedly altered membrane transport and intracellular binding of vincristine in multidrug-resistant Chinese hamster cells selected for resistance to vinca alkaloids. J. Cell. Physiol. 126,266-274.
105. Skou, J. C, and Norby, J. G. (1979). "(Na.K)ATPase Structure and Kinetics." Academic Press, New York.
106. Stein, W. D., Cardarelli, C., 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.
107. Stow, M. W., and Warr, J. R. (1993). Reduced influx is a factor in accounting for reduced vincristine accumulation in certain verapamil-hypersensitive multidrug-resistant CHO cell lines. FEBS Lett. 320, 87-91.
108. Stutts, M. J., Gabriel, S. E., Olsen, J. C, Gatzy, J. T., O'Connell, T. L., Price, E. M., and Boucher, R. C. (1993). Functional consequences of heterologous expression of the cystic fibrosis transmembrane conductance regulator in fibroblasts. J. Biol. Chem. 268, 20653-20658.
109. Stutts, M. J., Canessa, C. M., Olsen, J. C, Hamrick, M., Cohn, J. A., Rossier, B. C, and Boucher, R. C. (1995). CFTR as a c-AMP dependent regulator of sodium channels. Science 269, 847-850.
110. Tew, K. D., Houghton, P. J., and Houghton, J. A. (1993). "Preclinical and clinical Modulation of Anticancer Drugs," pp. 156-160. CRC Press, Boca Raton, FL.
111. Trombe, M. C. (1993). Pleiotropic drug resistance in Streptococcus pneumoniae: The cross-chat hypothesis. Mol. Microbiol. 8,199-200.
112. Tsui, L.-C. (1992). The spectrum of cystic fibrosis mutations. Trends Genet. 8, 392-398.
113. Valverde, M., 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 355, 830-833.
114. Van Es, H. H. G., Renkema, H., Aerts, H., and Schurr, E. (1994). Enhanced lysosomal acidification leads to increased chloroquine accumulation in CHO cells expressing the pfmdr 1 gene. Mol. Biol. Parasitai. 68, 209-215.
115. Wadkins, R. M., and Houghton, P. J. (1993). The role of drug-lipid interactions in the biological activity of modulators of multi-drug resistance. Biochem. Biophys. Acta 1153, 225-236.
116. Wadkins, R. M., and Houghton, P. J. (1995). Kinetics of transport of dialkyloxacarbocyanines in multidrug-resistant cell lines overexpressing p-glycoprotein: Interrelationship of dye alkyl chain length, cellular flux, and drug resistance. Biochemistry 34, 3858-3872.
117. Watanabe, T. (1963). Infective heredity of multiple drug resistance in bacteria. Bacterial. Rev. 27, 87-115.
118. Wei, L. Y., and Roepe, P. D. (1994). Low external pH and osmotic shock increase the expression of human MDR protein. Biochemistry 33, 7229-7238.
119. Wei, L. Y., Stutts, M. J., Hoffman, M. M., and Roepe, P. D. (1995). Overexpression of the cystic fibrosis transmembrane conductance regulator in NIH 3T3 cells lowers membrane potential and intracellular pH and confers a multidrug resistance phenotype. Biophys. J. 69, 883-895.
120. Weisburg, J. H., Curcio, M., Caron, P. C, Raghu, G., Mechetner, E., Roepe, P. D., and Scheinberg, D. A. (1996). The multidrug resistance (MDR) phenotype confers immunological resistance. J. Exp. Med. 183, 2699-2704.
121. + symport across the plasma membrane. Escherichia coli. Biochem. J. 132, 587-592.
122. + exchange in Ehrlich ascites tumor cells. Regulation by extracellular ATP and 12-O-tetradecanoylphorbol 13-acetate. J. Biol. Chem. 261, 4529-4534.
123. Wilson, C. M., Serrano, A. E., Wasley, A., Bogenschutz, M. P., Shankar, A. H., and Wirth, D. F. (1989). Amplification of a gene related to mammalian mdr genes in drug-resistant Plasmodium falciparum. Science 244, 1184-1186.
124. Yang, C.-P. H., DePinho, S. G., Greenberger, L. M., Arceci, R. J., and Horwitz, S. B. (1989). Progesterone interacts with p-glycoprotein in multidrug-resistant cells and in the endometrium of Gravid Uterus. J. Biol. Chem. 264, 782-788.