Diversification of the expanded teleost-specific toll-like receptor family in Atlantic cod, Gadus morhua

BMC Evolutionary Biology

Jorge MO Fernandes¹  Joaquín Dopazo²  Viswanath Kiron¹  Arvind YM Sundaram¹ 

[1] Faculty of Biosciences and Aquaculture, University of Nordland, Bodø 8049, Norway;Bioinformatics Department, Centro de Investigación Príncipe Felipe, Valencia, 46012, Spain

关键词: Neofunctionalisation;    Thermal stress;    Positive selection;    Innate immunity;    TLR;    Toll-like receptors;    Atlantic cod;   

Others  :  1130522
DOI  :  10.1186/1471-2148-12-256

 received in 2012-10-01, accepted in 2012-12-26,  发布年份 2012

【 摘 要 】

Background

Toll-like receptors (Tlrs) are major molecular pattern recognition receptors of the innate immune system. Atlantic cod (Gadus morhua) is the first vertebrate known to have lost most of the mammalian Tlr orthologues, particularly all bacterial recognising and other cell surface Tlrs. On the other hand, its genome encodes a unique repertoire of teleost-specific Tlrs. The aim of this study was to investigate if these duplicate Tlrs have been retained through adaptive evolution to compensate for the lack of other cell surface Tlrs in the cod genome.

Results

In this study, one tlr21, 12 tlr22 and two tlr23 genes representing the teleost-specific Tlr family have been cloned and characterised in cod. Phylogenetic analysis grouped all tlr22 genes under a single clade, indicating that the multiple cod paralogues have arisen through lineage-specific duplications. All tlrs examined were transcribed in immune-related tissues as well as in stomach, gut and gonads of adult cod and were differentially expressed during early development. These tlrs were also differentially regulated following immune challenge by immersion with Vibrio anguillarum, indicating their role in the immune response. An increase in water temperature from 4 to 12°C was associated with a 5.5-fold down-regulation of tlr22d transcript levels in spleen. Maximum likelihood analysis with different evolution models revealed that tlr22 genes are under positive selection. A total of 24 codons were found to be positively selected, of which 19 are in the ligand binding region of ectodomain.

Conclusion

Positive selection pressure coupled with experimental evidence of differential expression strongly support the hypothesis that teleost-specific tlr paralogues in cod are undergoing neofunctionalisation and can recognise bacterial pathogen-associated molecular patterns to compensate for the lack of other cell surface Tlrs.

