Expression of the Plasmodial pfmdr1 Gene in Mammalian Cells Is Associated with Increased Susceptibility to Chloroquine

REFERENCES

• Awad-el-Kariem, F. M., M. A. Miles, and D. C. Warhurst. 1992. Chloroquine-resistant Plasmodium falciparum isolates from the Sudan lack two mutations in the pfmdrl gene thought to be associated with chloroquine resistance. Trans. R. Soc. Trop. Med. Hyg. 86:587–589.
   PubMed Web of Science ®Google Scholar
• Barasch, J., B. Kiss, A. Prince, L. Saiman, D. Gruenert, and Q. al Awqati. 1991. Defective acidification of intracellular organelles in cystic fibrosis. Nature (London) 352:70–73.
   PubMed Web of Science ®Google Scholar
• Barnes, D. A., S. J. Foote, D. Galatis, D. J. Kemp, and A. F. Cowman. 1992. Selection for high-level chloroquine resistance results in deamplification of the pfmdrl gene and increased sensitivity to mefloquine in Plasmodium falciparum. EMBO J. 11:3067–3075.
   PubMed Web of Science ®Google Scholar
• Bray, P. G., R. E. Howells, G. Y. Ritchie, and S. A. Ward. 1992. Rapid chloroquine efflux phenotype in both chloroquine-sensitive and chloroquine-resistant Plasmodium falciparum. Biochem. Pharmacol. 44:1317–1324.
   PubMed Web of Science ®Google Scholar
• Cain, C. C., and R. F. Murphy. 1986. Growth inhibition of 3T3 fibroblasts by lysosomotropic amines: correlation with effects on intravesicular pH but not vacuolation. J. Cell. Physiol. 129:65–70.
   PubMedGoogle Scholar
• Castillo, G., J. C. Vera, C. P. Yang, S. B. Horwitz, and O. M. Rosen. 1990. Functional expression of murine multidrug resistance in Xenopus laevis oocytes. Proc. Natl. Acad. Sci. USA 87:4737–4741.
   PubMedGoogle Scholar
• Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156–159.
   PubMed Web of Science ®Google Scholar
• Cornwell, M. M., I. Pastan, and M. M. Gottesman. 1987. Certain calcium channel blockers bind specifically to multidrug-resistant human KB carcinoma membrane vesicles and inhibit drug binding to P-glycoprotein. J. Biol. Chem. 262:2166–2170.
   PubMed Web of Science ®Google Scholar
• Cornwell, M. M., T. Tsuruo, M. M. Gottesman, and I. Pastan. 1987. ATP-binding properties of P glycoprotein from multidrug-resistant KB cells. FASEB J. 1:51–54.
   PubMed Web of Science ®Google Scholar
• Cowman, A. F., S. Karcz, D. Galatis, and J. G. Culvenor. 1991. A P-glycoprotein homologue of Plasmodium falciparum is localized on the digestive vacuole. J. Cell Biol. 113:1033–1042.
   PubMed Web of Science ®Google Scholar
• de Groot, P. G., R. P. J. Oude Elferink, M. Hollemans, A. Strijland, A. Westerveld, P. Meera Khan, and J. M. Tager. 1981. Inactivation by chloroquine of alfa-galactosidase in cultured human skin fibroblasts. Exp. Cell Res. 136:327–333.
   PubMedGoogle Scholar
• Devault, A., and P. Gros. 1990. Two members of the mouse mdr gene family confer multidrug resistance with overlapping but distinct drug specificities. Mol. Cell. Biol. 10:1652–1663.
   PubMed Web of Science ®Google Scholar
• Endicott, J. A., and V. Ling. 1989. The biochemistry of P-glyco-protein-mediated multidrug resistance. Annu. Rev. Biochem. 58:137–171.
   PubMed Web of Science ®Google Scholar
• Ferrari, V., and D. J. Cutler. 1991. Simulation of kinetic data on the influx and efflux of chloroquine by erythrocytes infected with Plasmodium falciparum. Evidence for a drug-importer in chloro-quine-sensitive strains. Biochem. Pharmacol. 42:S167–S179.
