Avian Toll-like receptor allelic diversity far exceeds human polymorphism: an insight from domestic chicken breeds
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu srovnávací studie, časopisecké články, práce podpořená grantem
Grantová podpora
504214
Grantová Agentura, Univerzita Karlova (Charles University Grant Agency) - International
504214
Grantová Agentura, Univerzita Karlova (Charles University Grant Agency) - International
204069
Univerzita Karlova v Praze (Charles University) - International
204069
Univerzita Karlova v Praze (Charles University) - International
PRIMUS/17/SCI/12
Univerzita Karlova v Praze (Charles University) - International
SVV 260434/2018
Ministerstvo Školství, Mládeže a Tělovýchovy (Ministry of Education, Youth and Sports) - International
INTER-COST LTC18060
Ministerstvo Školství, Mládeže a Tělovýchovy (Ministry of Education, Youth and Sports) - International
SVV 260434/2018
Ministerstvo Školství, Mládeže a Tělovýchovy (Ministry of Education, Youth and Sports) - International
P502/12/P179
Grantová Agentura České Republiky (Grant Agency of the Czech Republic) - International
PubMed
30552359
PubMed Central
PMC6294777
DOI
10.1038/s41598-018-36226-1
PII: 10.1038/s41598-018-36226-1
Knihovny.cz E-zdroje
- MeSH
- frekvence genu MeSH
- genetická variace * MeSH
- kur domácí * MeSH
- lidé MeSH
- sekvenční analýza DNA MeSH
- toll-like receptory genetika MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- srovnávací studie MeSH
- Názvy látek
- toll-like receptory MeSH
Immune genes show remarkable levels of adaptive variation shaped by pathogen-mediated selection. Compared to humans, however, population polymorphism in animals has been understudied. To provide an insight into immunogenetic diversity in birds, we sequenced complete protein-coding regions of all Toll-like receptor (TLR) genes with direct orthology between mammals and birds (TLR3, TLR4, TLR5 and TLR7) in 110 domestic chickens from 25 breeds and compared their variability with a corresponding human dataset. Chicken TLRs (chTLRs) exhibit on average nine-times higher nucleotide diversity than human TLRs (hTLRs). Increased potentially functional non-synonymous variability is found in chTLR ligand-binding ectodomains. While we identified seven sites in chTLRs under positive selection and found evidence for convergence between alleles, no selection or convergence was detected in hTLRs. Up to six-times more alleles were identified in fowl (70 chTLR4 alleles vs. 11 hTLR4 alleles). In chTLRs, high numbers of alleles are shared between the breeds and the allelic frequencies are more equal than in hTLRs. These differences may have an important impact on infectious disease resistance and host-parasite co-evolution. Though adaptation through high genetic variation is typical for acquired immunity (e.g. MHC), our results show striking levels of intraspecific polymorphism also in poultry innate immune receptors.
