Origin and evolution of sulfadoxine resistant Plasmodium falciparum

PLoS Pathogens

Volumn 6, Issue 3, 2010, Pages

  Vinayak, Sumiti ^a,b   Alam, Tauqeer ^b   Mixson Hayden, Tonya ^b   McCollum, Andrea M ^b   Sem, Rithy ^c,d   Shah, Naman K ^e   Lim, Pharath ^f   Muth, Sinuon ^c   Rogers, William O ^d   Fandeur, Thierry ^g   Barnwell, John W ^b   Escalante, Ananias A ^h   Wongsrichanalai, Chansuda ^d   Ariey, Frederick ^f   Meshnick, Steven R ^e   Udhayakumar, Venkatachalam ^b  

^a ATLANTA RESEARCH AND EDUCATION FOUNDATION   (United States)

^b NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

^c National Malaria Center   (Cambodia)

^d US Naval Medical Research Unit No 2 Jakarta   (Indonesia)

^e IL   (United States)

^f INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

^g INSTITUT PASTEUR   (France)

^h ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; DEOXYHYPUSINE SYNTHASE; PYRIMETHAMINE; SULFADOXINE; ANTIMALARIAL AGENT; MICROSATELLITE DNA;

AFRICA; ALLELE; ANTIMALARIAL DRUG RESISTANCE; ARTICLE; CAMBODIA; CAMEROON; CHROMOSOME 2; CHROMOSOME 3; CHROMOSOME 8; CODON; CONTROLLED STUDY; GENE LINKAGE DISEQUILIBRIUM; GENE MUTATION; GENETIC CONSERVATION; GENETIC SELECTION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HUMAN; KENYA; MALARIA FALCIPARUM; NONHUMAN; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SOUTH AMERICA; THAILAND; VENEZUELA; DRUG EFFECT; DRUG RESISTANCE; GENE; GENETICS; MOLECULAR EVOLUTION; PARASITOLOGY; PREVALENCE;

PLASMODIUM FALCIPARUM;

AFRICA; ANTIMALARIALS; CAMBODIA; CODON; DRUG RESISTANCE; EVOLUTION, MOLECULAR; GENES, PROTOZOAN; GENETIC VARIATION; HAPLOTYPES; HUMANS; LINKAGE DISEQUILIBRIUM; MALARIA, FALCIPARUM; MICROSATELLITE REPEATS; PLASMODIUM FALCIPARUM; PREVALENCE; SOUTH AMERICA; SULFADOXINE;

EID: 77950435762     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000830     Document Type: Article

References (70)

