Linkage disequilibrium between two chromosomally distinct loci associated with increased resistance to chloroquine in Plasmodium falciparum

Parasitology

Volumn 121, Issue 1, 2000, Pages 1-7

  Duraisingh, M T ^a,b   Von Seidlein, L ^b   Jepson, A ^b   Jones, P ^b   Sambou, I ^b   Pinder, M ^b   Warhurst, D C ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

Author keywords

cg2; Chloroquine; dhfr; Linkage disequilibrium; msp2; pfmdr1; Plasmodium falciparum

Indexed keywords

ANTIMALARIAL AGENT; CHLOROQUINE;

ALLELE; ANTIMALARIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG RESISTANCE; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENE MAPPING; GENETIC POLYMORPHISM; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

ANIMALS; ANTIMALARIALS; ATP-BINDING CASSETTE TRANSPORTERS; CHLOROQUINE; DRUG RESISTANCE; GENES, PROTOZOAN; HUMANS; LINKAGE DISEQUILIBRIUM; MALARIA, FALCIPARUM; PARASITIC SENSITIVITY TESTS; PLASMODIUM FALCIPARUM; POLYMORPHISM, GENETIC; PROTOZOAN PROTEINS;

PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 0002745249     PISSN: 00311820     EISSN: None     Source Type: Journal    
DOI: 10.1017/S0031182099006022     Document Type: Article

References (50)

