A selective sweep driven by pyrimethamine treatment in Southeast Asian malaria parasites

Molecular Biology and Evolution

Volumn 20, Issue 9, 2003, Pages 1526-1536

  Nair, Shalini ^a   Williams, Jeff T ^a   Brockman, Alan ^b,c   Paiphun, Lucy ^b   Mayxay, Mayfong ^d   Newton, Paul N ^e,f   Guthmann, Jean Paul ^g   Smithuis, Frank M ^h   Hien, Tran Tinh ⁱ   White, Nicholas J ^c,e   Nosten, François ^b,c,e   Anderson, Tim J C ^a  

^a SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^b SHOKLO MALARIA RESEARCH UNIT   (Thailand)

^c MAHIDOL UNIVERSITY   (Thailand)

^d NATIONAL UNIVERSITY OF LAOS   (Laos)

^e JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^f MAHOSOT HOSPITAL   (Laos)

^g EPICENTRE   (France)

^h MÉDECINS SANS FRONTIÈRES   (Switzerland)

ⁱ CHO QUAN HOSPITAL   (Viet Nam)

Author keywords

Dihydrofolate reductase; Expected heterozygosity; Microsatellite; Plasmodium falciparum; Pyrimethamine

Indexed keywords

ANTIMALARIAL AGENT; DIHYDROFOLATE REDUCTASE; FANSIDAR; PROTOZOAL DNA; PYRIMETHAMINE;

ARTICLE; CAMBODIA; CHROMOSOME 4; CONTROLLED STUDY; GENOME; HAPLOTYPE; HETEROZYGOSITY; HUMAN; HUMAN TISSUE; MALARIA; MICROSATELLITE MARKER; MYANMAR; NONHUMAN; PLASMODIUM FALCIPARUM; POINT MUTATION; SOUTHEAST ASIA; THAILAND; VIET NAM;

ALLELES; ANIMALS; ANTIMALARIALS; ASIA; DRUG RESISTANCE; MALARIA; MALARIA, FALCIPARUM; MICROSATELLITE REPEATS; MUTATION; PYRIMETHAMINE; SELECTION (GENETICS); TETRAHYDROFOLATE DEHYDROGENASE; VARIATION (GENETICS);

EUKARYOTA; PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 10744222802     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msg162     Document Type: Article

References (48)

