Genome-wide screen identifies new candidate genes associated with artemisinin susceptibility in Plasmodium falciparum in Kenya

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Borrmann, Steffen ^a,b   Straimer, Judith ^b,c   Mwai, Leah ^a,g   Abdi, Abdirahman ^a   Rippert, Anja ^b   Okombo, John ^a   Muriithi, Steven ^a   Sasi, Philip ^a   Kortok, Moses Mosobo ^a   Lowe, Brett ^a   Campino, Susana ^d   Assefa, Samuel ^d   Auburn, Sarah ^d   Manske, Magnus ^d   Maslen, Gareth ^d   Peshu, Norbert ^a   Kwiatkowski, Dominic P ^d,e   Marsh, Kevin ^a,f   Nzila, Alexis ^g   Clark, Taane G ^h  

^a KEMRI WELLCOME TRUST RESEARCH PROGRAMME   (Kenya)

^b Magdeburg University School of Medicine   (Germany)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g KING FAHD UNIVERSITY OF PETROLEUM AND MINERALS   (Saudi Arabia)

^h LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMALARIAL AGENT; ARTEMISININ DERIVATIVE; DIHYDROARTEMISININ; PROTOZOAL DNA;

DNA SEQUENCE; DRUG EFFECTS; DRUG RESISTANCE; DRUG SENSITIVITY; GENETICS; GENOME; HIGH THROUGHPUT SEQUENCING; HUMAN; ISOLATION AND PURIFICATION; KENYA; MALARIA, FALCIPARUM; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; SINGLE NUCLEOTIDE POLYMORPHISM;

ANTIMALARIALS; ARTEMISININS; BASE SEQUENCE; DNA, PROTOZOAN; DRUG RESISTANCE; GENOME, PROTOZOAN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; KENYA; MALARIA, FALCIPARUM; PARASITIC SENSITIVITY TESTS; PLASMODIUM FALCIPARUM; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA;

EID: 84888882898     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep03318     Document Type: Article

References (42)