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Darwin, C. The Variation of Animals and Plants Under Domestication. (Murray J., 1868). PubMed PMC
Huang YQ, et al. Haplotypic variation and characteristics across the toll-like receptor 3 locus in chickens. Anim. Genet. 2012;43:343–347. doi: 10.1111/j.1365-2052.2011.02244.x. PubMed DOI
Ruan W, Wu Y, Zheng SJ. Different genetic patterns in avian Toll-like receptor (TLR)5 genes. Mol. Biol. Rep. 2012;39:3419–3426. doi: 10.1007/s11033-011-1113-7. PubMed DOI
Ruan W, An J, Wu Y. Polymorphisms of Chicken TLR3 and 7 in Different Breeds. PLoS ONE. 2015;10:e0119967. doi: 10.1371/journal.pone.0119967. PubMed DOI PMC
Ruan WK, Wu YH, An J, Zheng SJ. Polymorphisms of chicken Toll-like receptors 4, 15, and 21 in different breeds. Poult. Sci. 2012;91:2512–2516. doi: 10.3382/ps.2012-02319. PubMed DOI
Hillel J, et al. Biodiversity of 52 chicken populations assessed by microsatellite typing of DNA pools. Genet. Sel. Evol. GSE. 2003;35:533–557. doi: 10.1186/1297-9686-35-6-533. PubMed DOI PMC
Muir WM, et al. Genome-wide assessment of worldwide chicken SNP genetic diversity indicates significant absence of rare alleles in commercial breeds. Proc. Natl. Acad. Sci. 2008;105:17312–17317. doi: 10.1073/pnas.0806569105. PubMed DOI PMC
Lyimo CM, et al. Global diversity and genetic contributions of chicken populations from African, Asian and European regions. Anim. Genet. 2014;45:836–848. doi: 10.1111/age.12230. PubMed DOI
Lyimo CM, et al. Maternal genealogical patterns of chicken breeds sampled in Europe. Anim. Genet. 2015;46:447–451. doi: 10.1111/age.12304. PubMed DOI
Weigend S, Romanov M. n. Current strategies for the assessment and evaluation of genetic diversity in chicken resources. Worlds Poult. Sci. J. 2001;57:275–288. doi: 10.1079/WPS20010020. DOI
Delany, M. E. Genetic diversity and conservation of poultry. In Poultry genetics, breeding, and biotechnology (eds. Muir, W. M. & Aggrey, S. E.) 257–281 (CABI Pub, 2003).
Groeneveld LF, et al. Genetic diversity in farm animals – a review. Anim. Genet. 2010;41:6–31. doi: 10.1111/j.1365-2052.2010.02038.x. PubMed DOI
Sachidanandam R, et al. A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature. 2001;409:928–933. doi: 10.1038/35057149. PubMed DOI
Wong GK-S, et al. A genetic variation map for chicken with 2.8 million single-nucleotide polymorphisms. Nature. 2004;432:717–722. doi: 10.1038/nature03156. PubMed DOI PMC
Vinkler M, Albrecht T. The question waiting to be asked: Innate immunity receptors in the perspective of zoological research. Folia Zool. 2009;58:15–28.
Medzhitov R. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 2001;1:135–145. doi: 10.1038/35100529. PubMed DOI
Kang, J. Y. & Lee, J.-O. Structural Biology of the Toll-Like Receptor Family. In Annual Review of Biochemistry, Vol. 80 (eds. Kornberg, R. D., Raetz, C. R. H., Rothman, J. E. & Thorner, J. W.) 80, 917–941 (Annual Reviews, 2011). PubMed
Velová, H., Gutowska-Ding, M. W., Burt, D. W. & Vinkler, M. Toll-like receptor evolution in birds: gene duplication, pseudogenisation and diversifying selection. Mol. Biol. Evol. 39, 2170–2184 (2018). PubMed PMC
Cormican P, et al. The avian Toll-Like receptor pathway–subtle differences amidst general conformity. Dev. Comp. Immunol. 2009;33:967–973. doi: 10.1016/j.dci.2009.04.001. PubMed DOI
Karpala AJ, Lowenthal JW, Bean AG. Activation of the TLR3 pathway regulates IFNβ production in chickens. Dev. Comp. Immunol. 2008;32:435–444. doi: 10.1016/j.dci.2007.08.004. PubMed DOI
