Quinoline resistance mechanisms in Plasmodium falciparum: The debate goes on

Parasitology

Volumn 114, Issue SUPPL. 1, 1997, Pages

  Ward, S A ^a   Bray, P G ^a   Hawley, S R ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Chloroquine; Compartimental pH; Drug efflux; Drug uptake; High affinity binding; Resistance; Verapamil

Indexed keywords

AMINOQUINOLINE DERIVATIVE; CHLOROQUINE; QUINOLINE;

BINDING AFFINITY; CONFERENCE PAPER; DRUG ACCUMULATION; DRUG EFFICACY; DRUG UPTAKE; ENDEMIC DISEASE; MALARIA; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

AMINOQUINOLINES; ANIMALS; ANTIMALARIALS; BIOLOGICAL TRANSPORT; CHLOROQUINE; DRUG RESISTANCE; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM;

GOES; PLASMODIUM FALCIPARUM;

EID: 0030884415     PISSN: 00311820     EISSN: None     Source Type: Journal    
DOI: 10.1017/s0031182097008974     Document Type: Article

References (96)

1. ADAGU, I. S., WARHURST, D. C., CARUCCI, D. J. & DURAISINGH, M. T. (1995). Pfmdr1 mutations and chloroquine-resistance in Plasmodium falciparum isolates from Zaire, Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 132.
2. 3H chloroquine. American Journal of Pathology 67, 277-280.
3. ANAND, N. (1984). Chemotherapy of malaria. In Proceedings of the Indo-UK Workshop on Malaria (ed. Sharma, V. P.). New Delhi, Malaria Research Centre (ICMR)
4. AWAD-EL-KARIEM, F. M., MILES, M. A. & WARHURST, D. C. (1992). Chloroquine-resistant Plasmodium falciparum isolates from Sudan lack two mutations in the pfmdr1 gene thought to be associated with chloroquine-resistance. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 587-589.
5. BARNES, D. A., FOOTE, S. J., GALATIS, D., KEMP, D. J. & COWMAN, A. F. (1992). Selection for high-level chloroquine resistance results in deamplification of the pfmdr1 gene and increased sensitivity to mefloquine in Plasmodium falciparum. EMBO Journal 11, 3067-3075.
6. BASCO, L. K., LE BRAS, J., RHOADES, Z. & WILSON, C. M. (1995). Analysis of pfmdr1 and drug susceptibility in fresh isolates of Plasmodium falciparum from subsaharan Africa. Molecular and Biochemical Parasitology 74, 157-166.
7. BASCO, L. K., PECOULAS, P. E., LE BRAS, J. & WILSON, C. M. (1996). Plasmodium falciparum: molecular characterization of multi-drug resistant Cambodian isolates. Experimental Parasitology 82, 97-103.
8. BRAY, P. G., BOULTER, M. K., RITCHIE, G. Y. & WARD, S. A. (1994). Relationship of global chloroquine transport and reversal of chloroquine resistance in P. falciparum. Molecular and Biochemical Parasitology 63, 87-94.
9. BRAY, P. G., HAWLEY, S. R., MUNGTHIN, M. & WARD, S. A. (1996a). Physicochemical properties correlated with drug resistance and the reversa! of drug resistance in Plasmodium falciparum. Molecular Pharmacology 50, 1559-1566.
10. BRAY, P. G., HAWLEY, S. R. & WARD, S. A. (1996b). 4-aminoquinoline resistance in Plasmodium falciparum: insights from the study of amodiaquine uptake. Molecular Pharmacology 50, 1551-1558.
11. BRAY, P. G., HOWELLS, R. E., RITCHIE, G. Y. & WARD, S. A. (1992a). Rapid chloroquine efflux phenotype in both chloroquine-sensitive and chloroquine-resistant Plasmodium falciparum. Biochemical Pharmacology 44, 1317-1324.
12. BRAY, P. G., HOWELLS, R. E. & WARD, S. A. (1992b). Vacuolar acidification and chloroquine sensitivity in Plasmodium falciparum. Biochemical Pharmacology 43, 1219-1227.