1. Anderson, T. J., B. Haubold, J. T. Williams et al. (16 co-authors). 2000a. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol. Biol. Evol. 17:1467-1482.
2. Anderson, T. J., X. Z. Su, A. Roddam, and K. P. Day. 2000b. Complex mutations in a high proportion of microsatellite loci from the protozoan parasite Plasmodium falciparum. Mol. Ecol. 9:1599-1608.
3. Babiker, H. A., L. C. Ranford-Cartwright, D. Currie, J. D. Charlwood, P. Billingsley, T. Teuscher, and D. Walliker. 1994. Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology 109(pt 4):413-421.
4. Barton, N. H. 2000. Genetic hitchhiking. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355:1553-1562.
5. Bunnag, D., and T. Harinasuta. 1987. The current status of drug resistance in malaria. Int. J. Parasitol. 17:169-180.
6. Clyde, D. F., and G. T. Shute. 1957. Resistance of Plasmodium falciparum in Tanganyika to pyrimethamine administered at weekly intervals. Trans. R. Soc. Trop. Med. Hyg. 51:505-513.
7. Conway, D. J., C. Roper, A. M. Oduola, D. E. Arnot, P. G. Kremsner, M. P. Grobusch, C. F. Curtis, and B. M. Greenwood. 1999. High recombination rate in natural populations of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 96:4506-4511.
8. Cornuet, J. M., and G. Luikart. 1996. Description and power analysis of two tests for detecting recent population bottle-necks from allele frequency data. Genetics 144:2001-2014.
9. Cortese, J. F., A. Caraballo, C. E. Contreras, and C. V. Plowe. 2002. Origin and dissemination of Plasmodium falciparum drug-resistance mutations in South America. J. Infect. Dis. 186:999-1006.
10. Cortese, J. F., and C. V. Plowe. 1998. Antifolate resistance due to new and known Plasmodium falciparum dihydrofolate reductase mutations expressed in yeast. Mol. Biochem. Parasitol. 94:205-214.
11. Doumbo, O. K., K. Kayentao, A. Djimde, J. F. Cortese, Y. Diourte, A. Konare, J. G. Kublin, and C. V. Plowe. 2000. Rapid selection of Plasmodium falciparum dihydrofolate reductase mutants by pyrimethamine prophylaxis. J. Infect. Dis. 182:993-996.
12. Endler, J. A. 1986. Natural selection in the wild. Princeton University Press, Princeton.
13. Fleiss, J. L. 1981. Statistical methods for rates and proportions. John Wiley & Sons, New York.
14. Goudet, J. 2000. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.1). [version 2.9.1].
15. Harr, B., M. Kauer, and C. Schlotterer. 2002. Hitchhiking mapping: a population-based fine-mapping strategy for adaptive mutations in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 99:12949-12954.
16. Hartl, D. L., and D. E. Dykhuizen. 1981. Potential for selection among nearly neutral allozymes of 6-phosphogluconate dehydrogenase in Escherichia coli. Proc. Natl. Acad. Sci. USA 78:6344-6348.
17. Hill, W. G., and H. A. Babiker. 1995. Estimation of numbers of malaria clones in blood samples. Proc. R. Soc. Lond. B Biol. Sci. 262:249-257.
18. Hill, W. G., and A. Robertson. 1966. The effect of linkage on limits to artificial selection. Genet. Res. 8:269-294.
19. Hughes, M. K., and A. L. Hughes. 1995. Natural selection on Plasmodium surface proteins. Mol. Biochem. Parasitol. 71:99-113.
20. Kim, Y., and W. Stephan. 2002. Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160:765-777.
21. Kohn, M. H., H. J. Pelz, and R. K. Wayne. 2000. Natural selection mapping of the warfarin-resistance gene. Proc. Natl. Acad. Sci. USA 97:7911-7915.
22. Levin, B. R., V. Perrot, and N. Walker. 2000. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154:985-997.
23. Mendez, F., A. Munoz, G. Carrasquilla, D. Jurado, M. Arevalo-Herrera, J. F. Cortese, and C. V. Plowe. 2002. Determinants of treatment response to sulfadoxine-pyrimethamine and subsequent transmission potential in falciparum malaria. Am. J. Epidemiol. 156:230-238.
24. Mu, J., J. Duan, K. D. Makova, D. A. Joy, C. Q. Huynh, O. H. Branch, W. H. Li, and X. Z. Su. 2002. Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature 418:323-326.
25. Nair, S., A. Brockman, L. Paiphun, F. Nosten, and T. J. Anderson. 2002. Rapid genotyping of loci involved in antifolate drug resistance in Plasmodium falciparum by primer extension. Int. J. Parasitol. 32:852-858.