1. ADAGU, I. S., WARHURST, D. C., OGALA, W. N., ABDU-AGUYE, I., AUDU, L. I., BAMGBOLA, F. O. & OVWIGHO, U. B. (1995a). Antimalarial drug response of Plasmodium falciparum from Zaria, Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 422-425.
2. ADAGU, I. S., WARHURST, D. C., CARUCCI, D. J. & DURAISINGH, M. T. (1995b). Pfmdr1 mutations and chloroquine-resistance in Plasmodium falciparum isolates from Zaria, Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 132.
3. ADAGU, I. S., DIAS, F., PINHEIRO, L., ROMBO, L., DOROSARIO, V. & WARHURST, D. C. (1996). Guinea Bissau: association of chloroquine resistance of Plasmodium falciparum with the Tyr86 allele of the multiple drug-resistance gene pfmdr1. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 90-91.
4. AWAD EL KARIEM, F. M., MILES, M. A. & WARHURST, D. C. (1992). Chloroquine-resistant Plasmodium falciparum isolates from the 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. BABIKER, H. A., RANFORD-CARTWRIGHT, L. C., CURRIE, D., CHARLWOOD, J. D., BILLINGSLEY, P., TEUSCHER, T. & WALLIKER, D. (1994). Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology 109, 413-421.
6. BASCO, L. K., ELDIN DE PECOULAS, P., LE BRAS, J. & WILSON, C. M. (1996). Plasmodium falciparum: Molecular characterisation of multidrug-resistant Cambodian isolates. Experimental Parasitology 82, 97-103.
7. 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.
8. BASCO, L. K. & RINGWALD, P. (1998). Molecular epidemiology of malaria in Yaounde, Cameroon. Analysis of chloroquine resistance and point mutations in the multidrug resistance (pfmdr1) gene of Plasmodium falciparum. American Journal of Tropical Medicine and Hygiene 59, 577-581.
9. BRAY, P. G., MUNGTHIN, M., RIDLEY, R. G. & WARD, S. A. (1998). Access to hematin: the basis of chloroquine resistance. Molecular Pharmacology 54, 170-179.
10. CARTER, R. & MCGREGOR, I. A. (1973). Enzyme variation in Plasmodium falciparum in the Gambia. Transactions of the Royal Society of Tropical Medicine and Hygiene 7, 830-837.
11. CARTER, R. & VOLLER, A. (1975). The distribution of enzyme variation in populations of Plasmodium falciparum in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 69, 371-376.
12. CASSOL, S., SALAS, T., GILL, M. J., MONTPETIT, M., RUDNIK, J., SY, C. T. & O'SHAUGHNESSY, M. V. (1992). Stability of dried blood spot specimens for detection of human immunodeficiency virus DNA by polymerase chain reaction. Journal of Clinical Microbiology 30, 3039-3042.
13. CONWAY, D. J. (1995). Natural selection on polymorphic malaria antigens and the search for a vaccine. Parasitology Today 13, 26-29.
14. CONWAY, D. J., GREENWOOD, B. M. & MCBRIDE, J. S. (1992). Longitudinal study of Plasmodium falciparum polymorphic antigens in a malaria-endemic population. Infection and Immunity 60, 1122-1127.
15. CONWAY, D. J. & MCBRIDE, J. S. (1991). Population genetics of Plasmodium falciparum within a malaria hyperendemic area. Parasitology 103, 7-16.
16. CONWAY, D. J., ROPER, C., ODUOLA, A. M., ARNOT, D. E., KREMSNER, P. G., GROBUSCH, M. P., CURTIS, C. F. & GREENWOOD, B. M. (1999). High recombination rate in natural populations of Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 96, 4506-4511.
17. DURAISINGH, M. T., DRAKELEY, C. J., MULLER, O., BAILEY, R., SNOUNOU, G., TARGETT, G. A., GREENWOOD, B. M. & WARHURST, D. C. (1997). Evidence for selection for the tyrosine-86 allele of the pfmdr1 gene of Plasmodium falciparum by chloroquine and amodiaquine. Parasitology 114, 205-211.
18. DURAISINGH, M. T., CURTIS, J. & WARHURST, D. C. (1998). Plasmodium falciparum: detection of polymorphisms in the dihydrofolate reductase and dihydropteroate synthase genes by PCR and restriction digestion. Experimental Parasitology 89, 1-8.
19. DURAISINGH, M. T., JONES, P., SAMBOU, I., VON SEIDLEIN, L., PINDER, M. & WARHURST, D. C. (1999). Inoculum effect leads to overestimation of in vitro resistance for artemisinin derivatives and standard antimalarials: a Gambian field study. Parasitology 119, 435-440.
20. DURAND, R., GABBETT, E., DI PIAZZA, J.-P., DELABRE, J.-F. & LE BRAS, J. (1999). Analysis of Kappa and Omega repeats of the cg2 gene and chloroquine susceptibility in isolates of Plasmodium falciparum from sub-saharan Africa. Molecular and Biochemical Parasitology 101, 185-197.
21. DYE, C. & WILLIAMS, B. G. (1997). Multigenic drug resistance among inbred malaria parasites. Proceedings of the Royal Society of London, B 264, 61-67.
22. FOOTE, S. J., KYLE, D. E., MARTIN, R. K., ODUOLA, A. M., 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, London 345, 255-258.
23. GARNHAM, P. C. C. (1966). Malaria Parasites and other Haemosporidia. Blackwell Scientific Publications, London.
24. GOLDBERG, D. E., SHARMA, V., OKSMAN, A., GLUZMAN, I. Y., WELLEMS, T. E. & PIWNICA-WORMS, D. (1997). Probing the chloroquine resistance locus of Plasmodium falciparum with a novel class of multidentate metal(III) coordination complexes. Journal of Biological Chemistry 272, 6567-6572.
25. HASTINGS, I. M. & MACKINNON, M. J. (1998). The emergence of drug-resistant malaria. Parasitology 117, 411-417.
26. HELLGREN, U., ERICSSON, O., KIHAMIA, C. M. & ROMBO, L. (1994). Malaria parasites and chloroquine concentrations in Tanzanian schoolchildren. Tropical Medicine and Parasitology 45, 293-297.
