Mutation analysis in pfmdr1 and pfmrp1 as potential candidate genes for artemisinin resistance in Plasmodium falciparum clinical isolates 4years after implementation of artemisinin combination therapy in Iran

Infection, Genetics and Evolution

Volumn 14, Issue 1, 2013, Pages 327-334

  Pirahmadi, Sakineh ^a   Zakeri, Sedigheh ^a   Afsharpad, Mandana ^a   Djadid, Navid Dinparast ^a  

^a PASTEUR INSTITUTE OF IRAN   (Iran)

Author keywords

Artemisinin; Haplotype; Mutations; Pfmdr1; Pfmrp1; Plasmodium falciparum

Indexed keywords

ARTEMISININ; CHLOROQUINE;

ADOLESCENT; ADULT; AGED; ANTIMALARIAL DRUG RESISTANCE; ARTICLE; CHILD; CODON; COPY NUMBER VARIATION; GENE; GENE MUTATION; GENE SEQUENCE; GENOTYPE; HAPLOTYPE; HUMAN; IRAN; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE ISOLATION; PFCRT GENE; PLASMODIUM FALCIPARUM; PMFMDR1 GENE; PMFMRP1 GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SCHOOL CHILD;

ARTEMISININS; DRUG RESISTANCE; GENE DOSAGE; HAPLOTYPES; HUMANS; IRAN; MALARIA, FALCIPARUM; MOLECULAR TYPING; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTATION; MUTATION RATE; PLASMODIUM FALCIPARUM; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84873166464     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2012.12.014     Document Type: Article

References (57)