Schwarz H, et al. Chicken toll-like receptor 3 recognizes its cognate ligand when ectopically expressed in human cells. J. Interferon Cytokine Res. 2007;27:97–101. doi: 10.1089/jir.2006.0098. PubMed DOI
Keestra AM, Putten JPM. van. Unique Properties of the Chicken TLR4/MD-2 Complex: Selective Lipopolysaccharide Activation of the MyD88-Dependent Pathway. J. Immunol. 2008;181:4354–4362. doi: 10.4049/jimmunol.181.6.4354. PubMed DOI
Kogut MH, et al. Expression and function of Toll-like receptors in chicken heterophils. Dev. Comp. Immunol. 2005;29:791–807. doi: 10.1016/j.dci.2005.02.002. PubMed DOI
Iqbal M, et al. Identification and functional characterization of chicken toll-like receptor 5 reveals a fundamental role in the biology of infection with Salmonella enterica serovar typhimurium. Infect. Immun. 2005;73:2344–2350. doi: 10.1128/IAI.73.4.2344-2350.2005. PubMed DOI PMC
Keestra AM, de Zoete MR, van Aubel RAMH, van Putten JPM. Functional characterization of chicken TLR5 reveals species-specific recognition of flagellin. Mol. Immunol. 2008;45:1298–1307. doi: 10.1016/j.molimm.2007.09.013. PubMed DOI
Philbin VJ, et al. Identification and characterization of a functional, alternatively spliced Toll-like receptor 7 (TLR7) and genomic disruption of TLR8 in chickens. Immunology. 2005;114:507–521. doi: 10.1111/j.1365-2567.2005.02125.x. PubMed DOI PMC
Temperley ND, Berlin S, Paton IR, Griffin DK, Burt DW. Evolution of the chicken Toll-like receptor gene family: A story of gene gain and gene loss. BMC Genomics. 2008;9:62. doi: 10.1186/1471-2164-9-62. PubMed DOI PMC
Yilmaz A, Shen S, Adelson DL, Xavier S, Zhu JJ. Identification and sequence analysis of chicken Toll-like receptors. Immunogenetics. 2005;56:743–753. doi: 10.1007/s00251-004-0740-8. PubMed DOI
Higgs R, et al. Induction of a novel chicken Toll-like receptor following Salmonella enterica serovar Typhimurium infection. Infect. Immun. 2006;74:1692–1698. doi: 10.1128/IAI.74.3.1692-1698.2006. PubMed DOI PMC
Roach JC, et al. The evolution of vertebrate Toll-like receptors. Proc. Natl. Acad. Sci. USA. 2005;102:9577–9582. doi: 10.1073/pnas.0502272102. PubMed DOI PMC
Tanji H, Ohto U, Shibata T, Miyake K, Shimizu T. Structural reorganization of the Toll-like receptor 8 dimer induced by agonistic ligands. Science. 2013;339:1426–1429. doi: 10.1126/science.1229159. PubMed DOI
Tanji H, et al. Toll-like receptor 8 senses degradation products of single-stranded RNA. Nat. Struct. Mol. Biol. 2015;22:109–115. doi: 10.1038/nsmb.2943. PubMed DOI
Shibata T, et al. Guanosine and its modified derivatives are endogenous ligands for TLR7. Int. Immunol. 2016;28:211–222. doi: 10.1093/intimm/dxv062. PubMed DOI PMC
Zhang Z, et al. Structural Analysis Reveals that Toll-like Receptor 7 Is a Dual Receptor for Guanosine and Single-Stranded RNA. Immunity. 2016;45:737–748. doi: 10.1016/j.immuni.2016.09.011. PubMed DOI
Reddick LE, Alto NM. Bacteria Fighting Back: How Pathogens Target and Subvert the Host Innate Immune System. Mol. Cell. 2014;54:321–328. doi: 10.1016/j.molcel.2014.03.010. PubMed DOI PMC
Alcaide M, Edwards SV. Molecular Evolution of the Toll-Like Receptor Multigene Family in Birds. Mol. Biol. Evol. 2011;28:1703–1715. doi: 10.1093/molbev/msq351. PubMed DOI
Downing T, Lloyd AT, O’Farrelly C, Bradley DG. The Differential Evolutionary Dynamics of Avian Cytokine and TLR Gene Classes. J. Immunol. 2010;184:6993–7000. doi: 10.4049/jimmunol.0903092. PubMed DOI
