Skip to main content

Advertisement

Log in

Comprehensive survey and genomic characterization of Toll-like receptors (TLRs) in channel catfish, Ictalurus punctatus: identification of novel fish TLRs

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

A comprehensive survey of channel catfish Toll-like receptors (TLRs) was undertaken following a genomic PCR approach based on degenerate primers. Twenty different TLRs were identified in channel catfish. Channel catfish TLR sequences were characterized by phylogenetic analysis based on their conserved Toll/interleukin-1 receptor domain and by in-depth analysis of leucine-rich repeat (LRR) motifs of the ligand binding extracellular domain (ECD). The catfish have representatives of all the TLR types defined in vertebrates with the exception of TLR6, TLR10, TLR11, TLR12, TLR13, TLR15, TLR23, and TLR24. Additionally, two new types were discovered: TLR25 and TLR26. TLR25 is also present in cyprinids, cichlids, plecoglossids, and adrianichthyids, suggesting its presence early in fish evolution. To date, TLR26 was found only in channel catfish. Like TLR18–23, TLR25 and TLR26 were not found in any other vertebrate classes and appear to be fish specific. Data mining using the catfish TLR sequences revealed that in addition to ictalurids and cyprinids, TLR4 is also present in salmonids. TLR19 and TLR20 were both found in ictalurids, cyprinids, and salmonids, demonstrating a wider range than previously known. The LRR structure within ECDs appeared generally well conserved. TLR7 demonstrated a very high identity to human TLR7 strongly suggesting that ligand specificity maybe conserved. Finally, expression profiling confirmed that most TLRs are widely expressed in a diversity of tissues and revealed marked differences of expression level.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Akira S (2006) TLR signaling. Curr Top Microbiol Immunol 311:1–16

    Article  PubMed  CAS  Google Scholar 

  • Alexopoulou L, Holt AC, Medzhitov R, Flavell RA (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732–738

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignmentsearch tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Baoprasertkul P, Peatman E, Somridhivej B, Liu Z (2006) Toll-like receptor 3 and TICAM genes in catfish: species-specific expression profiles following infection with Edwardsiella ictaluri. Immunogenetics 58:817–830

    Article  PubMed  CAS  Google Scholar 

  • Baoprasertkul P, Peatman E, Abernathy J, Liu Z (2007a) Structural characterisation and expression analysis of toll-like receptor 2 gene from catfish. Fish Shellfish Immunol 22:418–426

    Article  PubMed  CAS  Google Scholar 

  • Baoprasertkul P, Xu P, Peatman E, Kucuktas H, Liu Z (2007b) Divergent Toll-like receptors in catfish (Ictalurus punctatus): TLR5S, TLR20, TLR21. Fish Shellfish Immunol 23:1218–1230

    Article  PubMed  CAS  Google Scholar 

  • Bell JK, Mullen GED, Leifer CA, Mazzoni A, Davies DR et al (2003) Leucine-rich repeats and pathogen recognition in Toll-like receptors. Trends Immunol 24:528–533

    Article  PubMed  CAS  Google Scholar 

  • Bell JK, Botos I, Hall PR, Askins J, Shiloach J et al (2005) The molecular structure of the Toll-like receptor 3 ligand-binding domain. Proc Natl Acad Sci U S A 102:10976–10980

    Article  PubMed  CAS  Google Scholar 

  • Beutler BA (2009) TLRs and innate immunity. Blood 113:1399–1407

    Article  PubMed  CAS  Google Scholar 

  • Bilodeau AL, Waldbieser GC (2005) Activation of TLR3 and TLR5 in channel catfish exposed to virulent Edwardsiella ictaluri. Dev Comp Immunol 29:713–721

    Article  PubMed  CAS  Google Scholar 

  • Botos I, Liu L, Wang Y, Segal DM, Davies DR (2009) The toll-like receptor 3:dsRNA signaling complex. Biochim Biophys Acta 1789:667–674