13. BROOKS, D. R., WANG, P., READ, M., WATKINS, W. M., SIMS, P. F. & HYDE, J. E. (1994). Sequence variation of the hydroxymethyldihydropterin pyrophosphokinase dihydropteroate synthetase gene in lines of the human malaria parasite, Plasmodium falciparum with differing resistance to sulphadoxine. European Journal of Biochemistry 224, 397-405.
14. BRUCE-CHWATT, L. J., BLACK, R. H., CANFIELD, C. J., CLYDE, D. F., PETERS, W. & WERNSDORFER, W. H. (1986). Chemotherapy of Malaria, revised 2nd edition. Geneva, World Health Organisation.
15. CHOI, I. & MEGO, J. L. (1988). Purification of Plasmodium falciparum digestive vacuoles and partial characterisation of the vacuolar membrane ATPase. Molecular and Biochemical Parasitology 31, 71-78.
16. CHOU, A. C., CHEVLI, R. & FITCH, C. D. (1980). Ferriprotoporphyrin IX fulfils the criteria for identification as the chloroquine receptor of malaria parasites. Biochemistry 19, 1543-1549.
17. CHOU, A. C. & FITCH, C. D. (1992). Heme polymerase: modulation by chloroquine treatment of a rodent malaria. Life Sciences 51, 2037-2078.
18. COATNEY, G. R. (1963). Pitfalls in a discovery: the chronicle of chloroquine. American Journal of Tropical Medicine and Hygiene 12, 121-128.
19. COWMAN, A. F., GALATIS, D. & THOMPSON, J. K. (1994). Selection for mefloquine resistance in Plasmodium falciparium is linked to amplifiction of the pfmdr1 gene and cross-resistance to halofantrine and quinine. Proceedings of the National Academy of Sciences, USA 91, 1143-1147.
20. COWMAN, A. F., KARCZ, S., GALATIS, D. & CULVENOR, J. G. (1991). A P-glycoprotein homologue of Plasmodium falciparum is localised on the digestive vacuole. Journal of Cell Biology 113, 1033-1045.
21. DE DUVE, C. (1963). General properties of lysosomes: the lysosome concept. In CIBA Foundation Symposium on Lysosomes (ed. De Rueck, A. V. S. & Cameron, M. P.), pp. 1-31. Boston, USA, Little, Brown.
22. DE DUVE, C., DE BARSY, T., POOLE, B., TROUET, A., TULKENS, P. & VAN HOOF, F. (1974). Lysosomotropic agents. Biochemical Pharmacology 23, 2495-2531.
23. DIRIBE, C. O. & WARHURST, D. C. (1985). A study of the uptake of chloroquine in malaria-infected erythrocytes. Biochemical Pharmacology 34, 3019-3027.
24. DORN, A., STOFFEL, R., MATILE, H., BUBENDORF, A. & RIDLEY, R. G. (1995). Malarial haemozoin/β-haematin supports haem polymerisation in the absence of protein. Nature 374, 269-271.
25. EGAN, T. J., ROSS, D. C. & ADAMS, P. A. (1994). Quinoline anti-malarial drugs inhibit spontaneous formation of β-haematin (malaria pigment). FEBS Letters 352, 54-57.
26. EKONG, R. M., ROBSON, K. J. H., BAKER, D. A. & WARHURST, D. C. (1993). Transcripts of multidrug resistance genes in chloroquine-sensitive and chloroquine-resistant Plasmodium falciparum. Parasitology 106, 107-115.
27. FERRARI, V. & CUTLER, D. J. (1990). Uptake of chloroquine by human erythrocytes. Biochemical Pharmacology 39, 753-762.
28. FITCH, C. D. (1969). Chloroquine resistance in malaria: a deficiency of chloroquine binding. Proceedings of the National Academy of Sciences, USA 64, 1181-1187.
29. FITCH, C. D. (1970). Plasmodium falciparum in owl monkeys. Drug resistance and chloroquine binding capacity. Science 169, 289-290.
30. FITCH, C. D. (1983). Mode of action of antimalarial drugs. In Malaria and the Red Cell (ed. Evered, D. & Whelan, J.). Ciba Foundation Symposium. Pitman, London. 94, 222-232.