Smirnova I, Poltorak A, Chan EK, McBride C, Beutler B. Phylogenetic variation and polymorphism at the Toll-like receptor 4 locus (TLR4) Genome Biol. 2000;1:research002. doi: 10.1186/gb-2000-1-1-research002. PubMed DOI PMC
Vinkler M, Bryjová A, Albrecht T, Bryja J. Identification of the first Toll-like receptor gene in passerine birds: TLR4 orthologue in zebra finch (Taeniopygia guttata) Tissue Antigens. 2009;74:32–41. doi: 10.1111/j.1399-0039.2009.01273.x. PubMed DOI
Vinkler M, Bainová H, Bryja J. Protein evolution of Toll-like receptors 4, 5 and 7 within Galloanserae birds. Genet. Sel. Evol. 2014;46:72. doi: 10.1186/s12711-014-0072-6. PubMed DOI PMC
Beaumont C, et al. Effect of two candidate genes on the Salmonella carrier state in fowl. Poult. Sci. 2003;82:721–726. doi: 10.1093/ps/82.5.721. PubMed DOI
Leveque G, et al. Allelic Variation in TLR4 Is Linked to Susceptibility to Salmonella enterica Serovar Typhimurium Infection in Chickens. Infect. Immun. 2003;71:1116–1124. doi: 10.1128/IAI.71.3.1116-1124.2003. PubMed DOI PMC
The 1000 Genomes Project Consortium. A global reference for human genetic variation. Nature526, 68–74 (2015). PubMed PMC
Miao Y-W, et al. Chicken domestication: an updated perspective based on mitochondrial genomes. Heredity. 2013;110:277–282. doi: 10.1038/hdy.2012.83. PubMed DOI PMC
Tixier-Boichard M, Bed’hom B, Rognon X. Chicken domestication: from archeology to genomics. C. R. Biol. 2011;334:197–204. doi: 10.1016/j.crvi.2010.12.012. PubMed DOI
Larson G, Fuller DQ. The Evolution of Animal Domestication. Annu. Rev. Ecol. Evol. Syst. 2014;45:115–136. doi: 10.1146/annurev-ecolsys-110512-135813. DOI
Van Reeth K. Avian and swine influenza viruses: our current understanding of the zoonotic risk. Vet. Res. 2007;38:243–260. doi: 10.1051/vetres:2006062. PubMed DOI
Guard-Petter J. The chicken, the egg and Salmonella enteritidis. Environ. Microbiol. 2001;3:421–430. doi: 10.1046/j.1462-2920.2001.00213.x. PubMed DOI
Hermans D, et al. Poultry as a Host for the Zoonotic Pathogen Campylobacter jejuni. Vector-Borne Zoonotic Dis. 2012;12:89–98. doi: 10.1089/vbz.2011.0676. PubMed DOI
Stanley J, et al. Helicobacter pullorum sp. nov.-genotype and phenotype of a new species isolated from poultry and from human patients with gastroenteritis. Microbiol. Read. Engl. 1994;140(Pt 12):3441–3449. doi: 10.1099/13500872-140-12-3441. PubMed DOI
Javed S, Gul F, Javed K, Bokhari H. Helicobacter pullorum: An Emerging Zoonotic Pathogen. Front. Microbiol. 2017;8:604. doi: 10.3389/fmicb.2017.00604. PubMed DOI PMC
Hampson DJ. The Spirochete Brachyspira pilosicoli, Enteric Pathogen of Animals and Humans. Clin. Microbiol. Rev. 2018;31(UNSP):e00087–17. PubMed PMC
Barrow PA. The paratyphoid salmonellae. Rev. Sci. Tech. Int. Off. Epizoot. 2000;19:351–375. doi: 10.20506/rst.19.2.1225. PubMed DOI
Georgel, P., Macquin, C. & Bahram, S. The Heterogeneous Allelic Repertoire of Human Toll-Like Receptor (TLR) Genes. PLoS ONE4, (2009). PubMed PMC
Barreiro, L. B. et al. Evolutionary Dynamics of Human Toll-Like Receptors and Their Different Contributions to Host Defense. PLoS Genet. 5, (2009). PubMed PMC
Buhler S, Sanchez-Mazas A. HLA DNA Sequence Variation among Human Populations: Molecular Signatures of Demographic and Selective Events. PLOS ONE. 2011;6:e14643. doi: 10.1371/journal.pone.0014643. PubMed DOI PMC
Wang Y, et al. Sequence variations of the MHC class I gene exon 2 and exon 3 between infected and uninfected chickens challenged with Marek’s disease virus. Infect. Genet. Evol. 2014;21:103–109. doi: 10.1016/j.meegid.2013.10.020. PubMed DOI