1. Dondorp, A. M. et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361, 455-67 (2009).
2. Noedl, H. et al. Evidence of artemisinin-resistant malaria in western Cambodia. N Engl J Med 359, 2619-20 (2008).
3. Phyo, A. P. et al. Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet (2012).
4. Eastman, R. T. & Fidock, D. A. Artemisinin-based combination therapies: a vital tool in efforts to eliminate malaria. Nat Rev Microbiol 7, 864-74 (2009).
5. Nayyar, G., Breman, J., Newton, P. & Herrington, J. Poor-quality antimalarial drugs in southeast Asia and sub-Saharan Africa. Lancet Infect Dis 12, 488-496 (2012).
6. Rathod, P. K., McErlean, T. & Lee, P. C. Variations in frequencies of drug resistance in Plasmodium falciparum. Proc Natl Acad Sci USA 94, 9389-93 (1997). (Pubitemid 27357839)
7. Bjorkman, J., Nagaev, I., Berg, O. G., Hughes, D. & Andersson, D. I. Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287, 1479-82 (2000). (Pubitemid 30127140)
8. Mackinnon, M. J. & Marsh, K. The selection landscape of malaria parasites. Science 328, 866-71 (2010).
9. Borrmann, S. et al. Declining responsiveness of Plasmodium falciparum infections to artemisinin-based combination treatments on the Kenyan coast. PLoS ONE 6, e26005 (2011).
10. Sidhu, A. B. et al. Decreasing pfmdr1 copy number in plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin. J Infect Dis 194, 528-35 (2006). (Pubitemid 44162666)
11. Wongsrichanalai, C., Pickard, A. L., Wernsdorfer, W. H. & Meshnick, S. R. Epidemiology of drug-resistant malaria. Lancet Infect Dis 2, 209-18 (2002). (Pubitemid 34464751)
12. Witkowski, B. et al. Novel phenotypic assays for the detection of artemisininresistant Plasmodium falciparum malaria in Cambodia: in-vitro and ex-vivo drug-response studies. Lancet Infect Dis (2013).
13. Gardner, M. J. et al.Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498-511 (2002).
14. van Schalkwyk, D. A. et al. Culture-adapted Plasmodium falciparum isolates from UK travellers: in vitro drug sensitivity, clonality and drug resistance markers. Malar J 12, 320 (2013).
15. Hunt, P. et al. Experimental evolution, genetic analysis and genome re-sequencing reveal the mutation conferring artemisinin resistance in an isogenic lineage of malaria parasites. BMC Genomics 11, 499 (2010).
16. Gibney, P. A., Fries, T., Bailer, S. M. & Morano, K. A. Rtr1 is the Saccharomyces cerevisiae homolog of a novel family of RNA polymerase II-binding proteins. Eukaryot Cell 7, 938-48 (2008). (Pubitemid 351961573)
17. Price, R. N. et al. Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet 364, 438-47 (2004). (Pubitemid 39036891)
18. Yuan, J. et al. Chemical genomic profiling for antimalarial therapies, response signatures, and molecular targets. Science 333, 724-9 (2011).
19. Wootton, J. C. et al. Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418, 320-3 (2002). (Pubitemid 34790681)
20. Roper, C. et al. Intercontinental spread of pyrimethamine-resistant malaria. Science 305, 1124 (2004). (Pubitemid 39100317)
21. Su, X. et al. A genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum. Science 286, 1351-3 (1999).
22. Bethke, L. L. et al. Duplication, gene conversion, and genetic diversity in the species-specific acyl-CoA synthetase gene family of Plasmodium falciparum. Mol Biochem Parasitol 150, 10-24 (2006). (Pubitemid 44332573)
23. Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913-8 (2007). (Pubitemid 47598625)
24. Mu, J. et al. Plasmodium falciparum genome-wide scans for positive selection, recombination hot spots and resistance to antimalarial drugs. Nat Genet 42, 268-71 (2010).
25. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-95 (1989). (Pubitemid 19274682)
26. Amambua-Ngwa, A. et al. SNP genotyping identifies new signatures of selection in a deep sample of West African Plasmodium falciparum malaria parasites. Mol Biol Evol 29, 3249-53 (2012).
27. Fidock, D. A. et al. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell 6, 861-71 (2000).
28. Sidhu, A. B., Verdier-Pinard, D. & Fidock, D. A. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 298, 210-3 (2002).
29. Hunt, P. et al.Gene encoding a deubiquitinating enzyme is mutated in artesunateand chloroquine-resistant rodent malaria parasites. Mol Microbiol 65, 27-40 (2007). (Pubitemid 46934481)
30. Cheeseman, I. H. et al. A major genome region underlying artemisinin resistance in malaria. Science 336, 79-82 (2012).
31. Mok, S. et al. Artemisinin resistance in Plasmodium falciparum is associated with an altered temporal pattern of transcription. BMC Genomics 12, 391 (2011).
32. Prieto, J. H., Koncarevic, S., Park, S. K., Yates, J. 3rd & Becker, K. Large-scale differential proteome analysis in Plasmodium falciparum under drug treatment. PLoS ONE 3, e4098 (2008).
33. Dondorp, A. M. et al. Artemisinin resistance: current status and scenarios for containment. Nat Rev Microbiol 8, 272-80.
34. Mwai, L. et al. Chloroquine resistance before and after its withdrawal in Kenya. Malar J 8, 106 (2009).
35. Anderson, T., Nkhoma, S., Ecker, A. & Fidock, D. How can we identify parasite genes that underlie antimalarial drug resistance? Pharmacogenomics 12, 59-85 (2011).
36. DeCoursey, T. E., Chandy, K. G., Gupta, S. & Cahalan, M. D. Voltage-gated K1 channels in human T lymphocytes: a role in mitogenesis? Nature 307, 465-8 (1984).
37. Olotu,A. et al.Defining clinical malaria: the specificity and incidence of endpoints from active and passive surveillance of children in rural Kenya. PLoS ONE 5, e15569 (2010).
38. Van Tyne, D. et al. Identification and functional validation of the novel antimalarial resistance locus PF10-0355 in Plasmodium falciparum. PLoS Genet 7, e1001383 (2011).
39. Park, D. J. et al. Sequence-based association and selection scans identify drug resistance loci in the Plasmodium falciparum malaria parasite. Proc Natl Acad Sci USA 109, 13052-7 (2012).
40. Manske, M. et al. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 487, 375-9 (2012).
41. Robinson, T. et al. Drug-resistant genotypes and multi-clonality in Plasmodium falciparum analysed by direct genome sequencing from peripheral blood of malaria patients. PLoS ONE 6, e23204 (2011).
42. MalariaGen. Sequence Read Archive. (Accessed on 10 Oct 2013). http://www.malariagen.net/data/sequence-read-archive.