31. FITCH, C. D., CHEVLI, R. & GONZALEZ, Y. (1974a). Chloroquine resistant Plasmodium falciparum: effect of substrate on chloroquine and amodiaquine accumulation. Antimicrobial Agents and Chemotherapy 6, 757-762.
32. FITCH, C. D., YUNIS, N. G., CHEVLI, R. & GONZALEZ, Y. (1974b). High-affinity accumulation of chloroquine by mouse erythrocytes infected with Plasmodium berghei. Journal of Clinical Investigation 54, 24-33.
33. FOJO, A. T., AIKIYAMA, S., GOTTESMAN, M. M. & PASTAN, I. (1985). Reduced drug accumulation in mutliple drug-resistant human KB carcinoma cells lines. Cancer Research 45, 3002-3007.
34. FOLEY, M., DEADY, L. W., NG, K., COWMAN, A. F. & TILLEY, L. (1994). Photoaffinity labelling of chloroquine-binding proteins in Plasmodium falciparum. Journal of Biological Chemistry 269, 6955-6961.
35. FOOTE, S. J., KYLE, D. E., MARTIN, R. K., ODUOLA, A. M. J., FORSYTH, K., KEMP, D. J. & COWMAN, A. F. (1990). Several alleles of the multidrug resistance gene are closely linked to chloroquine resistance in Plasmodium falciparum. Nature 345, 255-258.
36. FOOTE, S. J., THOMPSON, J. K., COWMAN, A. F. & KEMP, D. J. (1989). Amplification of the multidrug resistance gene in some chloroquine resistant isolates of Plasmodium falciparum. Cell 57, 921-930.
37. GEARY, T. G., DIVO, A. D. & JENSEN, J. B. (1987). Activity of quinoline-containing antimalarials against chloroquine sensitive and resistant strains of Plasmodium falciparum in vitro. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 499-503.
38. GEARY, T. G., DIVO, A. D., JENSEN, J. B., ZANGWILL, M. & GINSBURG, H. (1990). Kinetic modelling of the response of Plasmodium falciparum to chloroquine and its experimental testing in vitro. Implications for mechanism of action and resistance to the drug. Biochemical Pharmacology 40, 685-691.
39. 3H chloroquine by drug sensitive and resistant strains of the human malarial parasite Plasmodium falciparum. Biochemical Pharmacology 35, 3805-3812.
40. GINSBURG, H. & GEARY, T. G. (1987). Current concepts and new ideas on the mechanism of action of quinoline containing antimalarials. Biochemical Pharmacology 40, 1567-1576.
41. GINSBURG, H. & KRUGLIAK, M. (1992). Quinoline-containing antimalarials, mode of action, drug resistance and its reversal. An update with unresolved puzzles. Biochemical Pharmacology 43, 63-70.
42. GINSBURG, H., NISSANI, E. & KRUGLIAK, M. (1989). Alkalinisation of the food vacuole of malaria parasites by quinoline containing drugs and alkylamines is not correlated with their antimalarial activity. Biochemical Pharmacology 38, 2645-2654.
43. GINSBURG, H. & STEIN, W. D. (1991). Kinetic modelling of chloroquine uptake by malaria infected erythrocytes. Biochemical Pharmacology 41, 1463-1470.
44. GOTTESMAN, M. M. & PASTAN, I. (1993). Biochemistry of multidrug resistance mediated by the multidrug transporter. Annual Review of Biochemistry 62, 385-427.
45. HARUKI, K., BRAY, P. G., WARD, S. A., HOMMEL, M. & RITCHIE, G. Y. (1994). Chloroquine resistance in Plasmodium falciparum: further evidence for a lack of association with mutations of the pfmdr1 gene. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 694.
