Decreasing pfmdr1 copy number in Plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin

Journal of Infectious Diseases

Volumn 194, Issue 4, 2006, Pages 528-535

  Sidhu, Amar Bir Singh ^a   Uhlemann, Anne Catrin ^b,c   Valderramos, Stephanie G ^a   Valderramos, Juan Carlos ^a   Krishna, Sanjeev ^b   Fidock, David A ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^c NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMISININ; BENFLUMETOL; DNA; HALOFANTRINE; MEFLOQUINE; MESSENGER RNA; QUININE;

ARTICLE; COPY NUMBER; GENE; GENE AMPLIFICATION; GENE COPY; GENE DISRUPTION; GENETIC SUSCEPTIBILITY; HUMAN; IC 50; MALARIA; NONHUMAN; PFMDR1 GENE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK ASSESSMENT; TREATMENT FAILURE;

ANIMALS; ANTIMALARIALS; ARTEMISININS; ATP-BINDING CASSETTE TRANSPORTERS; DNA, PROTOZOAN; DRUG RESISTANCE, MULTIPLE; ETHANOLAMINES; FLUORENES; GENES, MDR; INHIBITORY CONCENTRATION 50; MALARIA, FALCIPARUM; MEFLOQUINE; PARASITIC SENSITIVITY TESTS; PHENANTHRENES; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PROTOZOAN PROTEINS; QUININE; SESQUITERPENES;

EID: 33746302565     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/507115     Document Type: Article

References (49)