26. Olliaro, P., W. R. Taylor, and J. Rigal. 2001. Controlling malaria: challenges and solutions. Trop. Med. Int. Health 6:922-927.
27. Paget-McNicol, S., and A. Saul. 2001. Mutation rates in the dihydrofolate reductase gene of Plasmodium falciparum. Parasitology 122:497-505.
28. Paul, R. E., M. J. Packer, M. Walmsley, M. Lagog, L. C. Ranford-Cartwright, R. Paru, and K. P. Day. 1995. Mating patterns in malaria parasite populations of Papua New Guinea. Science 269:1709-1711.
29. Payseur, B. A., A. D. Cutter, and M. W. Nachman. 2002. Searching for evidence of positive selection in the human genome using patterns of microsatellite variability. Mol. Biol. Evol. 19:1143-1153.
30. Plowe, C. V., J. F. Cortese, A. Djimde et al. (12 co-authors). 1997. Mutations in Plasmodium falciparum dihydrofolate reductase and dihydropteroate synthase and epidemiologic patterns of pyrimethamine-sulfadoxine use and resistance. J. Infect. Dis. 176:1590-1596.
31. Plowe, C. V., J. G. Kublin, and O. K. Doumbo. 1998. P. falciparum dihydrofolate reductase and dihydropteroate synthase mutations: epidemiology and role in clinical resistacne to antifolates. Drug Resist. Updates 1:389-396.
32. Polley, S. D., and D. J. Conway. 2001. Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 158:1505-1512.
33. Price, R. N., F. Nostén, C. Luxemburger, F. O. Ter Kuile, L. Paiphun, T. Chongsuphajaisiddhi, and N. J. White. 1996. Effects of artemisinin derivatives on malaria transmissibility. Lancet 347:1654-1658.
34. Roper, C., R. Pearce, B. Bredenkamp, J. Gumede, C. Drakeley, F. Mosha, D. Chandramohan, and B. Sharp. 2003. Antifolate antimalarial resistance in southeast Africa: a population-based analysis. Lancet 361:1174-1181.
35. Sabeti, P. C., D. E. Reich, J. M. Higgins et al. (17 co-authors). 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832-837.
36. Schlotterer, C. 2003. Hitchhiking mapping - functional genomics from the population genetics perspective. Trends Genet. 19:32-38.
37. Schrag, S. J., V. Perrot, and B. R. Levin. 1997. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc. R. Soc. Lond. B Biol. Sci. 264:1287-1291.
38. Sirawarapom, W., T. Sathitkul, R. Sirawarapom, Y. Yuthavong, and D. V. Santi. 1997. Antifolate-resistant mutants of Plasmodium falciparum dihydrofolate reductase. Proc. Natl. Acad. Sci. USA 94:1124-1129.
39. Smith, J. M., and J. Haigh. 1974. The hitch-hiking effect of a favourable gene. Genet. Res. 23:23-35.
40. Su, X., M. T. Ferdig, Y. Huang, C. Q. Huynh, A. Liu, J. You, J. C. Wootton, and T. E. Wellems. 1999. A genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum. Science 286:1351-1353.
41. Tishkoff, S. A., R. Varkonyi, N. Cahinhinan et al. (17 co-authors). 2001. Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science 293:455-462.
42. Vigouroux, Y., M. McMullen, C. T. Hittinger, K. Houchins, L. Schulz, S. Kresovich, Y. Matsuoka, and J. Doebley. 2002. Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. Proc. Natl. Acad. Sci. USA 99:9650-9655.
43. Volkman, S. K., D. L. Hartl, D. F. Wirth et al. (11 co-authors). 2002. Excess polymorphisms in genes for membrane proteins in Plasmodium falciparum. Science 298:216-218.
44. Watkins, W. M., E. K. Mberu, P. A. Winstanley, and C. V. Plowe. 1997. The efficacy of antifolate antimalarial combinations in Africa: a predictive model based on pharmacodynamic and pharmacokinetic analyses. Parasitol. Today 13:459-464.
45. White, N. J. 1992. Antimalarial drug resistance: the pace quickens. J. Antimicrob. Chemother. 30:571-585.
46. White, N. J., F. Nosten, S. Looareesuwan et al. (17 co-authors). 1999. Averting a malaria disaster. Lancet 353:1965-1967.
47. Wiehe, T. 1998. The effect of selective sweeps on the variance of the allele distribution of a linked multiallele locus: hitchhiking of microsatellites. Theor. Popul. Biol. 53:272-283.
48. Wootton, J. C., X. Feng, M. T. Ferdig, R. A. Cooper, J. Mu, D. I. Baruch, A. J. Magill, and X. Z. Su. 2002. Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418:320-323.