1. Eyles DE, Hoo CC, Warren M, Sandosham AA (1963) Plasmodium falciparum resistant to chloroquine in Cambodia. Am J Trop Med Hyg 12: 840-843.
2. Verdrager J (1986) Epidemiology of the emergence and spread of drug-resistant falciparum malaria in South-East Asia and Australasia. J Trop Med Hyg 89: 277-289.
3. Hurwitz ES, Johnson D, Campbell CC (1981) Resistance of Plasmodium falciparum malaria to sulfadoxine-pyrimethamine ('Fansidar') in a refugee camp in Thailand. Lancet 1: 1068-1070.
4. Wongsrichanalai C, Meshnick SR (2008) Declining artesunate-mefloquine efficacy against falciparum malaria on the Cambodia-Thailand border. Emerg Infect Dis 14: 716-719.
5. WHO (2002) Development of South-Asia surveillance network for malaria drug resistance. Report on informal consultative meeting. World Health Organization, Geneva, Switzerland.
6. Hurly MG (1959) Potentiation of pyrimethamine by sulphadiazine in human malaria. Trans R Soc Trop Med Hyg 53: 412-413.
7. Chulay JD, Watkins WM, Sixsmith DG (1984) Synergistic antimalarial activity of pyrimethamine and sulfadoxine against Plasmodium falciparum in vitro. Am J Trop Med Hyg 33: 325-330.
8. Laing AB (1970) Studies on the chemotherapy of malaria. I. The treatment of overt falciparum malaria with potentiating combinations of pyrimethamine and sulphormethoxine or dapsone in The Gambia. Trans R Soc Trop Med Hyg 64: 562-568.
9. WHO (2008) World Malaria Report 2008, World Health Organization, Geneva, Switzerland.
10. Brown GM (1962) The biosynthesis of folic acid. II. Inhibition by sulfonamides. J Biol Chem 237: 536-540.
11. Brooks DR, Wang P, Read M, Watkins WM, Sims PF, et al. (1994) Sequence variation of the hydroxymethyldihydropterin pyrophosphokinase: dihydropteroate synthase gene in lines of the human malaria parasite, Plasmodium falciparum, with differing resistance to sulfadoxine. Eur J Biochem 224: 397-405.
12. Triglia T, Cowman AF (1994) Primary structure and expression of the dihydropteroate synthetase gene of Plasmodium falciparum. Proc Natl Acad Sci U S A 91: 7149-7153.
13. Triglia T, Menting JG, Wilson C, Cowman AF (1997) Mutations in dihydropteroate synthase are responsible for sulfone and sulfonamide resistance in Plasmodium falciparum. Proc Natl Acad Sci U S A 94: 13944-13949.
14. Wang P, Read M, Sims PF, Hyde JE (1997) Sulfadoxine resistance in the human malaria parasite Plasmodium falciparum is determined by mutations in dihydropteroate synthetase and an additional factor associated with folate utilization. Mol Microbiol 23: 979-986.
15. Triglia T, Wang P, Sims PF, Hyde JE, Cowman AF (1998) Allelic exchange at the endogenous genomic locus in Plasmodium falciparum proves the role of dihydropteroate synthase in sulfadoxine-resistant malaria. EMBO J 17: 3807-3815.
16. Khim N, Bouchier C, Ekala MT, Incardona S, Lim P, et al. (2005) Countrywide survey shows very high prevalence of Plasmodium falciparum multilocus resistance genotypes in Cambodia. Antimicrob Agents Chemother 49: 3147-3152.
17. van den Broek IV, van der Wardt S, Talukder L, Chakma S, Brockman A, et al. (2004) Drug resistance in Plasmodium falciparum from the Chittagong Hill Tracts, Bangladesh. Trop Med Int Health 9: 680-687.
18. Ahmed A, Lumb V, Das MK, Dev V, Wajihullah, et al. (2006) Prevalence of mutations associated with higher levels of sulfadoxine-pyrimethamine resistance in Plasmodium falciparum isolates from Car Nicobar Island and Assam, India. Antimicrob Agents Chemother 50: 3934-3938.
19. Kublin JG, Witzig RS, Shankar AH, Zurita JQ, Gilman RH, et al. (1998) Molecular assays for surveillance of antifolate-resistant malaria. Lancet 351: 1629-1630.
20. Cortese JF, Caraballo A, Contreras CE, Plowe CV (2002) Origin and dissemination of Plasmodium falciparum drug-resistance mutations in South America. J Infect Dis 186: 999-1006.
21. McCollum AM, Mueller K, Villegas L, Udhayakumar V, Escalante AA (2007) Common origin and fixation of Plasmodium falciparum dhfr and dhps mutations associated with sulfadoxine-pyrimethamine resistance in a low-transmission area in South America. Antimicrob Agents Chemother 51: 2085-2091.
22. Bacon DJ, McCollum AM, Griffing SM, Salas C, Soberon V, et al. (2009) Dynamics of malaria drug resistance patterns in the Amazon basin region following changes in Peruvian national treatment policy for uncomplicated malaria. Antimicrob Agents Chemother 53: 2042-2051.