   PubMed Web of Science ®Google Scholar
• Foote, S. J., D. E. Kyle, R. K. Martin, A. M. Oduola, K. Forsyth, D. J. Kemp, and A. F. Cowman. 1990. Several alleles of the multidrug-resistance gene are closely linked to chloroquine resistance in Plasmodium falciparum. Nature (London) 345:255–258.
   PubMed Web of Science ®Google Scholar
• Foote, S. J., J. K. Thompson, A. F. Cowman, and D. J. Kemp. 1989. Amplification of the multidrug resistance gene in some chloro-quine-resistant isolates of P. falciparum. Cell 57:921–930.
   PubMed Web of Science ®Google Scholar
• Gill, D. R., S. C. Hyde, C. F. Higgins, M. A. Valverde, G. M. Mintenig, and F. V. Sepulveda. 1992. Separation of drug transport and chloride channel functions of the human multidrug resistance P-glycoprotein. Cell 71:23–32.
   PubMed Web of Science ®Google Scholar
• Ginsburg, H., and W. D. Stein. 1991. Kinetic modelling of chloroquine uptake by malaria-infected erythrocytes. Assessment of the factors that may determine drug resistance. Biochem. Pharmacol. 41:1463–1470.
   PubMed Web of Science ®Google Scholar
• Goldberg, D. E., and A. F. G. Slater. 1992. The pathway of hemoglobin degradation in malaria parasites. Parasitol. Today 8:280–283.
   PubMedGoogle Scholar
• Groen, A. K., R. C. Vervoorn, R. J. A. Wanders, R. van der Meer, and J. M. Tager. 1982. An evaluation of the metabolite indicator method for determining the cytosolic phosphate potential in rat liver cells. Biochim. Biophys. Acta 721:172–177.
   PubMedGoogle Scholar
• Gros, P., F. Talbot, D. Tang Wai, E. Bibi, and H. R. Kaback. 1992. Lipophilic cations: a group of model substrates for the multidrug-resis ance transporter. Biochemistry 31:1992–1998.
   PubMed Web of Science ®Google Scholar
• Hammond, J. R., R. M. Johnstone, and P. Gros. 1989. Enhanced efflux of [3H]vinblastine from Chinese hamster ovary cells trans-fected with a full-length complementary DNA clone for the mdr1 gene. Cancer Res. 49:3867–3871.
   PubMed Web of Science ®Google Scholar
• Higgins, C. F. 1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67–113.
   PubMedGoogle Scholar
• Karcz, S., and A. F. Cowman. 1991. Similarities and differences between the multidrug resistance phenotype of mammalian tumor cells and chloroquine resistance in Plasmodium falciparum. Exp. Parasitol. 73:233–240.
   PubMedGoogle Scholar
• Karcz, S. R., D. Galatis, and A. F. Cowman. 1993. Nucleotide binding of a P-glycoprotein homologue from Plasmodium falciparum. Mol. Biochem. Parasitol. 58:269–276.
   PubMedGoogle Scholar
• Kaufman, R. J. 1985. Identification of the components necessary for adenovirus translational control and their utilization in cDNA expression vectors. Proc. Natl. Acad. Sci. USA 82:689.
   PubMed Web of Science ®Google Scholar
• Krogstad, D. J., I. Y. Gluzman, B. L. Herwaldt, P. H. Schlesinger, and T. E. Wellems. 1992. Energy dependence of chloroquine accumulation and chloroquine efflux in Plasmodium falciparum. Biochem. Pharmacol. 43:57–62.
   PubMed Web of Science ®Google Scholar
• Krogstad, D. J., I. Y. Gluzman, D. E. Kyle, A. M. Oduola, S. K. Martin, W. K. Milhous, and P. H. Schlesinger. 1987. Efflux of chloroquine from Plasmodium falciparum: mechanism of chloroquine resistance. Science 238:1283–1285.
   PubMed Web of Science ®Google Scholar
• Krogstad, D. J., and P. H. Schlesinger. 1987. The basis of antimalarial action: non-weak base effects of chloroquine on acid vesicle pH. Am. J. Trop. Med. Hyg. 36:213–220.
