Association mapping by pooled sequencing identifies TOLL 11 as a protective factor against Plasmodium falciparum in Anopheles gambiae

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Redmond, Seth N ^a,b   Eiglmeier, Karin ^a,b   Mitri, Christian ^a,b   Markianos, Kyriacos ^c   Guelbeogo, Wamdaogo M ^d   Gneme, Awa ^d   Isaacs, Alison T ^a,b   Coulibaly, Boubacar ^e   Brito Fravallo, Emma ^a,b   Maslen, Gareth ^f,g   Mead, Daniel ^f,g   Niare, Oumou ^e   Traore, Sekou F ^e   Sagnon, N'Fale ^d   Kwiatkowski, Dominic ^f,g   Riehle, Michelle M ^h   Vernick, Kenneth D ^a,b,e  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d Burkina Faso   (Burkina Faso)

^e UNIVERSITY OF BAMAKO   (Mali)

^f WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^g UNIVERSITY OF OXFORD   (United Kingdom)

^h UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Genetic analysis; GWAS; Host pathogen interaction; Malaria; Mosquito; Pooled sequencing; Population genomics

Indexed keywords

PROTOZOAL DNA; PROTOZOAL RNA; TOLL LIKE RECEPTOR;

ADULT; AFRICA; ANIMAL EXPERIMENT; ANOPHELES GAMBIAE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENE MAPPING; GENE POOL; GENE REPLICATION; GENE SEQUENCE; GENE SILENCING; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; NONHUMAN; PARASITE LOAD; PHENOTYPE; PLASMODIUM FALCIPARUM; RNA INTERFERENCE; TOLL 11 GENE; ANIMAL; CHROMOSOMAL MAPPING; GENETICS; HOST PARASITE INTERACTION; HUMAN; INSECT GENOME; INSECT VECTOR; MALARIA FALCIPARUM; PARASITOLOGY; PATHOGENICITY; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSMISSION;

ANIMALS; ANOPHELES GAMBIAE; CHROMOSOME MAPPING; GENOME, INSECT; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HOST-PARASITE INTERACTIONS; HUMANS; INSECT VECTORS; MALARIA, FALCIPARUM; PHENOTYPE; PLASMODIUM FALCIPARUM; POLYMORPHISM, SINGLE NUCLEOTIDE; TOLL-LIKE RECEPTORS;

EID: 84945219062     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-2009-z     Document Type: Article

References (47)