23. Zhou Z, Griffing SM, de Oliveira AM, McCollum AM, Quezada WM, et al. (2008) Decline in sulfadoxine-pyrimethamine-resistant alleles after change in drug policy in the Amazon region of Peru. Antimicrob Agents Chemother 52: 739-741.
24. Pearce RJ, Pota H, Evehe MS, Ba el H, Mombo-Ngoma G, et al. (2009) Multiple origins and regional dispersal of resistant dhps in African Plasmodium falciparum malaria. PLoS Med 6: e1000055. doi:10.1371/journal.pmed. 1000055.
25. McCollum AM, Basco LK, Tahar R, Udhayakumar V, Escalante AA (2008) Hitchhiking and selective sweeps of Plasmodium falciparum sulfadoxine and pyrimethamine resistance alleles in a population from central Africa. Antimicrob Agents Chemother 52: 4089-4097.
26. Nair S, Williams JT, Brockman A, Paiphun L, Mayxay M, et al. (2003) A selective sweep driven by pyrimethamine treatment in southeast asian malaria parasites. Mol Biol Evol 20: 1526-1536.
27. McCollum AM, Poe AC, Hamel M, Huber C, Zhou Z, et al. (2006) Antifolate resistance in Plasmodium falciparum: multiple origins and identification of novel dhfr alleles. J Infect Dis 194: 189-197.
28. Mita T, Tanabe K, Takahashi N, Culleton R, Ndounga M, et al. (2009) Indigenous evolution of Plasmodium falciparum pyrimethamine resistance multiple times in Africa. J Antimicrob Chemother 63: 252-255.
29. Certain LK, Briceno M, Kiara SM, Nzila AM, Watkins WM, et al. (2008) Characteristics of Plasmodium falciparum dhfr haplotypes that confer pyrimethamine resistance, Kilifi, Kenya, 1987-2006. J Infect Dis 197: 1743-1751.
30. Roper C, Pearce R, Bredenkamp B, Gumede J, Drakeley C, et al. (2003) Antifolate antimalarial resistance in southeast Africa: a population-based analysis. Lancet 361: 1174-1181.
31. Roper C, Pearce R, Nair S, Sharp B, Nosten F, et al. (2004) Intercontinental spread of pyrimethamine-resistant malaria. Science 305: 1124.
32. Maiga O, Djimde AA, Hubert V, Renard E, Aubouy A, et al. (2007) A shared Asian origin of the triple-mutant dhfr allele in Plasmodium falciparum from sites across Africa. J Infect Dis 196: 165-172.
33. Ariey F, Fandeur T, Durand R, Randrianarivelojosia M, Jambou R, et al. (2006) Invasion of Africa by a single pfcrt allele of South East Asian type. Malar J 5: 34.
34. Ndiaye D, Daily JP, Sarr O, Ndir O, Gaye O, et al. (2006) Defining the origin of Plasmodium falciparum resistant dhfr isolates in Senegal. Acta Trop 99: 106-111.
35. Lynch C, Pearce R, Pota H, Cox J, Abeku TA, et al. (2008) Emergence of a dhfr mutation conferring high-level drug resistance in Plasmodium falciparum populations from southwest Uganda. J Infect Dis 197: 1598-1604.
36. Mita T, Tanabe K, Takahashi N, Tsukahara T, Eto H, et al. (2007) Independent evolution of pyrimethamine resistance in Plasmodium falciparum isolates in Melanesia. Antimicrob Agents Chemother 51: 1071-1077.
37. McCollum AM Drug resistant Plasmodium falciparum: Genetic hitchhiking, selective sweeps, and multiple origins [Ph.D Thesis], Emory University, Atlanta, USA.
38. Su X, Ferdig MT, Huang Y, Huynh CQ, Liu A, et al. (1999) A genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum. Science 286: 1351-1353.
39. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295.
40. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
41. Lewis PO, Zaykin D (2001) Genetic Data Analysis: Computer program for the analysis of allelic data. Version 1.0 (d16c). Free program distributed by the authors over the internet from http://lewis.eeb.uconn.edu/lewishome/software. html.
42. Lewontin RC, Krakauer J (1973) Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74: 175-195.
43. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B: Biol Sci 263: 1619-1626.
44. Wilding CS, Butlin RK, Grahame J (2001) Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J Evol Biol 14: 611-619.
45. Anderson TJ, Nair S, Sudimack D, Williams JT, Mayxay M, et al. (2005) Geographical distribution of selected and putatively neutral SNPs in Southeast Asian malaria parasites. Mol Biol Evol 22: 2362-2374.
46. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14: 671-688.
47. Beaumont MA (2005) Adaptation and speciation: what can F(st) tell us? Trends Ecol Evol 20: 435-440.