    Article  PubMed  CAS  Google Scholar 

  • Caldwell RB, Kierzek AM, Arakawa H, Bezzubov Y, Zaim J et al (2005) Full-length cDNAs from chicken bursal lymphocytes to facilitate gene function analysis. Genome Biol 6:R6

    Article  PubMed  Google Scholar 

  • Choe J, Kelker MS, Wilson IA (2005) Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 309:581–585

    Article  PubMed  CAS  Google Scholar 

  • Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303:1529–1531

    Article  PubMed  CAS  Google Scholar 

  • Ding X, Lu D, Hou Q, Li S, Liu X et al (2012) Orange-spotted grouper (Epinephelus coioides) toll-like receptor 22: molecular characterization, expression pattern and pertinent signaling pathways. Fish Shellfish Immunol 33:494–503

    Article  PubMed  CAS  Google Scholar 

  • Ewald SE, Engel A, Lee J, Wang M, Bogyo M et al (2011) Nucleic acid recognition by Toll-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J Exp Med 208:643–651

    Article  PubMed  CAS  Google Scholar 

  • Fedorova L, Fedorov A (2005) Puzzles of the human Genome: why do we need our introns? Curr Genomics 6:589–595

    Article  CAS  Google Scholar 

  • Franch R, Cardazzo B, Antonello J, Castagnaro M, Patarnello T et al (2006) Full-length sequence and expression analysis of Toll-like receptor 9 in the gilthead seabream (Sparus aurata L.). Gene 378:42–51

    Article  PubMed  CAS  Google Scholar 

  • Fujita M, Into T, Yasuda M, Okusawa T, Hamahira S et al (2003) Involvement of leucine residues at positions 107, 112, and 115 in a leucine-rich repeat motif of human Toll-like receptor 2 in the recognition of diacylated lipoproteins and lipopeptides and Staphylococcus aureus peptidoglycans. J Immunol 171:3675–3683

    PubMed  CAS  Google Scholar 

  • Gangloff M, Ludidi PL, Gay NJ (2005) Structures and motifs involved in Toll signaling. In: Rich T (ed) Toll and toll-like receptors: an immunologic perspective. Landes Biosciences/Kluwer Academic/Plenum, Georgetown, pp 56–75

    Chapter  Google Scholar 

  • Gautam JK, Ashish CLD, Krueger JK, Smith MF (2006) Structural and functional evidence for the role of the TLR2 DD loop in TLR1/TLR2 heterodimerization and signaling. J Biol Chem 281:30132–30142

    Article  PubMed  CAS  Google Scholar 

  • Gong J, Wei T, Zhang N, Jamitzky F, Heckl WM et al (2010) TollML: a database of toll-like receptor structural motifs. J Mol Model 16:1283–1289

    Article  PubMed  CAS  Google Scholar 

  • Hansen JD, Vojtech LN, Laing KJ (2011) Sensing disease and danger: a survey of vertebrate PRRs and their origins. Dev Comp Immunol 35:886–897

    Article  PubMed  CAS  Google Scholar 

  • Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC et al (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099–1103

    Article  PubMed  CAS  Google Scholar 

  • Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C et al (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303:1526–1529

    Article  PubMed  CAS  Google Scholar 

  • Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S et al (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408:740–745

    Article  PubMed  CAS  Google Scholar 

  • Heng J, Su J, Huang T, Dong J, Chen L (2011) The polymorphism and haplotype of TLR3 gene in grass carp (Ctenopharyngodon idella) and their associations with susceptibility/resistance to grass carp reovirus. Fish Shellfish Immunol 30:45–50

    Article  PubMed  CAS  Google Scholar 

  • Hirono I, Takami M, Miyata M, Miyazaki T, Han H-J et al (2004) Characterization of gene structure and expression of two toll-like receptors from Japanese flounder, Paralichthys olivaceus. Immunogenetics 56:38–46