1. Menge DM, Zhong D, Guda T, Gouagna LC, Githure JI, Beier J, et al. Quantitative Trait Loci Controlling Refractoriness to Plasmodium falciparum in Natural Anopheles gambiae from a Malaria Endemic Region in Western Kenya. Genetics. 2006;173(1):235-41
2. Riehle MM, Markianos K, Lambrechts L, Xia A, Sharakhov I, Koella JC, et al. A major genetic locus controlling natural Plasmodium falciparum infection is shared by East and West African Anopheles gambiae. Malar J. 2007;6:87
3. Riehle MM, Markianos K, Niaré O, Xu J, Li J, Touré AM, et al. Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science. 2006;312:577-9
4. Collins FH, Sakai RK, Vernick KD, Paskewitz S, Seeley DC, Miller LH, et al. Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science. 1986;234(4776):607-10
5. Dunstan SJ, Rockett KA, Quyen NTN, Teo YY, Thai CQ, Hang NT, et al. Variation in human genes encoding adhesion and proinflammatory molecules are associated with severe malaria in the Vietnamese. Genes and immunity. 2012;13:503-8
6. Jallow M, Teo YY, Small KS, Rockett KA, Deloukas P, Clark TG, et al. Genomewide and fine-resolution association analysis of malaria in West Africa. Nature genetics. 2009;41:657-65
7. Van Tyne D, Park DJ, Schaffner SF, Neafsey DE, Angelino E, Cortese JF, et al. Identification and functional validation of the novel antimalarial resistance locus PF10_0355 in Plasmodium falciparum. PLoS genetics. 2011;7:e1001383
8. Harris C, Lambrechts L, Rousset F, Abate L, Nsango SE, Fontenille D, et al. Polymorphisms in Anopheles gambiae immune genes associated with natural resistance to Plasmodium falciparum. PLoS Pathog. 2010;6
9. Horton AA, Lee Y, Coulibaly CA, Rashbrook VK, Cornel AJ, Lanzaro GC, et al. Identification of three single nucleotide polymorphisms in Anopheles gambiae immune signaling genes that are associated with natural Plasmodium falciparum infection. Malaria journal. 2010;9:160
10. Neafsey DE, Lawniczak MKN, Park DJ, Redmond SN, Coulibaly MB, Traoré SF, et al. SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science (New York, NY). 2010;330:514-7
11. Crawford JE, Bischoff E, Garnier T, Gneme A, Eiglmeier K, Holm I, et al. Evidence for population-specific positive selection on immune genes of Anopheles gambiae. G3 (Bethesda, Md). 2012;2:1505-19
12. Wilding CS, Weetman D, Steen K, Donnelly MJ. High, clustered, nucleotide diversity in the genome of Anopheles gambiae revealed through pooledtemplate sequencing: implications for high-throughput genotyping protocols. BMC genomics. 2009;10:320
13. King EG, Macdonald SJ, Long AD. Properties and power of the Drosophila Synthetic Population Resource for the routine dissection of complex traits. Genetics. 2012;191:935-49
14. King EG, Merkes CM, McNeil CL, Hoofer SR, Sen S, Broman KW, et al. Genetic dissection of a model complex trait using the Drosophila Synthetic Population Resource. Genome research. 2012;22:1558-66
15. Svenson KL, Gatti DM, Valdar W, Welsh CE, Cheng R, Chesler EJ, et al. Highresolution genetic mapping using the Mouse Diversity outbred population. Genetics. 2012;190:437-47
16. Valdar W, Solberg LC, Gauguier D, Burnett S, Klenerman P, Cookson WO, et al. Genome-wide genetic association of complex traits in heterogeneous stock mice. Nature genetics. 2006;38:879-87
17. Hastbacka J, de la Chapelle A, Kaitila I, Sistonen P, Weaver A, Lander E. Linkage disequilibrium mapping in isolated founder populations: diastrophic dysplasia in Finland. Nature genetics. 1992;2(3):204-11
18. Kong A, Masson G, Frigge ML, Gylfason A, Zusmanovich P, Thorleifsson G, et al. Detection of sharing by descent, long-range phasing and haplotype imputation. Nature genetics. 2008;40(9):1068-75
19. Boehnke M. Limits of resolution of genetic linkage studies: implications for the positional cloning of human disease genes. Am J Hum Genet. 1994;55:379-90
20. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, et al. The genome sequence of the malaria mosquito Anopheles gambiae. Science. 2002;298:129-49
21. Christophides GGK, Zdobnov E, Blass C, Brey PT, Collins FH, Danielli A, et al. Immunity-related genes and gene families in Anopheles gambiae. Science (New York, NY). 2002;159:159-65
22. Valanne S, Wang J-H, Rämet M. The Drosophila Toll signaling pathway. Journal of immunology (Baltimore, Md: 1950). 2011;186:649-56
