Evidence that mutant PfCRT facilitates the transmission to mosquitoes of chloroquine-treated Plasmodium gametocytes

Journal of Infectious Diseases

Volumn 203, Issue 2, 2011, Pages 228-236

  Ecker, Andrea ^a   Lakshmanan, Viswanathan ^b   Sinnis, Photini ^c   Coppens, Isabelle ^d   Fidock, David A ^a  

^a NewYork Presbyterian Hospital   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMALARIAL DRUG RESISTANCE; ANTIMALARIAL DRUG SUSCEPTIBILITY; ARTICLE; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; GAMETOCYTE; GENE; GENE MUTATION; IN VIVO STUDY; MOSQUITO; MOUSE; MUTANT; NONHUMAN; PARASITE TRANSMISSION; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM CHLOROQUINE RESISTANCE TRANSPORTER GENE; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; ANTIMALARIALS; CHLOROQUINE; CULICIDAE; DISEASE MODELS, ANIMAL; DRUG RESISTANCE; FEMALE; MALARIA; MEMBRANE TRANSPORT PROTEINS; MICE; MUTATION, MISSENSE; PARASITIC SENSITIVITY TESTS; PLASMODIUM BERGHEI; PROTOZOAN PROTEINS; VIRULENCE;

EID: 79851482799     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jiq036     Document Type: Article

References (48)