    Article  PubMed  CAS  Google Scholar 

  • Huang X-N, Wang Z-Y, Yao C-L (2011) Characterization of Toll-like receptor 3 gene in large yellow croaker, Pseudosciaena crocea. Fish Shellfish Immunol 31:98–106

    Article  PubMed  CAS  Google Scholar 

  • Huang R, Dong F, Jang S, Liao L, Zhu Z et al (2012) Isolation and analysis of a novel grass carp toll-like receptor 4 (tlr4) gene cluster involved in the response to grass carp reovirus. Dev Comp Immunol 38:383–388

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Piontkivska H (2008) Functional diversification of the toll-like receptor gene family. Immunogenetics 60:249–256

    Article  PubMed  CAS  Google Scholar 

  • Hwang SD, Asahi T, Kondo H, Hirono I, Aoki T (2010) Molecular cloning and expression study on Toll-like receptor 5 paralogs in Japanese flounder, Paralichthys olivaceus. Fish Shellfish Immunol 29:630–638

    Article  PubMed  CAS  Google Scholar 

  • Hwang SD, Kondo H, Hirono I, Aoki T (2011) Molecular cloning and characterization of Toll-like receptor 14 in Japanese flounder, Paralichthys olivaceus. Fish Shellfish Immunol 30:425–429

    Article  PubMed  CAS  Google Scholar 

  • Hynes NA, Furnes C, Fredriksen BN, Winther T, Bøgwald J et al (2011) Immune response of Atlantic salmon to recombinant flagellin. Vaccine 29:7678–7687

    Article  PubMed  CAS  Google Scholar 

  • Ishii M, Hashimoto M, Oguma K, Kano R, Moritomo T et al (2006) Molecular cloning and tissue expression of canine Toll-like receptor 2 (TLR2). Vet Immunol Immunopathol 110:87–95

    Article  PubMed  CAS  Google Scholar 

  • Iwami KI, Matsuguchi T, Masuda A, Kikuchi T, Musikacharoen T et al (2000) Cutting edge: naturally occurring soluble form of mouse Toll-like receptor 4 inhibits lipopolysaccharide signaling. J Immunol 165:6682–6686

    PubMed  CAS  Google Scholar 

  • Iwasaki A, Medzhitov R (2010) Regulation of adaptive immunity by the innate immune system. Science 327:291–295

    Article  PubMed  CAS  Google Scholar 

  • Janeway CA (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54(Pt 1):1–13

    Article  PubMed  CAS  Google Scholar 

  • Jault C, Pichon L, Chluba J (2004) Toll-like receptor gene family and TIR-domain adapters in Danio rerio. Mol Immunol 40:759–771

    Article  PubMed  CAS  Google Scholar 

  • Jurk M, Heil F, Vollmer J, Schetter C, Krieg AM et al (2002) Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat Immunol 3:499

    Article  PubMed  CAS  Google Scholar 

  • Kajava AV (1998) Structural diversity of leucine-rich repeat proteins. J Mol Biol 277:519–527

    Article  PubMed  CAS  Google Scholar 

  • Kajava AV, Vassart G, Wodak SJ (1995) Modeling of the three-dimensional structure of proteins with the typical leucine-rich repeats. Structure 3:867–877

    Article  PubMed  CAS  Google Scholar 

  • Kasamatsu J, Oshiumi H, Matsumoto M, Kasahara M, Seya T (2010) Phylogenetic and expression analysis of lamprey toll-like receptors. Dev Comp Immunol 34:855–865

    Article  PubMed  CAS  Google Scholar 

  • Kobe B, Deisenhofer J (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19:415–421

    Article  PubMed  CAS  Google Scholar 

  • Kobe B, Kajava AV (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11:725–732

    Article  PubMed  CAS  Google Scholar 

  • Kongchum P, Rexroad CE, Hallerman EM, David L, Palti Y (2009) Single nucleotide polymorphism identification, genetic mapping and tissue expression of the rainbow trout TLR9 gene. Anim Genet 40:1001

