Sequence-based association and selection scans identify drug resistance loci in the Plasmodium falciparum malaria parasite

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 32, 2012, Pages 13052-13057

  Park, Daniel J ^a,b   Lukens, Amanda K ^a,c   Neafsey, Daniel E ^a   Schaffner, Stephen F ^a   Chang, Hsiao Han ^b   Valim, Clarissa ^c   Ribacke, Ulf ^c   Van Tyne, Daria ^c   Galinsky, Kevin ^a   Galligan, Meghan ^c   Becker, Justin S ^c   Ndiaye, Daouda ^d   Mboup, Souleymane ^d   Wiegand, Roger C ^a   Hartl, Daniel L ^a,b   Sabeti, Pardis C ^a,b   Wirth, Dyann F ^a,c   Volkman, Sarah K ^a,c,e  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITÉ CHEIKH ANTA DIOP   (Senegal)

^e SIMMONS COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMODIAQUINE; ARTEMISININ; ATOVAQUONE; BENFLUMETOL; CHLOROQUINE; DIHYDROARTEMISININ; HALOFANTRINE; MEFLOQUINE; MULTIDRUG RESISTANCE PROTEIN 1; PIPERAQUINE; PRIMAQUINE; PYRIMETHAMINE; QUININE;

ANTIMALARIAL DRUG RESISTANCE; ARTICLE; CONTROLLED STUDY; CROSS POPULATION EXTENDED HAPLOTYPE HOMOZYGOSITY TEST; DATA ANALYSIS; FEASIBILITY STUDY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC SCREENING; GENOME; HAPLOTYPE; HUMAN; IN VITRO STUDY; MICROARRAY ANALYSIS; NATURAL SELECTION; NONHUMAN; PLASMODIUM FALCIPARUM; POWER ANALYSIS; PRIORITY JOURNAL; SENEGAL; UBIQUITINATION;

BASE SEQUENCE; DRUG RESISTANCE; GENE FREQUENCY; GENETIC LOCI; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; LINKAGE DISEQUILIBRIUM; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PRINCIPAL COMPONENT ANALYSIS; SELECTION, GENETIC; SENEGAL; SEQUENCE ANALYSIS, DNA;

PLASMODIUM FALCIPARUM;

EID: 84864655057     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1210585109     Document Type: Article

References (48)