【 授权许可】

   
2012 Sundaram et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Akira S, Uematsu S, Takeuchi O: Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
• [2]Imler JL, Zheng L: Biology of toll receptors: lessons from insects and mammals. J Leukoc Biol 2004, 75:18-26.
• [3]Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, Hood LE, Aderem A: The evolution of vertebrate toll-like receptors. Proc Natl Acad Sci USA 2005, 102:9577-9582.
• [4]Rebl A, Goldammer T, Seyfert HM: Toll-like receptor signaling in bony fish. Vet Immunol Immunopathol 2010, 134:139-150.
• [5]Ishii A, Kawasaki M, Matsumoto M, Tochinai S, Seya T: Phylogenetic and expression analysis of amphibian Xenopus toll-like receptors. Immunogenetics 2007, 59:281-293.
• [6]Brownlie R, Allan B: Avian toll-like receptors. Cell Tissue Res 2011, 343:121-130.
• [7]Palti Y: Toll-like receptors in bony fish: from genomics to function. Dev Comp Immunol 2011, 35:1263-1272.
• [8]Brownlie R, Zhu J, Allan B, Mutwiri GK, Babiuk LA, Potter A, Griebel P: Chicken TLR21 acts as a functional homologue to mammalian TLR9 in the recognition of CpG oligodeoxynucleotides. Mol Immunol 2009, 46:3163-3170.
• [9]Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA: The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86:973-983.
• [10]Matsuo A, Oshiumi H, Tsujita T, Mitani H, Kasai H, Yoshimizu M, Matsumoto M, Seya T: Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from birnaviruses. J Immunol 2008, 181:3474-3485.
• [11]Sundaram AYM, Consuegra S, Kiron V, Fernandes JMO: Positive selection within teleost toll-like receptors tlr21 and tlr22 subfamilies and their response to temperature stress and microbial components in zebrafish. Mol Biol Rep 2012, 39:8965-8975.
• [12]Rebl A, Siegl E, Köllner B, Fischer U, Seyfert HM: Characterization of twin toll-like receptors from rainbow trout (Oncorhynchus mykiss): evolutionary relationship and induced expression by Aeromonas salmonicida salmonicida. Dev Comp Immunol 2007, 31:499-510.
• [13]Stafford JL, Ellestad KK, Magor KE, Belosevic M, Magor BG: A toll-like receptor (TLR) gene that is up-regulated in activated goldfish macrophages. Dev Comp Immunol 2003, 27:685-698.
• [14]Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrom M, Gregers TF, Rounge TB, Paulsen J, Solbakken MH, Sharma A, Wetten OF, Lanzen A, Winer R, Knight J, Vogel JH, Aken B, Andersen O, Lagesen K, Tooming-Klunderud A, Edvardsen RB, Tina KG, Espelund M, Nepal C, Previti C, Karlsen BO, Moum T, Skage M, Berg PR, Gjoen T, Kuhl H, et al.: The genome sequence of Atlantic cod reveals a unique immune system. Nature 2011, 477:207-210.
• [15]Hughes AL: Gene duplication and the origin of novel proteins. Proc Natl Acad Sci USA 2005, 102:8791-8792.
• [16]Lynch M, Conery JS: The evolutionary fate and consequences of duplicate genes. Science 2000, 290:1151-1155.
• [17]Ohno S: Evolution by gene duplication. Berlin: Springer-Verlag; 1970.
• [18]Force A, Lynch M, Pickett FB, Amores A, Yan Y, Postlethwait J: Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999, 151:1531-1545.
• [19]Hahn MW: Distinguishing among evolutionary models for the maintenance of gene duplicates. J Hered 2009, 100:605-617.
• [20]Mazet FM, Shimeld S: Gene duplication and divergence in the early evolution of vertebrates. Curr Opin Genet Dev 2002, 12:393-396.
• [21]Lokesh J, Fernandes JMO, Korsnes K, Bergh Ø, Brinchmann MF, Kiron V: Transcriptional regulation of cytokines in the intestine of Atlantic cod fed yeast derived mannan oligosaccharide or β-glucan and challenged with Vibrio anguillarum. Fish Shellfish Immunol 2012, 33:626-631.
• [22]Campos C, Valente LMP, Fernandes JMO: Molecular evolution of zebrafish dnmt3 genes and thermal plasticity of their expression during embryonic development. Gene 2012, 500:93-100.
• [23]Stanke M, Diekhans M, Baertsch R, Haussler D: Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 2008, 24:637-644.
• [24]Campos C, Valente LMP, Borges P, Bizuayehu T, Fernandes JMO: Dietary lipid levels have a remarkable impact on the expression of growth-related genes in Senegalese sole (Solea senegalensis Kaup). J Exp Biol 2010, 213:200-209.
• [25]Matsushima N, Tanaka T, Enkhbayar P, Mikami T, Taga M, Yamada K, Kuroki Y: Comparative sequence analysis of leucine-rich repeats (LRRs) within vertebrate toll-like receptors. BMC Genomics 2007, 8:124. BioMed Central Full Text
• [26]Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
• [27]Swofford DL: PAUP* version 4.0b10. Phylogenetic analysis using parsimony (*and other methods). Massachusetts: Sinauer Associates; 2003.
• [28]Fernandes JMO, Ruangsri J, Kiron V: Atlantic cod piscidin and its diversification through positive selection. PLoS One 2010, 5:e9501.
• [29]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321.