46. HAWLEY, S. R., BRAY, P. G., O'NEILL, P. M., NAISBITT, D. J., PARK, B. K. & WARD, S. A. (1996b). Manipulation of the N-alkyl substituent of amodiaquine to overcome the verapamil sensitive chloroquine resistance component. Antimicrobial Agents and Chemotherapy 40, 2345-2349.
47. HAWLEY, S. R., BRAY, P. G., PARK, B. K. & WARD, S. A. (1996a). Amodiaquine accumulation in Plasmodium falciparum as a possible explanation for its superior antimalarial activity over chloroquine. Molecular and Biochemical Parasitology 52, 723-733.
48. HOMEWOOD, C. A., WARHURST, D. C., PETERS, W. & BAGGALEY, V. C. (1972). Lysosomes, pH and the antimalarial action of chloroquine. Nature 235, 50-52.
49. HYDE, J. E. (1990). The dihydrofolate reductase thymidylate synthetase gene in the drug resistance of malaria parasites. Pharmacology and Therapeutics 48, 45-59.
50. KARCZ, S., CAPPAI, R., HANDMAN, E. & COWMAN, A. F. (1993a). Altered sensitivity to antimalarial drugs in Leishmania expressing a Plasmodium falciparium P-glycoprotein homologue. Resistance against anticancer drugs: molecular mechanisms and clinical opportunities. General Motors Cancer Research Foundation, Toronto Abstract F8.
51. KARCZ, S. R., HERRMANN, V. R. & COWMAN, A. F. (1993b). Cloning and characterisation of a vacuolar ATPase A subunit homologue from Plasmodium falciparum. Molecular and Biochemical Parasitology 58, 333-334.
52. KARCZ, S. R., HERRMANN, V. R., TROTTEIN, F. & COWMAN, A. F. (1994). Cloning and characterisation of the vacuolar ATPase B sub-unit from Plasmodium falciparum. Molecular and Biochemical Pharmacology 65, 123-133.
53. KROGSTAD, D. J., GLUZMAN, I. Y., HERWALDT, L., SCHLESINGER, P. H. & WELLEMS, T. E. (1992). Energy dependence of chloroquine accumulation and chloroquine efflux in Plasmodium falciparum. Biochemical Pharmacology 43, 57-62.
54. KROGSTAD, D. J., GLUZMAN, I. Y., KYLE, D. E., ODUOLA, A. M. J., MARTIN, S. K., MILHOUS, W. K. & SCHLESINGER, P. H. (1987). Efflux of chloroquine from Plasmodium falciparum: mechanism of chloroquine resistance. Science 235, 1283-1285.
55. KROGSTAD, D. J. & SCHLESINGER, P. H. (1987). The basis of antimalarial action: non weak base effects of chloroquine on acid vesicle pH. American Journal of Tropical Medicine and Hygiene 36, 213-220.
56. KROGSTAD, D. J., SCHLESINGER, P. H. & GLUZMAN, I. Y. (1985). Antimalarials increase vesicle pH in Plasmodium falciparum. Journal of Cell Biology 101, 2302-2309.
57. MACOMBER, P. B., O'BRIEN, R. L. & HAHN, F. E. (1966). Chloroquine: physiological basis of drug resistance in Plasmodium berghei. Science 152, 1374-1375.
58. MACOMBER, P. B., SPRINZ, H. & TOUSIMIS, A. J. (1967). Morphological effects of chloroquine on Plasmodium berghei in mice. Nature 214, 937-939.
59. MARTIN, S. K., ODUOLA, A. M. J. & MILHOUS, W. K. (1987). Reversal of chloroquine resistance in Plasmodium falciparum by verapamil. Science 235, 899-901.
60. MARTINEY, J. A., CERAMI, A. & SLATER, A. F. G. (1995). Verapamil reversal of chloroquine resistance in the malaria parasite Plasmodium falciparum is specific for resistant parasites and independent of the weak base effect. Journal of Biological Chemistry 270, 22393-22398.
61. NATEGHPOUR, M., WARD, S. A. & HOWELLS, R. E. (1993). Development of halofantrine resistance and determination of cross-resistance patterns in Plasmodium falciparum. Antimicrobial Agents and Chemotherapy 37, 2337-2343.