1. Afonso A., Hunt P., Cheesman S., Alves A.C., Cunha C.V., do Rosário V., Cravo P. 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. 2006, 50:480-489.
2. Alker A.P., Lim P., Sem R., Shah N.K., Yi P., Bouth D.M., Tsuyuoka R., Maguire J.D., Fandeur T., Ariey F., Wongsrichanalai C., Meshnick S.R. Pfmdr1 and in vivo resistance to artesunate-mefloquine in falciparum malaria on the Cambodian-Thai border. Am. J. Trop. Med. Hyg. 2007, 76:641-647.
3. Anderson T.J., Nair S., Qin H., Singlam S., Brockman A., Paiphun L., Nosten F. Are transporter genes other than the chloroquine resistance locus (pfcrt) and multidrug resistance gene (pfmdr) associated with antimalarial drug resistance?. Antimicrob. Agents Chemother. 2005, 349:2180-2188.
4. Barnes A.J., Ong E.L., Dunbar E.M., Mandal B.K., Wilkins E.G. Failure of chloroquine and proguanil prophylaxis in travellers to Kenya. Lancet 1991, 338:1338-1339.
5. Barnes D.A., Foote S.J., Galatis D., Kemp D.J., Cowman A.F. Selection for high-level chloroquine resistance results in deamplification of the pfmdrl gene and increased sensitivity to mefloquine in Plasmodium falciparum. EMBO J. 1992, 11:3067-3075.
6. Bouige P., Laurent D., Piloyan L., Dassa E. Phylogenetic and functional classification of ATP-binding cassette (ABC) systems. Curr. Protein Pept. Sci. 2002, 3:541-559.
7. Cooper R.A., Hatwig C.L., Ferdig M.T. Pfcrt is more than the Plasmodium falciparum chloroquine resistance gene: a functional and evolutionary perspective. Acta Trop. 2005, 94:170-180.
8. Cowman A.F., Karcz S. Drug resistance and the p-glycoprotein homologues of Plasmodium falciparum. Semin. Cell Biol. 1993, 4:29-35.
9. Cowman A.F., Galatis D., Thompson J.K. 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, 91:1143-1147.
10. Dahlström S., Ferreira P.E., Veiga M.I., Sedighi N., Wiklund L., Mårtensson A., Färnert A., Sisowath C., Osório L., Darban H., Andersson B., Kaneko A., Conseil G., Björkman A., Gil J.P. Plasmodium falciparum multidrug resistance protein 1 and artemisinin-based combination therapy in Africa. J. Infect. Dis. 2009, 200:1456-1464.
11. Dondorp A.M., Nosten F., Yi P., Das D., Phyo A.P., Tarning J., Lwin K.M., Ariey F., Hanpithakpong W., Lee S.J., Ringwald P., Silamut K., Imwong M., Chotivanich K., Lim P., Herdman T., An S.S., Yeung S., Singhasivanon P., Day N.P., Lindegardh N., Socheat D., White N.J. Artemisinin resistance in Plasmodium falciparum malaria. N. Engl. J. Med. 2009, 361:455-467.
12. Duraisingh M.T., Drakeley C.J., Muller O., Bailey R., Snounou G., Targett G.A., Greenwood B.M., Warhurst D.C. Evidence for selection for the tyrosine-86 allele of the pfmdr 1 gene of Plasmodium falciparum by chloroquine and amodiaquine. Parasitology 1997, 114(Pt 3):205-211.
13. Duraisingh M.T., Jones P., Sambou I., von Seidlein L., Pinder M., Warhurst D.C. The tyrosine-86 allele of the pfmdr1 gene of Plasmodium falciparum is associated with increased sensitivity to the anti-malarials mefloquine and artemisinin. Mol. Biochem. Parasitol. 2000, 108:13-23.
14. Duraisingh M.T., Cowman A.F. Contribution of the pfmdr1 gene to antimalarial drug-resistance. Acta Trop. 2005, 94:181-190.
15. Eckstein-Ludwig U., Webb R.J., Van Goethem I.D., East J.M., Lee A.G., Kimura M., O'Neill P.M., Bray P.G., Ward S.A., Krishna S. Artemisinin target the SERCA of Plasmodium falciparum. Nature 2003, 424:957-961.
16. Foote S.J., Kyle D.E., Martin R.K., Oduola A.M., Forsyth K., Kemp D.J., Cowman A.F. Several alleles of the multidrug-resistance gene are closely linked to chloroquine resistance in Plasmodium falciparum. Nature 1990, 345:255-258.
17. Gregson A., Plowe C.V. Mechanisms of resistance of malaria parasites to antifolates. Pharmacol. Rev. 2005, 57:117-145.
18. Guerra C.A., Gikandi P.W., Tatem A.J., Noor A.M., Smith D.L., Hay S.I., Snow R.W. The limits and intensity of Plasmodium falciparum transmission: implications for malaria control and elimination worldwide. PLoS Med. 2008, 5:e38.
19. Halim H., Rasyid A., Ahmad Z. Evaluation of four-year hospital implementation of DOTS strategy (1998-2002). Acta Med. Indones. 2006, 38:130-134.