1. Snow RW, Trape JF, Marsh K. The past, present and future of childhood malaria mortality in Africa. Trends Parasitol 2001; 17:593-7. (Pubitemid 34088120)
2. Fidock DA, Nomura T, Talley AK, et al. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT evidence for their role in chloroquine resistance. Mol Cell 2000; 6:861-71.
3. Sidhu AB, Verdier-Pinard D, Fidock DA. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 2002; 298:210-3.
4. Lakshmanan V, Bray PG, Verdier-Pinard D, et al. A critical role for PfCRT K76T in Plasmodium falciparum verapamil-reversible chloroquine resistance. EMBO J 2005; 24:2294-305. (Pubitemid 41032582)
5. Sanchez CP, McLean JE, Rohrbach P, Fidock DA, Stein WD, Lanzer M. Evidence for a pfcrt-associated chloroquine efflux system in the human malarial parasite Plasmodium falciparum. Biochemistry 2005; 44:9862-70. (Pubitemid 41033452)
6. Lehane AM, Kirk K. Chloroquine resistance-conferring mutations in pfcrt give rise to a chloroquine-associated H+ leak from the malaria parasite's digestive vacuole. Antimicrob Agents Chemother 2008; 52:4374-80.
7. Picot S, Olliaro P, de Monbrison F, Bienvenu AL, Price RN, Ringwald P. A systematic review and meta-analysis of evidence for correlation between molecular markers of parasite resistance and treatment outcome in falciparum malaria. Malar J 2009; 8:89.
8. Handunnetti SM, Gunewardena DM, Pathirana PP, Ekanayake K, Weerasinghe S, Mendis KN. Features of recrudescent chloroquine-resistant Plasmodium falciparum infections confer a survival advantage on parasites and have implications for disease control. Trans R Soc Trop Med Hyg 1996; 90:563-7. (Pubitemid 26356644)
9. Robert V, Awono-Ambene HP, Le Hesran JY, Trape JF. Gametocytemia and infectivity to mosquitoes of patients with uncomplicated Plasmodium falciparum malaria attacks treated with chloroquine or sulfadoxine plus pyrimethamine. Am J Trop Med Hyg 2000; 62:210-6. (Pubitemid 30257580)
10. Drakeley CJ, Jawara M, Targett GA, et al. Addition of artesunate to chloroquine for treatment of Plasmodium falciparum malaria in Gambian children causes a significant but short-lived reduction in infectiousness for mosquitoes. Trop Med Int Health 2004; 9:53-61. (Pubitemid 38178012)
11. Hallett RL, Sutherland CJ, Alexander N, et al. Combination therapy counteracts the enhanced transmission of drug-resistant malaria parasites to mosquitoes. Antimicrob Agents Chemother 2004; 48:3940-3. (Pubitemid 39304625)
12. Sinden RE. Gametocytogenesis of Plasmodium falciparum in vitro: ultrastructural observations on the lethal action of chloroquine. Ann Trop Med Parasitol 1982; 76:15-23. (Pubitemid 12150842)
13. Butcher GA. Antimalarial drugs the mosquito transmission of Plasmodium. Int J Parasitol 1997; 27:975-87. (Pubitemid 27423685)
14. Peters W, Chance ML, Lissner R, Momen H, Warhurst DC. The chemotherapy of rodent malaria, XXX. The enigmas of the "NS lines" of P. berghei. Ann Trop Med Parasitol 1978; 72:23-36.
15. Ramkaran AE, Peters W. Infectivity of chloroquine resistant Plasmodium berghei to Anopheles stephensi enhanced by chloroquine. Nature 1969; 223:635-6.
16. Ramkaran AE, Peters W. Action of chloroquine on infectivity of gametocytes of rodent malarias. Trans R Soc Trop Med Hyg 1970; 64:8.
17. Ichimori K, Curtis CF, Targett GA. The effects of chloroquine on the infectivity of chloroquine-sensitive and -resistant populations of Plasmodium yoelii nigeriensis to mosquitoes. Parasitology 1990; 00 (Pt 3);377-81.
18. Hogh B, Gamage-Mendis A, Butcher GA, et al. The differing impact of chloroquine pyrimethamine/sulfadoxine upon the infectivity of malaria species to the mosquito vector. Am J Trop Med Hyg 1998; 58:176-82. (Pubitemid 28096223)
19. Hunt P, Cravo PV, Donleavy P, Carlton JM, Walliker D. Chloroquine resistance in Plasmodium chabaudi: are chloroquine-resistance transporter (crt) and multi-drug resistance (mdr1) orthologues involved? Mol Biochem Parasitol 2004; 133:27-35. (Pubitemid 37510305)
20. Peters W. Drug resistance in Plasmodium berghei Vincke Lips, 1948. I. Chloroquine resistance. Exp Parasitol 1965; 17:80-9.
21. Hawking F. Chloroquine resistance in Plasmodium berghei. Am J Trop Med Hyg 1966; 15:287-93.
22. Macomber PB, O'Brien RL, Hahn FE. Chloroquine: physiological basis of drug resistance in Plasmodium berghei. Science 1966; 152:1374-5.
23. Macomber PB, Sprinz H, Tousimis AJ. Morphological effects of chloroquine on Plasmodium berghei in mice. Nature 1967; 214:937-9.