1. Uhlemann AC, Krishna S. Antimalarial multi-drug resistance in Asia: mechanisms and assessment. Curr Top Microbiol Immunol 2005; 295: 39-53.
2. Baird JK. Effectiveness of antimalarial drugs. N Engl J Med 2005; 352: 1565-77.
3. Wongsrichanalai C, Pickard AL, Wernsdorfer WH, Meshnick SR. Epidemiology of drug-resistant malaria. Lancet Infect Dis 2002; 2:209-18.
4. Uhlemann A-C, Yuthavong Y, Fidock DA. Mechanisms of antimalarial drug action and resistance. In: Sherman I, ed. Molecular approaches to malaria. 2nd ed. Washington, DC: ASM Press, 2005:229-61.
5. Fidock DA, Nomura T, Talley AK, et al. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell 2000; 6:861-71.
6. Djimde A, Doumbo OK, Steketee RW, Plowe CV. Application of a molecular marker for surveillance of chloroquine-resistant falciparum malaria. Lancet 2001; 358:890-1.
7. Sidhu AB, Verdier-Pinard D, Fidock DA. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 2002; 298:210-3.
8. Ashley EA, White NJ. Artemisinin-based combinations. Curr Opin Infect Dis 2005; 18:531-6.
9. Foote SJ, Thompson JK, Cowman AF, Kemp DJ. Amplification of the multidrug resistance gene in some chloroquine-resistant isolates of P. falciparum. Cell 1989; 57:921-30.
10. Wilson CM, Serrano AE, Wasley A, Bogenschutz MP, Shankar AH, Wirth DF. Amplification of a gene related to mammalian mdr genes in drug-resistant Plasmodium falciparum. Science 1989; 244:1184-6.
11. Cowman AF, Karcz S, Galatis D, Culvenor JG. A P-glycoprotein homologue of Plasmodium falciparum is localized on the digestive vacuole. J Cell Biol 1991; 113:1033-42.
12. Foley M, Tilley L. Quinoline antimalarials: mechanisms of action and resistance and prospects for new agents. Pharmacol Ther 1998; 79:55-87.
13. O'Neill PM, Bray PG, Hawley SR, Ward SA, Park BK. 4-Aminoquinolines-past, present, and future: a chemical perspective. Pharmacol Ther 1998; 77:29-58.
14. Duraisingh MT, Cowman AF. Contribution of the pfmdr1 gene to antimalarial drug-resistance. Acta Trop 2005; 94:181-90.
15. Woodrow CJ, Krishna S. Antimalarial drugs: recent advances in molecular determinants of resistance and their clinical significance. Cell Mol Life Sci 2006; 15 May [electronically published ahead of print].
16. Triglia T, Foote SJ, Kemp DJ, Cowman AF. Amplification of the multidrug resistance gene pfmdr1 in Plasmodium falciparum has arisen as multiple independent events. Mol Cell Biol 1991; 11:5244-50.
17. Wilson CM, Volkman SK, Thaithong S, et al. Amplification of pfmdr 1 associated with mefloquine and halofantrine resistance in Plasmodium falciparum from Thailand. Mol Biochem Parasitol 1993; 57:151-60.
18. Volkman SK, Wilson CM, Wirth DF. Stage-specific transcripts of the Plasmodium falciparum pfmdr1 gene. Mol Biochem Parasitol 1993; 57: 203-11.
19. Peel SA, Bright P, Yount B, Handy J, Baric RS. A strong association between mefloquine and halofantrine resistance and amplification, overexpression, and mutation in the P-glycoprotein gene homolog (pfmdr) of Plasmodium falciparum in vitro. Am J Trop Med Hyg 1994; 51:648-58.
20. Cowman AF, Galatis D, Thompson JK. Selection for mefloquine resistance in Plasmodium falciparum is linked to amplification of the pfmdr1 gene and cross-resistance to halofantrine and quinine. Proc Natl Acad Sci USA 1994; 91:1143-7.
21. Barnes DA, Foote SJ, Galatis D, Kemp DJ, Cowman AF. Selection for high-level chloroquine resistance results in deamplification of the pfmdr1 gene and increased sensitivity to mefloquine in Plasmodium falciparum. EMBO J 1992; 11:3067-75.
22. Basco LK, Le Bras J, Rhoades Z, Wilson CM. Analysis of pfmdr1 and drug susceptibility in fresh isolates of Plasmodium falciparum from subsaharan Africa. Mol Biochem Parasitol 1995; 74:157-66.
23. Chaiyaroj SC, Buranakiti A, Angkasekwinai P, Looressuwan S, Cowman AF. Analysis of mefloquine resistance and amplification of pfmdr1 in multidrug-resistant Plasmodium falciparum isolates from Thailand. Am J Trop Med Hyg 1999; 61:780-3.
24. Pickard AL, Wongsrichanalai C, Purfield A, et al. Resistance to anti-malarials in Southeast Asia and genetic polymorphisms in pfmdr1. Antimicrob Agents Chemother 2003; 47:2418-23.
25. Nelson AL, Purfield A, McDaniel P, et al. pfmdr1 genotyping and in vivo mefloquine resistance on the Thai-Myanmar border. Am J Trop Med Hyg 2005; 72:586-92.