20. Happi C.T., Gbotosho G.O., Folarin A., Sowunmi A., Hudson T., O'Neil M., Milhous W., Wirth D.F., Oduola A.M. Selection of Plasmodium falciparum multidrug resistance gene 1 alleles in asexual stages and gametocytes by artemether-lumefantrine in Nigerian children with uncomplicated Falciparum malaria. Antimicrob. Agents Chemother. 2009, 53:888-895.
21. Hastings I.M., Ward S.A. Coartem (Artemether-lumefantrine) in Africa: the beginning of the end?. J. Infect. Dis. 2005, 192:1303-1304.
22. Imwong M., Dondorp A.M., Nosten F., Yi P., Mungthin M., Hanchana S., Das D., Phyo A.P., Lwin K.M., Pukrittayakamee S., Lee S.J., Saisung S., Koecharoen K., Nguon C., Day N.P., Socheat D., White N.J. Exploring the contribution of candidate genes to artemisinin resistance in Plasmodium falciparum. Antimicrob. Agents Chemother. 2010, 54:2886-2892.
23. Jambou R., Legrand E., Niang M., Khim N., Lim P., Volney B., Ekala M.T., Bouchier C., Esterre P., Fandeur T., Mercereau-Puijalon O. Resistance of Plasmodium falciparum field isolates to in-vitro artemether and point mutations of the SERCA-type PfATPase6. Lancet 2005, 366:1960-1963.
24. Klokouzas A., Tiffert T., van Schalkwyk D., Wu C.P., van Veen H.W., Barrand M.A., Hladky S.B. Plasmodium falciparum expresses a multidrug resistance-associated protein. Biochem. Biophys. Res. Commun. 2004, 321:197-201.
25. Kublin J.G., Cortese J.F., Njunju E.M., Mukadam R.A., Wirima J.J., Kazembe P.N., Djimdé A.A., Kouriba B., Taylor T.E., Plowe C.V. Reemergence of chloroquine sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J. Infect. Dis. 2003, 187:1870-1875.
26. Laufer M.K., Djimdé A.A., Plowe C.V. Monitoring and deterring drug resistance malaria in the era of combination therapy. Am. J. Trop. Med. Hyg. 2007, 77:160-169.
27. Lim P., Alker A.P., Khim N., Shah N.K., Incardona S., Doung S., Yi P., Bouth D.M., Bouchier C., Puijalon O.M., Meshnick S.R., Wongsrichanalai C., Fandeur T., Le Bras J., Ringwald P., Ariey F. Pfmdr1 copy number and artemisinin derivatives combination therapy failure in falciparum malaria in Cambodia. Malar. J. 2009, 8:11.
28. Meshnick S.R. Artemisinin; mechanisms of action, resistance andtoxicity. Int. J. Parasitol. 2002, 32:1655-1660.
29. Mugittu K., Genton B., Mshinda H., Beck H.P. Molecular monitoring of Plasmodium falciparum resistance to artemisinin in Tanzania. Malar. J. 2006, 5:126.
30. Mu J., Ferdig M.T., Feng X., Joy D.A., Duan J., Furuya T., Subramanian G., Aravind L., Cooper R.A., Wootton J.C., Xiong M., Su X.Z. Multiple transporters associated with malaria parasite responses to chloroquine and quinine. Mol. Microbiol. 2003, 49:977-989.
31. Noedl H., Se Y., Schaecher K., Smith B.L., Socheat D., Fukuda M.M. Artemisinin Resistance in Cambodia 1 (ARC1) study consortium, evidence of artemisinin-resistant malaria in Western Cambodia. N. Engl. J. Med. 2008, 359:2619-2620.
32. Nosten F., White N.J. Artemisinin-based combination treatment of falciparum malaria. Am. J. Trop. Med. Hyg. 2007, 77:181-192.
33. Olliaro P. Drug resistance hampers our capacity to roll back malaria. Clin. Infect. Dis. 2005, 4:S247-257.
34. Pickard A.L., Wongsrichanalai C., Purfield A., Kamwendo D., Emery K., Zalewski C., Kawamoto F., Miller R.S., Meshnick S.R. Resistance to anti-malarials in Southeast Asia and genetic polymorphisms in pfmdr1. Antimicrob. Agents Chemother. 2003, 47:2418-2423.
35. Picot S., Olliaro P., de Monbrison F., Bienvenu A.L., Price R.N., 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.
36. Price R.N., Cassar C., Brockman A., Duraisingh M., van Vugt M., White N.J., Nosten F., Krishna S. The pfmdr1 gene is associated with a multidrug-resistant phenotype in Plasmodium falciparum from the Western border of Thailand. Antimicrob. Agents Chemother. 1999, 43:2943-2949.
37. Price R.N., Uhlemann A.C., Brockman A., McGready R., Ashley E., Phaipun L., Patel R., Laing K., Looareesuwan S., White N.J., Nosten F., Krishna S. Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet 2004, 364:438-447.