23. Garver LS, Bahia AC, Das S, Souza-Neto JA, Shiao J, Dong Y, et al. Anopheles Imd pathway factors and effectors in infection intensity-dependent anti-Plasmodium action. PLoS pathogens. 2012;8:e1002737
24. Mitri C, Jacques J-C, Thiery I, Riehle MM, Xu J, Bischoff E, et al. Fine pathogen discrimination within the APL1 gene family protects Anopheles gambiae against human and rodent malaria species. PLoS pathogens. 2009;5:e1000576
25. Tauszig S, Jouanguy E, Hoffmann JA, Imler JL. Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2000;97:10520-5
26. Nakamoto M, Moy RH, Xu J, Bambina S, Yasunaga A, Shelly SS, et al. Virus recognition by Toll-7 activates antiviral autophagy in Drosophila. Immunity. 2012;36:658-67
27. Ramirez JL, Dimopoulos G. The Toll immune signaling pathway control conserved anti-dengue defenses across diverse Ae. aegypti strains and against multiple dengue virus serotypes. Developmental and comparative immunology. 2010;34:625-9
28. Shin SW, Bian G, Raikhel AS. A toll receptor and a cytokine, Toll5A and Spz1C, are involved in toll antifungal immune signaling in the mosquito Aedes aegypti. The Journal of biological chemistry. 2006;281:39388-95
29. Goltsev Y, Rezende GL, Vranizan K, Lanzaro G, Valle D, Levine M. Developmental and evolutionary basis for drought tolerance of the Anopheles gambiae embryo. Developmental biology. 2009;330:462-70
30. Marinotti O, Calvo E, Nguyen QK, Dissanayake S, Ribeiro JMC, James AA. Genome-wide analysis of gene expression in adult Anopheles gambiae. Insect molecular biology. 2006;15:1-12
31. Mendes AM, Awono-Ambene PH, Nsango SE, Cohuet A, Fontenille D, Kafatos FC, et al. Infection intensity-dependent responses of Anopheles gambiae to the African malaria parasite Plasmodium falciparum. Infection and immunity. 2011;79:4708-15
32. Riehle MM, Guelbeogo WM, Gneme A, Eiglmeier K, Holm I, Bischoff E, et al. A cryptic subgroup of Anopheles gambiae is highly susceptible to human malaria parasites. Science. 2011;331:596-8
33. Rousset F. GENEPOP'007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources. 2008;8:103-6
34. Kumar S, Tamura K, Jakobsen IB, Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics. 2001;17(12):1244-5
35. Ponnudurai T, Lensen AH, Leeuwenberg AD, Meuwissen JH. Cultivation of fertile Plasmodium falciparum gametocytes in semi-automated systems. 1. Static cultures. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1982;76:812-8
36. Singer VL, Jones LJ, Yue ST, Haugland RP. Characterization of PicoGreen reagent and development of a fluorescence-based solution assay for double-stranded DNA quantitation. Anal Biochem. 1997;249(2):228-38
37. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome biology. 2009;10:R25
38. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics (Oxford, England). 2009;25:2078-9
39. Qanbari S, Strom TM, Haberer G, Weigend S, Gheyas AA, Turner F, Burt DW, Preisinger R, Gianola D. Simianer H: A High Resolution Genome-Wide Scan for Significant Selective Sweeps: An Application to Pooled Sequence Data in Laying Chickens PLoS ONE. 2012;7:e49525
40. Reimers M, Carey VJ. Bioconductor: an open source framework for bioinformatics and computational biology. Methods Enzymol. 2006;411:119-34
41. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. American journal of human genetics. 2007;81:559-75
42. Schlotterer C, Tobler R, Kofler R, Nolte V. Sequencing pools of individuals-mining genome-wide polymorphism data without big funding. Nature reviews Genetics. 2014;15(11):749-63
43. McLaren W, Pritchard B, Rios D, Chen Y, Flicek P, Cunningham F. Deriving the consequences of genomic variants with the Ensembl API and SNP Effect Predictor. Bioinformatics (Oxford, England). 2010;26:2069-70
44. Megy K, Emrich SJ, Lawson D, Campbell D, Dialynas E, Hughes DST, et al. VectorBase: improvements to a bioinformatics resource for invertebrate vector genomics. Nucleic acids research. 2012;40:D729-34
45. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome biology. 2004;5:R80
46. Lobo NF, Sangaré DM, Regier AA, Reidenbach KR, Bretz DA, Sharakhova MV, et al. Breakpoint structure of the Anopheles gambiae 2Rb chromosomal inversion. Malaria journal. 2010;9:293
47. Fisher RA. Statistical Methods for Research Workers. Edinburgh: Oliver & Boyd; 1954