27. HILL, W. G. & ROBERTSON, A. (1968). The effects of inbreeding at loci with heterozygote advantage. Genetics 60, 615-628.
28. MACKINNON, M. J. (1997). Survival probability of drug resistant mutants in malaria parasites. Proceedings of the Royal Society of London, B 264, 53-59.
29. MAYNARD-SMITH, J. (1989). Evolutionary Genetics. Oxford University Press, Oxford.
30. MAXWELL, C. A., MYAMBA, J., NJUNWA, K. J., GREENWOOD, B. M. & CURTIS, C. F. (1999). Comparison of bednets impregnated with different pyrethroids for their impact on mosquitoes and on re-infection with malaria after clearance of pre-existing infections with chlorproguanil-dapsone. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 4-11.
31. MENON, A., SNOW, R. W., OTOO, L. & GREENWOOD, B. M. (1987). Decline in the sensitivity of Plasmodium falciparum to chloroquine in the Gambia. Lancet 1, 1029-1039.
32. MENON, A., OTOO, L. N., HERBAGE, E. A. & GREENWOOD, B. M. (1990). A national survey of the prevalence of chloroquine resistant Plasmodium falciparum in The Gambia. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 638-640.
33. MULLER, O., VAN HENSBROEK, M. B., JAFFAR, S., DRAKELEY, C., OKORIE, C., JOOF, D., PINDER, M. & GREENWOOD, B. M. (1996). A randomised trial of chloroquine, amodiaquine and pyrimethamine-sulfadoxine in Gambian children with uncomplicated malaria. Tropical Medicine and International Health 1, 124-132.
34. ODUOLA, A. M., SOWUNMI, A., MILHOUS, W. K., BREWER, T. G., KYLE, D. E., GERENA, L., ROSSAN, R. N., SALAKO, L. A. & SCHUSTER, B. G. (1998). In vitro and in vivo reversal of chloroquine resistance in Plasmodium falciparum with promethazine. American Journal of Tropical Medicine and Hygiene 58, 625-629.
35. O'NEILL, M. J., BRAY, D. H., BOARDMAN, P., PHILLIPSON, J. D. & WARHURST, D. C. (1985). Plants as sources of antimalarial drugs. Part 1. In vitro test method for the evaluation of crude extracts from plants. Planta Medica 1985, 394-398.
36. PANTON, L. J., TULLOCH, S., BRADLEY, A. K. & GREENWOOD, B. M. (1985). Susceptibility of Plasmodium falciparum in The Gambia to pyrimethamine, Maloprim and chloroquine. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 484-490.
37. PAUL, R. E., PACKER, M. J., WALMSLEY, M., LAGOG, M., RANFORD-CARTWRIGHT, L. C., PARU, R. & DAY, K. P. (1995). Mating patterns in malaria parasite populations of Papua New Guinea. Science 269, 1709-1711.
38. PETERSON, D. S., MILHOUS, W. K. & WELLEMS, T. E. (1990). Molecular basis of differential resistance to cycloguanil and pyrimethamine in Plasmodium falciparum malaria. Proceedings of the National Academy of Sciences, USA 87, 3018-3022.
39. PONNUDURAI, T., LEEUWENBERG, A. D. & MEUWISSEN, J. H. (1981). Chloroquine sensitivity of isolates of Plasmodium falciparum adapted to in vitro culture. Tropical and Geographical Medicine 33, 50-54.
40. SU, X., KIRKMAN, L. A., FUJIOKA, H. & WELLEMS, T. E. (1997). Complex polymorphisms in an approximately 330 kDa protein are linked to chloroquine-resistant P. falciparum in Southeast Asia and Africa. Cell 91, 593-603.
41. THOMSON, M. C., D'ALESSANDRO, U., BENNETT, S., CONNOR, S. J., LANGEROCK, P., JAWAR, M., TODD, J. & GREENWOOD, B. M. (1994). Malaria prevalence is inversely related to vector density in the Gambia, West Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 638-643.
42. 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 and Cellular Biology 14, 2419-2428.
43. VAN ES, H. H., 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, 209-219.
44. VAN NIEROP, W. H., FREAN, J. A. & MARKUS, M. B. (1999). Comparison of in vitro chloroquine sensitivity testing with detection of pfmdr1 point mutations in Plasmodium falciparum. South African Journal of Science 95, 133-137.
45. VIRIYAKOSOL, S., SIRIPOON, N., PETCHARAPIRAT, C., PETCHARAPIRAT, P., JARRA, W., THAITHONG, S., BROWN, K. N. & SNOUNOU, G. (1995). Genotyping of Plasmodium falciparum isolates by the polymerase chain reaction and potential uses in epidemiological studies. Bulletin of the World Health Organization 93, 85-95.
46. VON SEIDLEIN, L., DURAISINGH, M. T., DRAKELEY, C. J., BAILEY, R., GREENWOOD, B. M. & PINDER, M. (1997). Polymorphism of the pfmdr1 gene and chloroquine resistance in Plasmodium falciparum in The Gambia. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 450-453.
47. VOLKMAN, S. K., WOODCOCK, S., COWMAN, A. F. & WIRTH, D. F. (1995). Functional complementation of the ste6 gene of Saccharomyces cerevisiae with the pfmdr1 gene of Plasmodium falciparum. Proceedings of the National Academy of Sciences 92, 8921-8925.
48. WELLEMS, T. E., PANTON, L. J., GLUZMAN, I. Y., DO ROSARIO, V. E., GWADZ, R. W. & WALKER-JONAH, A. (1990). Chloroquine resistance not linked to mdr-like genes in a Plasmodium falciparum cross. Nature, London 345, 253-255.
49. WILSON, C. M., VOLKMAN, S. K., THAITHONG, S., MARTIN, R. 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.
50. WUNSCH, S., SANCHEZ, C. P., GEKLE, M., GROSSE-WORTMANN, L., WIESNER, J. & LANZER, M. (1998). Differential stimulation of the Na+/H+ exchanger determines chloroquine uptake in Plasmodium falciparum. Journal of Cell Biology 140, 335-345.