Experimental evolution of resistance to artemisinin combination therapy results in amplification of the mdr1 gene in a rodent malaria parasite

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Rodrigues, Louise A ^a   Henriques, Gisela ^a   Borges, Sofia T ^a   Hunt, Paul ^b   Sanchez, Cecília P ^c   Martinelli, Axel ^a   Cravo, Pedro ^a  

^a INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMISININ; ARTESUNATE; ARTESUNATE PLUS MEFLOQUINE; GENE PRODUCT; MEFLOQUINE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN ATPASE6; PROTEIN UBP1; UNCLASSIFIED DRUG; ANTIMALARIAL AGENT; ARTEMISININ DERIVATIVE; MULTIDRUG RESISTANCE PROTEIN; PROTOZOAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMALARIAL DRUG RESISTANCE; ANTIMALARIAL DRUG SUSCEPTIBILITY; ARTICLE; CONTROLLED STUDY; CYTOLYSIS; DRUG EXPOSURE; ERYTHROCYTE; GENE AMPLIFICATION; GENE DUPLICATION; GENE EXPRESSION; GENE SEQUENCE; IN VIVO STUDY; MOLECULAR CLONING; MOUSE; NONHUMAN; PLASMODIUM CHABAUDI; PLASMODIUM CHABAUDI INFECTION; POINT MUTATION; REAL TIME POLYMERASE CHAIN REACTION; RODENT; WESTERN BLOTTING; ANIMAL; DNA SEQUENCE; DRUG EFFECT; DRUG RESISTANCE; GENETICS; MALARIA; METABOLISM; PARASITOLOGY; POLYMERASE CHAIN REACTION;

ARTESUNATE; PLASMODIUM CHABAUDI; RODENTIA;

ANIMALS; ANTIMALARIALS; ARTEMISININS; BLOTTING, WESTERN; DRUG RESISTANCE; MALARIA; MEFLOQUINE; MICE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PLASMODIUM CHABAUDI; POLYMERASE CHAIN REACTION; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 77955451229     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011593     Document Type: Article

References (38)