26. Price RN, Cassar C, Brockman A, et al. The pfmdr1 gene is associated with a multidrug-resistant phenotype in Plasmodium falciparum from the western border of Thailand. Antimicrob Agents Chemother 1999; 43:2943-9.
27. Price RN, Uhlemann AC, Brockman A, et al. Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet 2004; 364:438-47.
28. Sidhu AB, Valderramos SG, Fidock DA. pfmdr1 mutations contribute to quinine resistance and enhance mefloquine and artemisinin sensitivity in Plasmodium falciparum. Mol Microbiol 2005; 57:913-26.
29. Fidock DA, Wellems TE. Transformation with human dihydrofolate reductase renders malaria parasites insensitive to WR99210 but does not affect the intrinsic activity of proguanil. Proc Natl Acad Sci USA 1997; 94:10931-6.
30. Elmendorf HG, Haldar K. Identification and localization of ERD2 in the malaria parasite Plasmodium falciparum: separation from sites of sphingomyelin synthesis and implications for organization of the Golgi. EMBO J 1993; 12:4763-73.
31. 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.
32. Kidgell C, Volkman SK, Daily J, et al. A systematic map of genetic variation in Plasmodium falciparum. PLoS Pathog 2006; 2:e57.
33. Su X-Z, Kirkman LS, Wellems TE. Complex polymorphisms in a ∼330 kDa protein are linked to chloroquine-resistant P. falciparum in Southeast Asia and Africa. Cell 1997; 91:593-603.
34. Price RN, Uhlemann AC, van Vugt M, et al. Molecular and pharmacological determinants of the therapeutic response to artemether-lumefantrine in multidrug-resistant Plasmodium falciparum malaria. Clin Infect Dis 2006; 42:1570-7.
35. Krishna S, Woodrow CJ, Staines HM, Haynes RK, Mercereau-Puijalon O. Re-evaluation of how artemisinins work in light of emerging evidence of in vitro resistance. Trends Mol Med 2006; 12:200-5.
36. Basco LK, Le Bras J. In vitro activity of halofantrine and its relationship to other standard antimalarial drugs against African isolates and clones of Plasmodium falciparum. Am J Trop Med Hyg 1992; 47:521-7.
37. Basco LK, Bickii J, Ringwald P. In vitro activity of lumefantrine (benflumetol) against clinical isolates of Plasmodium falciparum in Yaounde, Cameroon. Antimicrob Agents Chemother 1998; 42:2347-51.
38. Reed MB, Saliba KJ, Caruana SR, Kirk K, Cowman AF. Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature 2000; 403:906-9.
39. Sisowath C, Stromberg J, Martensson A, et al. In vivo selection of Plasmodium falciparum pfmdr1 86N coding alleles by artemether-lumefantrine (Coartem). J Infect Dis 2005; 191:1014-7.
40. Martensson A, Stromberg J, Sisowath C, et al. Efficacy of artesunate plus amodiaquine versus that of artemether-lumefantrine for the treatment of uncomplicated childhood Plasmodium falciparum malaria in Zanzibar, Tanzania. Clin Infect Dis 2005; 41:1079-86.
41. Cooper RA, Ferdig MT, Su XZ, et al. Alternative mutations at position 76 of the vacuolar transmembrane protein PfCRT are associated with chloroquine resistance and unique stereospecific quinine and quinidine responses in Plasmodium falciparum. Mol Pharmacol 2002; 61:35-42.
42. Johnson DJ, Fidock DA, Mungthin M, et al. Evidence for a central role for PfCRT in conferring Plasmodium falciparum resistance to diverse antimalarial agents. Mol Cell 2004; 15:867-77.
43. Lim AS, Galatis D, Cowman AF. Plasmodium falciparum: amplification and overexpression of pfmdr1 is not necessary for increased mefloquine resistance. Exp Parasitol 1996; 83:295-303.
44. Looareesuwan S, Kyle DE, Viravan C, et al. Treatment of patients with recrudescent falciparum malaria with a sequential combination of artesunate and mefloquine. Am J Trop Med Hyg 1992; 47:794-9.
45. 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.
46. Ferdig MT, Cooper RA, Mu J, et al. Dissecting the loci of low-level quinine resistance in malaria parasites. Mol Microbiol 2004; 52:985-97.
47. Brasseur P, Kouamouo J, Moyou-Somo R, Druilhe P. Multi-drug resistant falciparum malaria in Cameroon in 1987-1988. II. Mefloquine resistance confirmed in vivo and in vitro and its correlation with quinine resistance. Am J Trop Med Hyg 1992; 46:8-14.
48. Uhlemann AC, Ramharter M, Lell B, Kremsner PG, Krishna S. Amplification of Plasmodium falciparum multidrug resistance gene 1 in isolates from Gabon. J Infect Dis 2005; 192:1830-5.
49. World Health Organization. Position of WHO's Roll Back Malaria Department on malaria treatment policy. Available at: http://www.who.int/malaria/docs/ who_apt_position.htm. Accessed 7 July 2006.