24. Janse CJ, Ramesar J, Waters AP. High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc 2006; 1:346-56.
25. Valderramos SG, Valderramos JC, Musset L, et al. Identification of a mutant PfCRT-mediated chloroquine tolerance phenotype in Plasmodium falciparum. PLoS Pathog 2010; 6:e10000887.
26. Folsch H, Pypaert M, Schu P, Mellman I. Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J Cell Biol 2001; 152:595-606. (Pubitemid 34280241)
27. Fidock DA, Nomura T, Wellems TE. Cycloguanil and its parent compound proguanil demonstrate distinct activities against Plasmodium falciparum malaria parasites transformed with human dihydrofolate reductase. Mol Pharmacol 1998; 54:1140-7. (Pubitemid 29002060)
28. Waller KL, Muhle RA, Ursos LM, et al. Chloroquine resistance modulated in vitro by expression levels of the Plasmodium falciparum chloroquine resistance transporter. J Biol Chem 2003; 278:33593-601. (Pubitemid 37055813)
29. Sa JM, Twu O, Hayton K, et al. Geographic patterns of Plasmodium falciparum drug resistance distinguished by differential responses to amodiaquine chloroquine. Proc Natl Acad Sci U S A 2009; 106:18883-9.
30. Beshir K, Sutherland CJ, Merinopoulos I, et al. Amodiaquine resistance in Plasmodium falciparum malaria in Afghanistan is associated with the pfcrtSVMNT allele at 72 to 76. Antimicrob Agents Chemother 2010; 54:3714-6.
31. van Dijk MR, Waters AP, Janse CJ. Stable transfection of malaria parasite blood stages. Science 1995; 268:1358-62.
32. Gautret P, Landau I, Tailhardat L, et al. The effects of subcurative doses of chloroquine on Plasmodium vinckei petteri gametocytes on their infectivity to mosquitoes. Int J Parasitol 2000; 30:1193-8.
33. Cheesman S, Creasey A, Degnan K, et al. Validation of pyrosequencing for accurate high throughput estimation of allele frequencies in malaria parasites. Mol Biochem Parasitol 2007; 152:213-9. (Pubitemid 46335719)
34. Sutherland CJ, Alloueche A, Curtis J, et al. Gambian children successfully treated with chloroquine can harbor transmit Plasmodium falciparum gametocytes carrying resistance genes. Am J Trop Med Hyg 2002; 67:578-85. (Pubitemid 36014913)
35. Wongsrichanalai C, Pickard AL, Wernsdorfer WH, Meshnick SR. Epidemiology of drug-resistant malaria. Lancet Infect Dis 2002; 2:209-18. (Pubitemid 34464751)
36. Kublin JG, Cortese JF, Njunju EM, et al. Reemergence of chloroquine-sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J Infect Dis 2003; 187:1870-5. (Pubitemid 36724485)
37. Ord R, Alexander N, Dunyo S, et al. Seasonal carriage of pfcrt pfmdr1 alleles in Gambian Plasmodium falciparum imply reduced fitness of chloroquine-resistant parasites. J Infect Dis 2007; 196:1613-9. (Pubitemid 351411958)
38. Mwai L, Ochong E, Abdirahman A, et al. Chloroquine resistance before after its withdrawal in Kenya. Malar J 2009; 8:106.
39. Mons B. Intra erythrocytic differentiation of Plasmodium berghei. Acta Leiden 1986; 54:1-124.
40. Buckling AG, Taylor LH, Carlton JM, Read AF. Adaptive changes in Plasmodium transmission strategies following chloroquine chemotherapy. Proc Biol Sci 1997; 264:553-9.
41. Buckling A, Ranford-Cartwright LC, Miles A, Read AF. Chloroquine increases Plasmodium falciparum gametocytogenesis in vitro. Parasitology 1999; 118:339-46. (Pubitemid 29186944)
42. Peatey CL, Skinner-Adams TS, Dixon MW, McCarthy JS, Gardiner DL, Trenholme KR. Effect of antimalarial drugs on Plasmodium falciparum gametocytes. J Infect Dis 2009; 200:1518-21.
43. Thurston JP. The morphology of Plasmodium berghei before after treatment with drugs. Trans R Soc Trop Med Hyg 1953; 47:248-56.
44. Saliba KJ, Folb PI, Smith PJ. Role for the Plasmodium falciparum digestive vacuole in chloroquine resistance. Biochem Pharmacol 1998; 56:313-20. (Pubitemid 28473206)
45. Sisowath C, Petersen I, Veiga MI, et al. In vivo selection of Plasmodium falciparum parasites carrying the chloroquine-susceptible pfcrt K76 allele after treatment with artemether-lumefantrine in Africa. J Infect Dis 2009; 199:750-7.
46. Delves MJ, Sinden RE. A semi-automated method for counting fluorescent malaria oocysts increases the throughput of transmission blocking studies. Malar J 2010; 9:35.
47. Eastman RT, Fidock DA. Artemisinin-based combination therapies: a vital tool in efforts to eliminate malaria. Nat Rev Microbiol 2009; 7:864-74.
48. Wells TN, Alonso PL, Gutteridge WE. New medicines to improve control and contribute to the eradication of malaria. Nat Rev Drug Discov 2009; 8:879-91.