1. WHO Guidelines for the Treatment of Malaria (2006) [http://www.who.int/malaria/docs/treatmentguidelines2006.pdf].
2. White N (1999) Antimalarial drug resistance and combination chemotherapy. Philos Trans R Soc Lond B Biol Sci 354(1384): 739-49.
3. White NJ, Pongtavornpinyo W, Maude RJ, Saralamba S, Aguas R, et al. (2009) Hyperparasitaemia and low dosing are an important source of anti-malarial drug resistance. Malar J 11;8: 253.
4. Yeung S, White NJ (2005) How do patients use antimalarial drugs? A review of the Evidence. Trop Med Int Health 10(2): 121-38.
5. Wongsrichanalai C, Sirichaisinthop J, Karwacki JJ, Congpuong K, Miller RS, et al. (2001) Drug resistant malaria on the Thai-Myanmar and Thai-Cambodian borders. Southeast Asian J Trop Med Public Health 32(1): 41-9.
6. Price RN, Nosten F, Luxemburger C, van Vugt M, Phaipun L, et al. (1997) Artesunate/mefloquine treatment of multi-drug resistant falciparum malaria. Trans R Soc Trop Med Hyg 91(5): 574-7.
7. Noedl H, Socheat D, Satimai W (2009) Artemisinin-resistant malaria in Asia. N Engl J Med 361(5): 540-1.
8. Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, et al. (2009) Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 30;361(5): 455-67.
9. Carrara VI, Zwang J, Ashley EA, Price RN, Stepniewska K, et al. (2009) Changes in the treatment responses to artesunate-mefloquine on the northwestern border of Thailand during 13 years of continuous deployment. PLoS One 4(2): e4551.
10. Eckstein-Ludwig U, Webb RJ, Van Goethem ID, East JM, Lee AG, et al. (2003) Artemisinins target the SERCA of Plasmodium falciparum. Nature 21;424(6951): 957-61.
11. Uhlemann AC, Cameron A, Eckstein-Ludwig U, Fischbarg J, Iserovich P, et al. (2005) A single amino acid residue can determine the sensitivity of SERCAs to artemisinins. Nat Struct Mol Biol 12: 628-629.
12. Jambou R, Legrand E, Niang M, Khim N, Lim P, et al. (2005) Resistance of Plasmodium falciparum field isolates to in-vitro artemether and point mutations of the SERCA-type PfATPase6. Lancet 3;366(9501): 1960-3.
13. Szakács G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM (2006) Targeting multidrug resistance in cancer. Nat Rev Drug Discov 5(3): 219-34.
14. Wilson CM, Volkman SK, Thaithong S, Martin RK, Kyle DE, et al. (1993) Amplification of pfmdr 1 associated with mefloquine and halofantrine resistance in Plasmodium falciparum from Thailand. Mol Biochem Parasitol 57(1): 151-60.
15. Price RN, Cassar C, Brockman A, Duraisingh M, van Vugt M, et al. (1999) The pfmdr1 gene is associated with a multidrug-resistant phenotype in Plasmodium falciparum from the western border of Thailand. Antimicrob Agents Chemother 43(12): 2943-9.
16. Price RN, Uhlemann AC, Brockman A, McGready R, Ashley E, et al. (2004) Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet 6;364(9432): 438-47.
17. Price RN, Uhlemann AC, Van Vugt M, Brockman A, Hutagalung R, et al. (2006) Molecular and pharmacological determinants of the therapeutic response to artemether-lumefantrine in multidrug-resistant Plasmodium falciparum malaria. Clin Infect Dis 1;42(11): 1570-7.
18. Lim P, Alker AP, Khim N, Shah NK, Incardona S, et al. (2009) Pfmdr1 copy number and arteminisin derivatives combination therapy failure in falciparum malaria in Cambodia. Malar J Jan 12;8: 11.
19. Rogers WO, Sem R, Tero T, Chim P, Lim P, et al. (2009) Failure of artesunatemefloquine combination therapy for uncomplicated Plasmodium falciparum malaria in southern Cambodia. Malar J 12;8: 10.
20. Cowman AF, Galatis D, Thompson JK (1994) 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 91: 1143-1147.
21. Peel SA, Bright P, Yount B, Handy J, Baric RS (1994) 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 51: 648-658.
22. Sidhu AB, Uhlemann AC, Valderramos SG, Valderramos JC, Krishna S, et al. (2006) Decreasing pfmdr1 copy number in plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin. J Infect Dis 15;194(4): 528-35.
23. Nair S, Nash D, Sudimack D, Jaidee A, Barends M, et al. (2007) Recurrent gene amplification and soft selective sweeps during evolution of multidrug resistance in malaria parasites. Mol Biol Evol 24(2): 562-73.
24. Vinayak S, Alam MT, Sem R, Shah NK, Susanti AI, et al. (2010) Multiple genetic backgrounds of the amplified Plasmodium falciparum multidrug resistance (pfmdr1) gene and selective sweep of 184F mutation in Cambodia. J Infect Dis 15;201(10): 1551-60.
25. Carlton JM, Hayton K, Cravo PV, Walliker D (2001) Of mice and malaria mutants: unravelling the genetics of drug resistance using rodent malaria models. Trends Parasitol 17(5): 236-42.
26. Hayton K, Ranford-Cartwright LC, Walliker D (2002) Sulfadoxine-pyrimethamine resistance in the rodent malaria parasite Plasmodium chabaudi. Antimicrob Agents Chemother 46(8): 2482-9.
27. Cravo PV, Carlton JM, Hunt P, Bisoni L, Padua RA, et al. (2003) Genetics of mefloquine resistance in the rodent malaria parasite Plasmodium chabaudi. Antimicrob Agents Chemother 47(2): 709-18.
28. Afonso A, Hunt P, Cheesman S, Alves AC, Cunha CV, et al. (2006) Malaria parasites can develop stable resistance to artemisinin but lack mutations in candidate genes atp6 (encoding the sarcoplasmic and endoplasmic reticulum Ca2+ ATPase), tctp, mdr1, and cg10. Antimicrob Agents Chemother 50(2): 480-9.
29. Hunt P, Afonso A, Creasey A, Culleton R, Sidhu AB, et al. (2007) Gene encoding a deubiquitinating enzyme is mutated in artesunate- and chloroquineresistant rodent malaria parasites. Mol Microbiol 65(1): 27-40.
30. Chavchich M, Gerena L, Peters J, Chen N, Cheng Q, et al. (2010) Induction of resistance to artemisinin derivatives in Plasmodium falciparum: Role of Pfmdr1 amplification and expression. Antimicrob Agents Chemother. 29. [Epub ahead of print]
31. Ferreira ID, Nogueira F, Borges ST, do Rosário VE, Cravo P (2004) Is the expression of genes encoding enzymes of glutathione (GSH) metabolism involved in chloroquine resistance in Plasmodium chabaudi parasites? Mol Biochem Parasitol 136(1): 43-50.
32. White NJ (1991) The clinical evaluation of antimalarial treatment response. Acta Leiden 60(1): 141-6.
33. Schlagenhauf P, Petersen E (2009) Antimalarial drug resistance: the monocombi- counterfeit triangle. Expert Rev Anti Infect Ther 7(9): 1039-42.
34. Uhlemann AC, McGready R, Ashley EA, Brockman A, Singhasivanon P, et al. (2007) Intrahost selection of Plasmodium falciparum pfmdr1 alleles after antimalarial treatment on the northwestern border of Thailand. J Infect Dis 195(1): 134-41.
35. Zhang Z, Wu JY, Hait WN, Yang JM (2004) Regulation of the stability of Pglycoprotein by ubiquitination. Mol Pharmacol 66(3): 395-403.
36. Rosário V (1981) Cloning of naturally occurring mixed infections of malaria parasites. Science 212(4498): 1037-1188.
37. Corpet F (1988) MultAlin - Multiple sequence alignment with hierarchical clustering Nucl. Acids Res 16 (22): 10881-10890.
38. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4): 402-8.