Worley K, et al. Single locus typing of MHC class I and class II B loci in a population of red jungle fowl. Immunogenetics. 2008;60:233–247. doi: 10.1007/s00251-008-0288-0. PubMed DOI
Li WH, Sadler LA. Low nucleotide diversity in man. Genetics. 1991;129:513–523. PubMed PMC
Zhao Z, Yu N, Fu Y-X, Li W-H. Nucleotide Variation and Haplotype Diversity in a 10-kb Noncoding Region in Three Continental Human Populations. Genetics. 2006;174:399–409. doi: 10.1534/genetics.106.060301. PubMed DOI PMC
Gagneux P, et al. Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proc. Natl. Acad. Sci. 1999;96:5077–5082. doi: 10.1073/pnas.96.9.5077. PubMed DOI PMC
Fornuskova A, Bryja J, Vinkler M, Macholán M, Piálek J. Contrasting patterns of polymorphism and selection in bacterial-sensing toll-like receptor 4 in two house mouse subspecies. Ecol. Evol. 2014;4:2931–2944. doi: 10.1002/ece3.1137. PubMed DOI PMC
Wlasiuk G, Khan S, Switzer WM, Nachman MW. A History of Recurrent Positive Selection at the Toll-Like Receptor 5 in Primates. Mol. Biol. Evol. 2009;26:937–949. doi: 10.1093/molbev/msp018. PubMed DOI PMC
Bainová H, et al. First evidence of independent pseudogenization of Toll-like receptor 5 in passerine birds. Dev. Comp. Immunol. 2014;45:151–155. doi: 10.1016/j.dci.2014.02.010. PubMed DOI
Hillier LW, et al. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004;432:695–716. doi: 10.1038/nature03154. PubMed DOI
Boyd A, Philbin VJ, Smith AL. Conserved and distinct aspects of the avian Toll-like receptor (TLR) system: implications for transmission and control of bird-borne zoonoses. Biochem. Soc. Trans. 2007;35:1504–1507. doi: 10.1042/BST0351504. PubMed DOI
Ohto U, Fukase K, Miyake K, Shimizu T. Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/MD-2. Proc. Natl. Acad. Sci. USA. 2012;109:7421–7426. doi: 10.1073/pnas.1201193109. PubMed DOI PMC
Park BS, et al. The structural basis of lipopolysaccharide recognition by the TLR4–MD-2 complex. Nature. 2009;458:1191–1195. doi: 10.1038/nature07830. PubMed DOI
Areal H, Abrantes J, Esteves PJ. Signatures of positive selection in Toll-like receptor (TLR) genes in mammals. BMC Evol. Biol. 2011;11:368. doi: 10.1186/1471-2148-11-368. PubMed DOI PMC
Grueber, C. E., Wallis, G. P. & Jamieson, I. G. Episodic Positive Selection in the Evolution of Avian Toll-Like Receptor Innate Immunity Genes. PLoS ONE9, (2014). PubMed PMC
Key FM, Teixeira JC, de Filippo C, Andrés AM. Advantageous diversity maintained by balancing selection in humans. Curr. Opin. Genet. Dev. 2014;29:45–51. doi: 10.1016/j.gde.2014.08.001. PubMed DOI
Eriksson J, et al. Identification of the Yellow Skin Gene Reveals a Hybrid Origin of the Domestic Chicken. PLOS Genet. 2008;4:e1000010. doi: 10.1371/journal.pgen.1000010. PubMed DOI PMC
Liu Y-P, et al. Multiple maternal origins of chickens: out of the Asian jungles. Mol. Phylogenet. Evol. 2006;38:12–19. doi: 10.1016/j.ympev.2005.09.014. PubMed DOI
Dannemann M, Andrés AM, Kelso J. Introgression of Neandertal- and Denisovan-like Haplotypes Contributes to Adaptive Variation in Human Toll-like Receptors. Am. J. Hum. Genet. 2016;98:22–33. doi: 10.1016/j.ajhg.2015.11.015. PubMed DOI PMC
Anderson KL, Brewer MT, Rasmussen MA, Carlson SA. Identification of heritage chicken breeds with diminished susceptibility to intestinal colonization by multiple antibiotic-resistant Salmonella spp. Livest. Sci. 2015;182:34–37. doi: 10.1016/j.livsci.2015.10.018. DOI
Pavel, I. & Tuláček, F. Vzorník plemen drůbeže (Catalogue of poultry breeds). (Český svaz chovatelů 2006).