62. ODUOLA, A. M. J., MILHOUS, W., SALAKO, L. A., WALKER, O. & DESJARDINS, R. E. (1987). Reduced in vitro susceptibility to mefloquine in West African isolates of Plasmodium falciparum. Lancet 2, 1304-1305.
63. ORJIH, A. U. & FITCH, C. D. (1993). Hemozoin production by Plasmodium falciparum: variation with strain and exposure to chloroquine. Biochimica et Biophysica Acta 1157, 270-274.
64. PEEL, S. A., BRIGHT, P., YOUNT, B., HANDY, J. & BARIC, R. S. (1994). A strong association between mefloquine and halofantrine resistance and amplification, overexpression, and mutation in the P-glycoprotein gene homologue (pfmdr1) of Plasmodium falciparum. American Journal of Tropical Medicine and Hygiene 51, 648-658.
65. PETERS, W. (1969). Drug resistance in malaria - a perspective. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 25-45.
66. PETERS, W. (1980). Chemotherapy of malaria. In Malaria, Vol. I (ed. Kreier, J. P.), pp. 145-283. New York, Academic Press.
67. PETERS, W. (1987). Chemotherapy and Drug Resistance in Malaria, 2nd edn. London, Academic Press.
68. PETERS, W., ROBINSON, B. L. & MILHOUS, W. K. (1993). The chemotherapy of rodent malaria. LI. Studies on a new 8-aminoquinoline, WR 238,605. Annals of Tropical Medicine and Parasitology 87, 547-552.
69. 3H by Plasmodium knowlesi in vitro. Journal of Pharmacology and Experimental Therapeutics 168, 187-192.
70. RITCHIE, G. Y., MUNGTHIN, M., GREEN, J. E., BRAY, P. G., HAWLEY, S. R. & WARD, S. A. (1996). In vitro selection of halofantrine resistance in Plasmodium falciparum is not correlated with amplification of pfmdr1 or overexpression of Pgh1. Molecular and Biochemical Parasitology 83, 35-46.
71. ROGAN, A. M., HAMILTON, T. C., YOUNG, R. C., KLECKER, R. W., JR. & OZOLS, R. F. (1984). Reversal of adriamycin resistance by verapamil in human ovarian cancer. Science 244, 994-996.
72. ROSENTHAL, P. J., MCKERROW, J. H., AIKAWA, M., NAGASAWA, H. & LEECH, J. H. (1988). A malarial cysteine protease is necessary for haemoglobin degradation by Plasmodium falciparum. Journal of Clinical Investigation 82, 1560-1566.
73. RUBIO, J. P. & COWMAN, A. F. (1996). The ATP-binding cassette (ABC) gene family of Plasmodium falciparum. Parasitology Today 12, 135-140.
74. SLATER, A. F. G. (1993). Chloroquine: mechanism of drug action and resistance in Plasmodium falciparum. Pharmacology and Therapeutics 57, 203-236.
75. SLATER, A. F. G. & CERAMI, A. (1992). Inhibition by chloroquine of a novel haeme polymerase enzyme activity in malaria trophozoites. Nature 355, 167-169.
76. THAITHONG, S., BEALE, G. K. & CHUTMONGKONKUL, M. (1983). Susceptibility of Plasmodium falciparum to five drugs : an in vitro study of isolates mainly from Thailand. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 228-231.
77. VAN ES, H. H. G., KARCZ, S., COWMAN, A., GROS, P. & SCHURR, E. (1993). CHO cells expressing the pfmdr1. gene show altered chloroquine uptake characteristics. Resistance against anticancer drugs: molecular mechanisms and clinical opportunities. General Motors Cancer Research Foundation, Toronto, Abstract F14.
78. VAN ES, H. H. G., KARCZ, S., CHU, F., COWMAN, A. F., VIDAL, S., GROS, P. & SCHURR, E. (1994a). Expression of the plasmodial pfmdr1 gene in mammalian cells is associated with increased susceptibility to chloroquine. Molecular Cell Biology 14, 2149-2428.