• [30]Nagasawa K, Giannetto A, Fernandes JMO: Photoperiod influences growth and mll (mixed-lineage leukaemia) expression in Atlantic cod. PLoS One 2012, 7:e36908.
• [31]Korber B: HIV signature and sequence variation analysis. In Computational analysis of HIV molecular sequences. Edited by Rodrigo A, Learn G. Netherlands: Kluwer Academic Publishers; 2000:55-72.
• [32]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
• [33]Nei M, Kumar S: Molecular evolution and phylogenetics. New York: Oxford University Press; 2000.
• [34]Tajima F: Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 1993, 135:599-607.
• [35]Sarropoulou E, Fernandes JMO, Mitter K, Magoulas A, Mulero V, Sepulcre MP, Figueras A, Novoa B, Kotoulas G: Evolution of a multifunctional gene: the warm temperature acclimation protein Wap65 in the European seabass Dicentrarchus labrax. Mol Phylogenet Evol 2010, 55:640-649.
• [36]Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL: Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010, 26:2455-2457.
• [37]Oshiumi H, Matsuo A, Matsumoto M, Seya T: Pan-vertebrate toll-like receptors during evolution. Curr Genomics 2008, 9:488-493.
• [38]Kaji T, Yoshida S, Kawai K, Fuchigami Y, Watanabe W, Kubodera H, Kishimoto T: ASK3, a novel member of the apoptosis signal-regulating kinase family, is essential for stress-induced cell death in HeLa cells. Biochem Biophys Res Commun 2010, 395:213-218.
• [39]Xiao X, Qin Q, Chen X: Molecular characterization of a toll-like receptor 22 homologue in large yellow croaker (Pseudosciaena crocea) and promoter activity analysis of its 5′-flanking sequence. Fish Shellfish Immunol 2011, 30:224-233.
• [40]Su J, Heng J, Huang T, Peng L, Yang C, Li Q: Identification, mRNA expression and genomic structure of TLR22 and its association with GCRV susceptibility/resistance in grass carp (Ctenopharyngodon idella). Dev Comp Immunol 2012, 36:450-462.
• [41]Bell JK, Botos I, Hall PR, Askins J, Shiloach J, Segal DM, Davies DR: The molecular structure of the toll-like receptor 3 ligand-binding domain. Proc Natl Acad Sci USA 2005, 102:10976-10980.
• [42]Baoprasertkul P, Xu P, Peatman E, Kucuktas H, Liu Z: Divergent toll-like receptors in catfish (Ictalurus punctatus): TLR5S, TLR20, TLR21. Fish Shellfish Immunol 2007, 23:1218-1230.
• [43]Li YW, Luo XC, Dan XM, Qiao W, Huang XZ, Li AX: Molecular cloning of orange-spotted grouper (Epinephelus coioides) TLR21 and expression analysis post Cryptocaryon irritans infection. Fish Shellfish Immunol 2012, 32:476-481.
• [44]Riccioli A, Starace D, Galli R, Fuso A, Scarpa S, Palombi F, De Cesaris P, Ziparo E, Filippini A: Sertoli cells initiate testicular innate immune responses through TLR activation. J Immunol 2006, 177:7122-7130.
• [45]Kambris Z, Hoffmann JA, Imler JL, Capovilla M: Tissue and stage-specific expression of the Tolls in Drosophila embryos. Gene Expr Patterns 2002, 2:311-317.
• [46]Kaul D, Habbel P, Derkow K, Krüger C, Franzoni E, Wulczyn FG, Bereswill S, Nitsch R, Schott E, Veh R, Naumann T, Lehnardt S: Expression of toll-like receptors in the developing brain. PLoS One 2012, 7:e37767.
• [47]Lv J, Huang R, Li H, Luo D, Liao L, Zhu Z, Wang Y: Cloning and characterization of the grass carp (Ctenopharyngodon idella) toll-like receptor 22 gene, a fish-specific gene. Fish Shellfish Immunol 2012, 32:1022-1031.
• [48]Meijer AH, Gabby Krens SF, Medina Rodriguez IA, He S, Bitter W, Ewa Snaar-Jagalska B, Spaink HP: Expression analysis of the toll-like receptor and TIR domain adaptor families of zebrafish. Mol Immunol 2004, 40:773-783.
• [49]Zhou J, An H, Xu H, Liu S, Cao X: Heat shock up-regulates expression of toll-like receptor-2 and toll-like receptor-4 in human monocytes via p38 kinase signal pathway. Immunology 2005, 114:522-530.
• [50]Asea A: Heat shock proteins and toll-like receptors. In Toll-like receptors (TLRs) and innate immunity. Edited by Bauer S, Hartmann G. Berlin/Heidelberg: Springer; 2008:111-127. [Bauer S, Hartmann G (Series Editor): Handbook of Experimental Pharmacology]
• [51]Ohashi K, Burkart V, Flohé S, Kolb H: Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J Immunol 2000, 164:558-561.
• [52]Jin MS, Lee JO: Structures of the toll-like receptor family and its ligand complexes. Immunity 2008, 29:182-191.
• [53]Bell JK, Mullen GED, Leifer CA, Mazzoni A, Davies DR, Segal DM: Leucine-rich repeats and pathogen recognition in toll-like receptors. Trends Immunol 2003, 24:528-533.
• [54]Gojobori J, Innan H: Potential of fish opsin gene duplications to evolve new adaptive functions. Trends Genet 2009, 25:198-202.
• [55]Rodríguez-Trelles F, Tarrío R, Ayala FJ: Convergent neofunctionalization by positive Darwinian selection after ancient recurrent duplications of the xanthine dehydrogenase gene. Proc Natl Acad Sci USA 2003, 100:13413-13417.