1. Murray CJL, et al. (2012) Global malaria mortality between 1980 and 2010: A systematic analysis. Lancet 379:413-431.
2. malERA Consultative Group on Drugs (2011) A research agenda for malaria eradication: Drugs. PLoS Med 8:e1000402.
3. Altshuler DM, Daly MJ, Lander ES (2008) Genetic mapping in human disease. Science 322:881-888.
4. de Bakker PIW, et al. (2005) Efficiency and power in genetic association studies. Nat Genet 37:1217-1223.
5. Mu J, et al. (2010) Plasmodium falciparum genome-wide scans for positive selection, recombination hot spots and resistance to antimalarial drugs. Nat Genet 42:268-271.
6. Van Tyne D, et al. (2011) Identification and functional validation of the novel antimalarial resistance locus PF10-0355 in Plasmodium falciparum. PLoS Genet 7:e1001383.
7. Yuan J, et al. (2011) Chemical genomic profiling for antimalarial therapies, response signatures, and molecular targets. Science 333:724-729.
8. Volkman SK, Neafsey DE, Schaffner SF, Park DJ, Wirth DF (2012) Harnessing genomics and genome biology to understand malaria biology. Nat Rev Genet 13:315-328.
9. Albrechtsen A, Nielsen FC, Nielsen R (2010) Ascertainment biases in SNP chips affect measures of population divergence. Mol Biol Evol 27:2534-2547.
10. Sabeti PC, et al.; International HapMap Consortium (2007) Genome-wide detection and characterization of positive selection in human populations. Nature 449:913-918.
11. Mouzin E, Thior PM, Diouf MB, Sambou B (2010) Focus on senegal. Progress & impact series, no. 4, (WHO, Geneva, Switzerland). Available at http://www.path.org/publications/detail.php?i=2072.
12. Oyola SO, et al. (2012) Optimizing Illumina next-generation sequencing library preparation for extremely AT-biased genomes. BMC Genomics 13:1.
13. Melnikov A, et al. (2011) Hybrid selection for sequencing pathogen genomes from clinical samples. Genome Biol 12:R73.
14. Kang HM, et al. (2008) Efficient control of population structure in model organism association mapping. Genetics 178:1709-1723.
15. Price AL, Zaitlen NA, Reich DE, Patterson N (2010) New approaches to population stratification in genome-wide association studies. Nat Rev Genet 11:459-463.
16. Fidock DA, et al. (2000) Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell 6:861-871.
17. Wootton JC, et al. (2002) Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418:320-323.
18. Duraisingh MT, et al. (2000) 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 108:13-23.
19. Nkhoma S, et al. (2009) Parasites bearing a single copy of the multi-drug resistance gene (pfmdr-1) with wild-type SNPs predominate amongst Plasmodium falciparum isolates from Malawi. Acta Trop 111:78-81.
20. Nair S, et al. (2003) A selective sweep driven by pyrimethamine treatment in southeast Asian malaria parasites. Mol Biol Evol 20:1526-1536.
21. Kessl JJ, Meshnick SR, Trumpower BL (2007) Modeling the molecular basis of atovaquone resistance in parasites and pathogenic fungi. Trends Parasitol 23:494-501.
22. Dong CK, et al. (2011) Identification and validation of tetracyclic benzothiazepines as Plasmodium falciparum cytochrome bc1 inhibitors. Chem Biol 18:1602-1610.
23. Cheeseman IH, et al. (2012) A major genome region underlying artemisinin resistance in malaria. Science 336:79-82.
24. Kudaravalli S, Veyrieras JB, Stranger BE, Dermitzakis ET, Pritchard JK (2009) Gene expression levels are a target of recent natural selection in the human genome. Mol Biol Evol 26:649-658.
25. Venkatesan M, et al. (2012) Using CF11 cellulose columns to inexpensively and effectively remove human DNA from Plasmodium falciparum-infected whole blood samples. Malar J 11:41.
26. Laufer MK, et al. (2010) Return of chloroquine-susceptible falciparum malaria in Malawi was a reexpansion of diverse susceptible parasites. J Infect Dis 202:801-808.
27. Aurrecoechea C, et al. (2009) PlasmoDB: A functional genomic database for malaria parasites. Nucleic Acids Res 37(Database issue):D539-D543.
28. Leprohon P, Légaré D, Ouellette M (2011) ABC transporters involved in drug resistance in human parasites. Essays Biochem 50:121-144.
29. Cui L, Miao J (2010) Chromatin-mediated epigenetic regulation in the malaria parasite Plasmodium falciparum. Eukaryot Cell 9:1138-1149.
30. Coleman BI, Duraisingh MT (2008) Transcriptional control and gene silencing in Plasmodium falciparum. Cell Microbiol 10:1935-1946.
31. Castellini MA, et al. (2011) Malaria drug resistance is associated with defective DNA mismatch repair. Mol Biochem Parasitol 177:143-147.
32. Tarique M, Satsangi AT, Ahmad M, Singh S, Tuteja R (2012) Plasmodium falciparum MLH is schizont stage specific endonuclease. Mol Biochem Parasitol 181:153-161.
33. Meng X, et al. (2012) Cytoplasmic Metadherin (MTDH) provides survival advantage under conditions of stress by acting as RNA-binding protein. J Biol Chem 287:4485-4491.
34. Ponts N, et al. (2008) Deciphering the ubiquitin-mediated pathway in apicomplexan parasites: A potential strategy to interfere with parasite virulence. PLoS ONE 3:e2386.
35. Jarosz DF, Lindquist S (2010) Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 330:1820-1824.
36. Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193:673-675.
37. Daniels R, et al. (2008) A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malar J 7:223.
38. McKenna A, et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297-1303.
39. Broad Institute (2012) Tagging simulation data, drug data, PLINK-formatted input data for both sequence and array data, recombination maps, imputed genotypes, GWAS outputs, and R code for generating all figures. Available at ftp://ftp.broadinstitute.org/pub/malaria/pnas-park-2012-suppfile-1. zip.
40. Broad Institute (2012) Consensus sequence calls for each of 45 strains and 23 million bases. VCF file is bgzip compressed and indexed by tabix and vcftools (.tbi and .vcfidx files are also in this directory). Available at ftp://ftp.broadinstitute.org/pub/malaria/pnas-park-2012-suppfile-2.vcf.gz.
41. Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2:e190.
42. Purcell S, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559-575.
43. Plouffe D, et al. (2008) In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen. Proc Natl Acad Sci USA 105:9059-9064.
44. Anderson TJC, et al. (2010) Inferred relatedness and heritability in malaria parasites. Proc Biol Sci 277:2531-2540.
45. Anderson TJC, et al. (2010) High heritability of malaria parasite clearance rate indicates a genetic basis for artemisinin resistance in western Cambodia. J Infect Dis 201:1326-1330.
46. McVean G, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231-1241.
47. Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162-1169.
48. Kurtz S, et al. (2004) Versatile and open software for comparing large genomes. Genome Biol 5:R12.