79. VAN ES, H. H. G., RENKEMA, H., AERTS, H. & SCHURR, E. (1994b). Enhanced lysosomal acidification leads to increased chloroquine accumulation in CHO cells expressing the pfmdr1 gene. Molecular and Biochemical Parasitology 68, 209-215.
80. VERDIER, F., LE BRAS, J., CLAVIER, F., HATIN, I. & BLAYO, M. (1985). Chloroquine uptake by Plasmodium falciparum-infected human erythrocytes during in vitro culture and its relationshiop to chloroquine resistance. Antimicrobial Agents and Chemotherapy 27, 561-564.
81. WARD, S. A. (1988). Mechanisms of chloroquine resistance in malarial chemotherapy. TIPS 9, 241-246.
82. WELLEMS, T. E., PANTON, L. J., GLUZMAN, I. Y., DE ROSARIO, V. E., GWADZ, R. W., WALKER-JONAH, A. & KROGSTAD, D. J. (1990). Chloroquine resistance not linked to mdr-like gene in a Plasmodium falciparium cross. Nature 345, 253-255.
83. WELLEMS, T. E., WALKER-JONAH, A. & PANTON, L. J. (1991). Genetic mapping of the chloroquine resistance locus on Plasmodium falciparum chromosome 7. Proceedings of the National Academy of Sciences, USA 88, 3382-3386.
84. WERNSDORFER, W. H. (1984). Drug resistant malaria. Endeavour 8, 166-171.
85. WHO (1984). Advances in malaria chemotherapy. WHO Technical Report Series No. 711. World Health Organisation, Geneva.
86. WHO (1989). World malaria situation 1986-1987. Weekly Epidemiological Record 64, 241-254.
87. WILSON, C. M., SERRANO, A. E., WASLEY, A., BOGENSHUTZ, M. P., SHANKAR, A. H. & WIRTH, D. F. (1989). Amplification of a gene related to mammalian mdr genes in drug resistant P. falciparum. Science 244, 1184-1186.
88. WILSON, C. M., VOLKMAN, S. K., THAITHONG, S., MARTIN, S. K., KYLE, D. E., MILHOUS, W. K. & WIRTH, D. F. (1993). Amplification of pfmdr1 associated with mefloquine and halofantrine resistance in Plasmodium falciparum from Thailand. Molecular and Biochemical Parasitology 57, 151-160.
89. YAYON, A., CABANTCHIK, Z. I. & GINSBURG, H. (1984). Identification of the acidic compartment of Plasmodium falciparum-infected human erythrocytes as the target of the antimalarial drug chloroquine. EMBO Journal 3, 2695-2700.
90. YAYON, A., CABANTCHIK, Z. I. & GINSBURG, H. (1985). Susceptibility of human malaria parasites to chloroquine is pH dependent. Proceedings of the National Academy of Sciences, USA 82, 2784-2788.
91. YAYON, A. & GINSBURG, H. (1982). The transport of chloroquine across human erythrocyte membranes is mediated by a simple symmetric carrier. Biochimica et Biophysica Acta 686, 197-203.
92. YAYON, A. & GINSBURG, H. (1983). Chloroquine inhibits the degradation of endocytic vesicles in human malaria parasites. Cell Biology International Reports 7, 895-901.
93. ZALIS, M. G., WILSON, C. M., ZHANG, Y. & WIRTH, D. F. (1993). Characterisation of the pfmdr2 gene for Plasmodium falciparum. Molecular and Biochemical Parasitology 62, 83-93.
94. ZARCHIN, S., KRUGLIAK, M. & GINSBURG, H. (1986). Digestion of the host erythrocyte by malarial parasites is the primary target for quinoline-containing antimalarials. Biochemical Pharmacology 35, 2435-2442.
95. ZHANG, Y. & HEMPLEMAN, J. (1987). Lysis of malaia parasites and erythrocytes by FPIX-chloroquine and the inhibition of this effect by proteins. Biochemical Pharmacology 36, 1267-1273.
96. ZHANG, Y. & JUST, W. W. (1987). A comparative study on the effect of chloroquine and ammonium chloride on the feeding process of Plasmodium falciparum in vitro. Parasitology Research 73, 475-478.