    Article  PubMed  CAS  Google Scholar 

  • LeBouder E, Rey-Nores JE, Rushmere NK, Grigorov M, Lawn SD et al (2003) Soluble forms of Toll-like receptor (TLR)2 capable of modulating TLR2 signaling are present in human plasma and breast milk. J Immunol 171:6680–6689

    PubMed  CAS  Google Scholar 

  • Li Y, Berke IC, Modis Y (2012a) DNA binding to proteolytically activated TLR9 is sequence-independent and enhanced by DNA curvature. EMBO J 31:919–931

    Article  PubMed  CAS  Google Scholar 

  • Li Y-W, Luo X-C, Dan X-M, Qiao W, Huang X-Z et al (2012b) Molecular cloning of orange-spotted grouper (Epinephelus coioides) TLR21 and expression analysis post Cryptocaryon irritans infection. Fish Shellfish Immunol 32:476–481

    Article  PubMed  CAS  Google Scholar 

  • Liew FY, Xu D, Brint EK, O’Neill LAJ (2005) Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol 5:446–458

    Article  PubMed  CAS  Google Scholar 

  • Matsuo A, Oshiumi H, Tsujita T, Mitani H, Kasai H et al (2008) Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from birnaviruses. J Immunol 181:3474–3485

    PubMed  CAS  Google Scholar 

  • Matsushima N, Tanaka T, Enkhbayar P, Mikami T, Taga M et al (2007) Comparative sequence analysis of leucine-rich repeats (LRRs) within vertebrate toll-like receptors. BMC Genomics 8:124

    Article  PubMed  CAS  Google Scholar 

  • Matsushima N, Miyashita H, Mikami T, Kuroki Y (2010) A nested leucine rich repeat (LRR) domain: the precursor of LRRs is a ten or eleven residue motif. BMC Microbiol 10:235

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449:819–826

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov R, Preston-Hurlburt P, Janeway CA (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394–397

    Article  PubMed  CAS  Google Scholar 

  • Meijer AH, Gabby Krens SF, Medina Rodriguez IA, He S, Bitter W et al (2004) Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish. Mol Immunol 40:773–783

    Article  PubMed  CAS  Google Scholar 

  • Mikami T, Miyashita H, Takatsuka S, Kuroki Y, Matsushima N (2012) Molecular evolution of vertebrate Toll-like receptors: evolutionary rate difference between their leucine-rich repeats and their TIR domains. Gene 503:235–243

    Article  PubMed  CAS  Google Scholar 

  • Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215

    Article  PubMed  CAS  Google Scholar 

  • Mitsuzawa H, Wada I, Sano H, Iwaki D, Murakami S et al (2001) Extracellular Toll-like receptor 2 region containing Ser40-Ile64 but not Cys30-Ser39 is critical for the recognition of Staphylococcus aureus peptidoglycan. J Biol Chem 276:41350–41356

    Article  PubMed  CAS  Google Scholar 

  • Miyake K (2006) Roles for accessory molecules in microbial recognition by Toll-like receptors. J Endotoxin Res 12:195–204

    Article  PubMed  CAS  Google Scholar 

  • O’Neill LAJ, Bowie AG (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7:353–364

    Article  PubMed  CAS  Google Scholar 

  • Offord V, Coffey TJ, Werling D (2010) LRRfinder: a web application for the identification of leucine-rich repeats and an integrative Toll-like receptor database. Dev Comp Immunol 34:1035–1041

    Article  PubMed  CAS  Google Scholar 

  • Oshiumi H, Tsujita T, Shida K, Matsumoto M, Ikeo K et al (2003) Prediction of the prototype of the human Toll-like receptor gene family from the pufferfish, Fugu rubripes, genome. Immunogenetics 54:791–800

    PubMed  CAS  Google Scholar 

  • Palti Y (2011) Toll-like receptors in bony fish: from genomics to function. Dev Comp Immunol 35:1263–1272

    Article  PubMed  CAS  Google Scholar 

  • Palti Y, Rodriguez MF, Vallejo RL, Rexroad CE (2006) Mapping of Toll-like receptor genes in rainbow trout. Anim Genet 37:597–598