38. Price R.N., Uhlemann A.C., van Vugt M., Brockman A., Hutagalung R., Nair S., Nash D., Singhasivanon P., Anderson T.J., Krishna S., White N.J., Nosten F. Molecular and pharmacological determinants of the therapeutic response to artemether-lumefantrine in multidrug-resistant Plasmodium falciparum malaria. Clin. Infect. Dis. 2006, 42:1570-1577.
39. Raj D.K., Mu J., Jiang H., Kabat J., Singh S., Sullivan M., Fay M.P., McCutchan T.F., Su X.Z. Disruption of a Plasmoium falciparum multidrug resistance-associated protein (PFMRP) alters its fitness and transport of antimalarial drugs and glutathione. J. Biol. Chem. 2009, 284:7687-7696.
40. Raman J., Mauff K., Muianga P., Mussa A., Maharaj R., Barnes K.I. Five Years of Antimalarial Resistance Marker Surveillance in Gaza Province, Mozambique, following Artemisinin-Based Combination Therapy Roll Out. PLoS One 2011, 6:e25992.
41. Reed M.B., Saliba K.J., Caruana S.R., Kirk K., Cowman A.F. Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature 2000, 403:906-909.
42. Shah N.K., Alker A.P., Sem R., Susanti A.I., Muth S., Maguire J.D., Duong S., Ariey F., Meshnick S.R., Wongsrichanalai C. Molecular surveillance for multidrug-resistant Plasmodium falciparum Cambodia. Emerg. Infect. Dis. 2008, 14:1637-1640.
43. Sidhu A.B., Valderramos S.G., Fidock D.A. Pfmdr1 mutations contribute to quinine resistance and enhance mefloquine and artemisinin sensitivity in Plasmodium falciparum. Mol. Microbiol. 2005, 57:913-926.
44. Sidhu A.B., Uhlemann A.C., Valderramos S.G., Valderramos J.C., Krishna S., Fidock D.A. Decreasing pfmdr1 copy number in Plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin. J. Infect. Dis. 2006, 194:528-535.
45. Sisowath C., Strömberg J., Mårtensson A., Msellem M., Obondo C., Björkman A. In vivo selection of Plasmodium falciparum pfmdr1 86N coding alleles by artemether-lumefantrine (Coartem). J. Infect. Dis. 2005, 191:1014-1017.
46. Snounou G., Viriyakosol S., Zhu X.P., Jarra W., Pinheiro L., do Rosario V.E., Thaithong S., Brown K.N. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol. Biochem. Parasitol. 1993, 61:315-320.
47. The malERA Consultative Group on Drugs A research Agenda for malaria eradication: drugs. PLoS Med. 2011, 8:e1000402.
48. Uhlemann A.C., Cameron A., Eckstein-Ludwig U., Fischbarg J., Iserovich P., Zuniga F.A., East M., Lee A., Brady L., Haynes R.K., Krishna S. A single amino acid residue can determine the sensitivity of SERCAs to artemisinins. Nat. Struct. Mol. Biol. 2005, 12:628-629.
49. Ursing J., Zakeri S., Gil J.P., Björkman A. Quinoline resistance associated polymorphisms in the pfcrt, pfmdr1 and pfmrp genes of Plasmodium falciparum in Iran. Acta Trop. 2006, 97:352-356.
50. Veiga M.I., Ferreira P.E., Jörnhagen L., Malmberg M., Kone A., Schmidt B.A., Petzold M., Björkman A., Nosten F., Gil J.P. Novel polymorphisms in Plasmodium falciparum ABC transporter genes are associated with major ACT antimalarial drug resistance. PLoS One 2011, 6:e20212.
51. White N.J. Qinghaosu (artemisinin): the price of success. Science 2008, 320:330-334.
52. Wilson C.M., Volkman S.K., Thaithong S., Martin R.K., Kyle D.E., Milhous W.K., Wirth D.F. Amplification of pfmdr 1 associated with mefloquine and halofantrine resistance in Plasmodium falciparum from Thailand. Mol. Biochem. Parasitol. 1993, 57:151-160.
53. Wongsrichanalai C., Meshnick S.R. Declining artesunate-mefloquine efficacy against falciparum malaria on the Cambodia-Thailand border. Emerg. Infect. Dis. 2008, 14:716-719.
54. World Health Organization, 2008. Malaria report. 2008. http://www.who.int/malaria/wmr.
55. World Health Organization, 2011. WHO-GMP update on artemisinin resistance. http://www.who.int/malaria/arupdate092011.pdf.
56. Zakeri S., Afsharpad M., Kazemzadeh T., Mehdizadeh K., Shabanil A., Djadid N.D. Association of pfcrt but not pfmdr1 alleles with chloroquine resistance in Iranian isolates of Plasmodium falciparum. Am. J. Trop. Med. Hyg. 2008, 78:633-640.
57. Zakeri S., Kakar Q., Ghasemi F., Raeisi A., Butt W., Safi N., Afsharpad M., Memon M.S., Gholizadeh S., Salehi M., Atta H., Zamani G., Djadid N.D. Detection of mixed Plasmodium falciparum & P. vivax infections by nested-PCR in Pakistan, Iran & Afghanistan. Indian J. Med. Res. 2010, 32:31-35.