48. Demontis D, Pertoldi C, Loeschcke V, Mikkelsen K, Axelsson T, et al. (2009) Efficiency of selection, as measured by single nucleotide polymorphism variation, is dependent on inbreeding rate in Drosophila melanogaster. Mol Ecol 18: 4551-4563.
49. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics 9: 323.
50. Goudet J FSTAT, a program to estimate and test gene diversities and fixation indices Version 2.9.3.2. www2.unil.ch/popgen/softwares/fstat.htm.
51. Smith JM, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci U S A 90: 4384-4388.
52. Hudson RR (1994) Analytical results concerning linkage disequilibrium in models with genetic transformation and conjugation. J Evol Biol 7: 535-548.
53. Haubold B, Hudson RR (2000) LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage Analysis. Bioinformatics 16: 847-848.
54. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37-48.
55. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG (2004) eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186: 1518-1530.
56. Nash D, Nair S, Mayxay M, Newton PN, Guthmann JP, et al. (2005) Selection strength and hitchhiking around two anti-malarial resistance genes. Proc Biol Sci 272: 1153-1161.
57. Harris EE, Hey J (1999) X chromosome evidence for ancient human histories. Proc Natl Acad Sci U S A 96: 3320-3324.
58. Gregson A, Plowe CV (2005) Mechanisms of resistance of malaria parasites to antifolates. Pharmacol Rev 57: 117-145.
59. Picot S, Olliaro P, de Monbrison F, Bienvenu AL, Price RN, et al. (2009) A systematic review and meta-analysis of evidence for correlation between molecular markers of parasite resistance and treatment outcome in falciparum malaria. Malar J 8: 89.
60. Curtis J, Duraisingh MT, Warhurst DC (1998) In vivo selection for a specific genotype of dihydropteroate synthetase of Plasmodium falciparum by pyrimethamine-sulfadoxine but not chlorproguanil-dapsone treatment. J Infect Dis 177: 1429-1433.
61. Wang P, Lee CS, Bayoumi R, Djimde A, Doumbo O, et al. (1997) Resistance to antifolates in Plasmodium falciparum monitored by sequence analysis of dihydropteroate synthetase and dihydrofolate reductase alleles in a large number of field samples of diverse origins. Mol Biochem Parasitol 89: 161-177.
62. Nzila AM, Mberu EK, Sulo J, Dayo H, Winstanley PA, et al. (2000) Towards an understanding of the mechanism of pyrimethamine-sulfadoxine resistance in Plasmodium falciparum: genotyping of dihydrofolate reductase and dihydropteroate synthase of Kenyan parasites. Antimicrob Agents Chemother 44: 991-996.
63. Omar SA, Adagu IS, Gump DW, Ndaru NP, Warhurst DC (2001) Plasmodium falciparum in Kenya: high prevalence of drug-resistance-associated polymorphisms in hospital admissions with severe malaria in an epidemic area. Ann Trop Med Parasitol 95: 661-669.
64. Staedke SG, Sendagire H, Lamola S, Kamya MR, Dorsey G, et al. (2004) Relationship between age, molecular markers, and response to sulphadoxine-pyrimethamine treatment in Kampala, Uganda. Trop Med Int Health 9: 624-629.
65. Kun JF, Lehman LG, Lell B, Schmidt-Ott R, Kremsner PG (1999) Low-dose treatment with sulfadoxine-pyrimethamine combinations selects for drug-resistant Plasmodium falciparum strains. Antimicrob Agents Chemother 43: 2205-2208.
66. Kublin JG, Dzinjalamala FK, Kamwendo DD, Malkin EM, Cortese JF, et al. (2002) Molecular markers for failure of sulfadoxine-pyrimethamine and chlorproguanil-dapsone treatment of Plasmodium falciparum malaria. J Infect Dis 185: 380-388.
67. Kyabayinze D, Cattamanchi A, Kamya MR, Rosenthal PJ, Dorsey G (2003) Validation of a simplified method for using molecular markers to predict sulfadoxine-pyrimethamine treatment failure in African children with falciparum malaria. Am J Trop Med Hyg 69: 247-252.
68. Nagesha HS, Din S, Casey GJ, Susanti AI, Fryauff DJ, et al. (2001) Mutations in the pfmdr1, dhfr and dhps genes of Plasmodium falciparum are associated with in-vivo drug resistance in West Papua, Indonesia. Trans R Soc Trop Med Hyg 95: 43-49.
69. Lumb V, Das MK, Mittra P, Ahmed A, Kumar M, et al. (2009) Emergence of an unusual sulfadoxine-pyrimethamine resistance pattern and a novel K540N mutation in dihydropteroate synthetase in Plasmodium falciparum isolates obtained from Car Nicobar Island, India, after the 2004 Tsunami. J Infect Dis 199: 1064-1073.
70. Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, et al. (2002) Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418: 320-323.