    Article  PubMed  CAS  Google Scholar 

  • Palti Y, Gahr SA, Purcell MK, Hadidi S, Rexroad CE et al (2010a) Identification, characterization and genetic mapping of TLR7, TLR8a1 and TLR8a2 genes in rainbow trout (Oncorhynchus mykiss). Dev Comp Immunol 34:219–233

    Article  PubMed  CAS  Google Scholar 

  • Palti Y, Rodriguez MF, Gahr SA, Purcell MK, Rexroad CE et al (2010b) Identification, characterization and genetic mapping of TLR1 loci in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 28:918–926

    Article  PubMed  CAS  Google Scholar 

  • Park BS, Song DH, Kim HM, Choi B-S, Lee H et al (2009) The structural basis of lipopolysaccharide recognition by the TLR4–MD-2 complex. Nature 458:1191–1195

    Article  PubMed  CAS  Google Scholar 

  • Peter ME, Kubarenko AV, Weber ANR, Dalpke AH (2009) Identification of an N-terminal recognition site in TLR9 that contributes to CpG-DNA-mediated receptor activation. J Immunol 182:7690–7697

    Article  PubMed  CAS  Google Scholar 

  • Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C et al (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085–2088

    Article  PubMed  CAS  Google Scholar 

  • Pridgeon JW, Russo R, Shoemaker CA, Klesius PH (2010) Expression profiles of toll-like receptors in anterior kidney of channel catfish, Ictalurus punctatus (Rafinesque), acutely infected by Edwardsiella ictaluri. J Fish Dis 33:497–505

    Article  PubMed  CAS  Google Scholar 

  • Purcell MK, Smith KD, Hood L, Winton JR, Roach JC (2006) Conservation of Toll-like receptor signaling pathways in teleost fish. Comp Biochem Physiol D Genomics Proteomics 1:77–88

    Article  CAS  Google Scholar 

  • Quiniou SMA, Waldbieser GC (2011) Mapping of the Toll-like receptor family in channel catfish, Ictalurus punctatus. Anim Genet 42:567–568

    Article  PubMed  CAS  Google Scholar 

  • Quiniou SMA, Katagiri T, Miller NW, Wilson M, Wolters WR et al (2003) Construction and characterization of a BAC library from a gynogenetic channel catfish Ictalurus punctatus. Genetics, Selection, Evolution: GSE 35:673–683

    Article  PubMed  CAS  Google Scholar 

  • Rebl A, Siegl E, Köllner B, Fischer U, Seyfert H-M (2007) Characterization of twin toll-like receptors from rainbow trout (Oncorhynchus mykiss): evolutionary relationship and induced expression by Aeromonas salmonicida salmonicida. Dev Comp Immunol 31:499–510

    Article  PubMed  CAS  Google Scholar 

  • Rebl A, Goldammer T, Seyfert H-M (2010) Toll-like receptor signaling in bony fish. Vet Immunol Immunopathol 134:139–150

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro CMS, Hermsen T, Taverne-Thiele AJ, Savelkoul HFJ, Wiegertjes GF (2010) Evolution of recognition of ligands from Gram-positive bacteria: similarities and differences in the TLR2-mediated response between mammalian vertebrates and teleost fish. J Immunol 184:2355–2368

    Article  PubMed  CAS  Google Scholar 

  • Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK et al (2005) The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci U S A 102:9577–9582

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez MF, Wiens GD, Purcell MK, Palti Y (2005) Characterization of Toll-like receptor 3 gene in rainbow trout (Oncorhynchus mykiss). Immunogenetics 57:510–519

    Article  PubMed  CAS  Google Scholar 

  • Rutz M, Metzger J, Gellert T, Luppa P, Lipford GB et al (2004) Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur J Immunol 34:2541–2550