   PubMed Web of Science ®Google Scholar
• Lemontt, J. F., M. Azzaria, and P. Gros. 1988. Increased mdr gene expression and decreased drug accumulation in multidrug-resis-tant human melanoma cells. Cancer Res. 48:6348–6353.
   PubMed Web of Science ®Google Scholar
• Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Martin, S. K., A. M. Oduola, and W. K. Milhous. 1987. Reversal of chloroquine resistance in Plasmodium falciparum by verapamil. Science 235:899–901.
   PubMed Web of Science ®Google Scholar
• Muller, R., and J. R. Baker. 1990. Medical parasitology. Gower Medical Publishing, London.
   Google Scholar
• Oude Elferink, R. P. J., R. Ottenhoff, W. G. M. Liefting, B. Schoemaker, A. K. Groen, and P. L. M. Jansen. 1990. ATP-dependent efflux of GSSG and GS-conjugate from isolated rat hepatocytes. Am. J. Physiol. 258:G699–G706.
   PubMed Web of Science ®Google Scholar
• Safa, A. R. 1988. Photoaffinity labeling of the multidrug-resistance-related P-glycoprotein with photoactive analogs of verapamil. Proc. Natl. Acad. Sci. USA 85:7187–7191.
   PubMed Web of Science ®Google Scholar
• Safa, A. R., C. J. Glover, M. B. Meyers, J. L. Biedler, and R. L. Felsted. 1986. Vinblastine photoaffinity labeling of a high molecular weight surface membrane glycoprotein specific for multidrug-resistant cells. J. Biol. Chem. 261:6137–6140.
   PubMed Web of Science ®Google Scholar
• Schurr, E., M. Raymond, J. C. Bell, and P. Gros. 1989. Characterization of the multidrug resistance protein expressed in cell clones stably transfected with the mouse mdrl cDNA. Cancer Res. 49:2729–2733.
   PubMed Web of Science ®Google Scholar
• Slater, A. F., and A. Cerami. 1992. Inhibition by chloroquine of a novel haem polymerase enzyme activity in malaria trophozoites. Nature (London) 355:167–169.
   PubMed Web of Science ®Google Scholar
• Tager, J. M., J. M. F. G. Aerts, R. J. A. Oude Elferink, A. K. Groen, M. Hollemans, and A. W. Schram. 1988. pH regulation of intracellular membrane flow, p. 123–155. In D. Haussinger (ed.), pH homeostasis. Mechanisms and control. Academic Press Ltd., London.
   Google Scholar
• Trager, W., and J. B. Jensen. 1976. Human malaria parasites in continuous culture. Science 193:673–675.
   PubMed Web of Science ®Google Scholar
• van Es, H. H. G., E. Skamene, and E. Schurr. 1993. Chemotherapy of malaria, a battle against all odds? Clin. Invest. Med. 16:285–293.
   Google Scholar
• Veignie, E., and S. Moreau. 1991. The mode of action of chloroquine. Non-weak base properties of 4-aminoquinolines and antimalarial effects on strains of Plasmodium. Ann. Trop. Med. Parasitol. 85:229–237.
   Google Scholar
• Wellems, T. E., L. J. Panton, I. Y. Gluzman, V. E. do Rosario, R. W. Gwadz, A. Walker Jonah, and D. J. Krogstad. 1990. Chloroquine resistance not linked to mdr-like genes in a Plasmodium falciparum cross. Nature (London) 345:253–255.
   PubMed Web of Science ®Google Scholar
• Wigler, M. A., A. Pellicer, S. Silverstein, R. Axel, G. Urlaub, and L. Chasin. 1979. DNA-mediated transfer of the adenine phosphori-bosyltransferase locus into mammalian cells. Proc. Natl. Acad. Sci. USA 76:1373–1376.
   PubMed Web of Science ®Google Scholar
• Wilson, C. G., S. K. Volkman, S. Thaithong, R. K. Martin, D. E. Kyle, W. K. Milhous, and D. F. Wirth. 1993. Amplification of pfmdrl associated with mefloquine and halofantrine resistance in Plasmodium falciparum from Thailand. Mol. Biochem. Parasitol. 57:151–160.
   PubMed Web of Science ®Google Scholar