Scrivener, D. Poultry Breeds and Management: An Introductory Guide. (Crowood Press, Limited, 2008).
Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinforma. Oxf. Engl. 2009;25:1451–2. doi: 10.1093/bioinformatics/btp187. PubMed DOI
R Core Team. A language and environment for statistical computing (R Foundation for Statistical Computing, Vienna). Available at: https://www.r-project.org/. (2015).
Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 1999;16:37–48. doi: 10.1093/oxfordjournals.molbev.a026036. PubMed DOI
Pond SLK, Posada D, Gravenor MB, Woelk CH, Frost SDW. Automated Phylogenetic Detection of Recombination Using a Genetic Algorithm. Mol. Biol. Evol. 2006;23:1891–1901. doi: 10.1093/molbev/msl051. PubMed DOI
Choi Y, Sims GE, Murphy S, Miller JR, Chan AP. Predicting the Functional Effect of Amino Acid Substitutions and Indels. PLOS ONE. 2012;7:e46688. doi: 10.1371/journal.pone.0046688. PubMed DOI PMC
Pond SLK, Frost SDW. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinforma. Oxf. Engl. 2005;21:2531–3. doi: 10.1093/bioinformatics/bti320. PubMed DOI
Murrell B, et al. FUBAR: A Fast, Unconstrained Bayesian AppRoximation for Inferring Selection. Mol. Biol. Evol. 2013;30:1196–1205. doi: 10.1093/molbev/mst030. PubMed DOI PMC
Yang J, Zhang Y. I-TASSER server: new development for protein structure and function predictions. Nucleic Acids Res. 2015;43:W174–181. doi: 10.1093/nar/gkv342. PubMed DOI PMC
Kanno A, et al. Essential role for Toll-like receptor 7 (TLR7)-unique cysteines in an intramolecular disulfide bond, proteolytic cleavage and RNA sensing. Int. Immunol. 2013;25:413–422. doi: 10.1093/intimm/dxt007. PubMed DOI
Hipp MM, et al. The Processed Amino-Terminal Fragment of Human TLR7 Acts as a Chaperone To Direct Human TLR7 into Endosomes. J. Immunol. 2015;194:5417–5425. doi: 10.4049/jimmunol.1402703. PubMed DOI PMC
McGuffin LJ, Buenavista MT, Roche DB. The ModFOLD4 server for the quality assessment of 3D protein models. Nucleic Acids Res. 2013;41:W368–W372. doi: 10.1093/nar/gkt294. PubMed DOI PMC
Pritchard JK, Stephens M, Donnelly P. Inference of Population Structure Using Multilocus Genotype Data. Genetics. 2000;155:945–959. PubMed PMC
Liu L, et al. Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science. 2008;320:379–381. doi: 10.1126/science.1155406. PubMed DOI PMC
Wei T, et al. Homology modeling of human Toll-like receptors TLR7, 8, and 9 ligand-binding domains. Protein Sci. 2009;18:1684–1691. doi: 10.1002/pro.186. PubMed DOI PMC
Yoon S, et al. Structural Basis of TLR5-Flagellin Recognition and Signaling. Science. 2012;335:859–864. doi: 10.1126/science.1215584. PubMed DOI PMC
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