    Article  PubMed  CAS  Google Scholar 

  • Sakharkar MK, Chow VTK, Kangueane P (2004) Distributions of exons and introns in the human genome. In silico Biol 4:387–393

    PubMed  CAS  Google Scholar 

  • Samanta M, Swain B, Basu M, Panda P, Mohapatra GB et al (2012) Molecular characterization of toll-like receptor 2 (TLR2), analysis of its inductive expression and associated down-stream signaling molecules following ligands exposure and bacterial infection in the Indian major carp, rohu (Labeo rohita). Fish Shellfish Immunol 32:411–425

    Article  PubMed  CAS  Google Scholar 

  • Shi Z, Cai Z, Sanchez A, Zhang T, Wen S et al (2011) A novel Toll-like receptor that recognizes vesicular stomatitis virus. J Biol Chem 286:4517–4524

    Article  PubMed  CAS  Google Scholar 

  • Skjaeveland I, Iliev DB, Zou J, Jørgensen T, Jørgensen JB (2008) A TLR9 homolog that is up-regulated by IFN-gamma in Atlantic salmon (Salmo salar). Dev Comp Immunol 32:603–607

    Article  PubMed  CAS  Google Scholar 

  • Skjaeveland I, Iliev DB, Strandskog G, Jørgensen JB (2009) Identification and characterization of TLR8 and MyD88 homologs in Atlantic salmon (Salmo salar). Dev Comp Immunol 33:1011–1017

    Article  PubMed  CAS  Google Scholar 

  • Slack JL, Schooley K, Bonnert TP, Mitcham JL, Qwarnstrom EE et al (2000) Identification of two major sites in the type I interleukin-1 receptor cytoplasmic region responsible for coupling to pro-inflammatory signaling pathways. J Biol Chem 275:4670–4678

    Article  PubMed  CAS  Google Scholar 

  • Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrøm M et al (2011) The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207–210

    Article  PubMed  CAS  Google Scholar 

  • Su J, Jang S, Yang C, Wang Y, Zhu Z (2009a) Genomic organization and expression analysis of Toll-like receptor 3 in grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 27:433–439

    Article  PubMed  CAS  Google Scholar 

  • Su J, Yang C, Xiong F, Wang Y, Zhu Z (2009b) Toll-like receptor 4 signaling pathway can be triggered by grass carp reovirus and Aeromonas hydrophila infection in rare minnow Gobiocypris rarus. Fish Shellfish Immunol 27:33–39

    Article  PubMed  CAS  Google Scholar 

  • Su J, Heng J, Huang T, Peng L, Yang C et al (2012) Identification, mRNA expression and genomic structure of TLR22 and its association with GCRV susceptibility/resistance in grass carp (Ctenopharyngodon idella). Dev Comp Immunol 36:450–462

    Article  PubMed  CAS  Google Scholar 

  • Subramaniam S, Stansberg C, Cunningham C (2004) The interleukin 1 receptor family. Dev Comp Immunol 28:415–428

    Article  PubMed  CAS  Google Scholar 

  • Sullivan C, Charette J, Catchen J, Lage CR, Giasson G et al (2009) The gene history of zebrafish tlr4a and tlr4b is predictive of their divergent functions. J Immunol 183:5896–5908

    Article  PubMed  CAS  Google Scholar 

  • Sundaram AY, Kiron V, Dopazo J, Fernandes JM (2012) Diversification of the expanded teleost-specific toll-like receptor family in Atlantic cod, Gadus morhua. BMC Evol Biol 12:256

    Article  PubMed  CAS  Google Scholar 

  • Swain P, Nayak SK, Nanda PK, Dash S (2008) Biological effects of bacterial lipopolysaccharide (endotoxin) in fish: a review. Fish Shellfish Immunol 24(4):394–9

    Google Scholar 

  • Svingerud T, Solstad T, Sun B, Nyrud MLJ, Kileng O et al (2012) Atlantic salmon type I IFN subtypes show differences in antiviral activity and cell-dependent expression: evidence for high IFNb/IFNc-producing cells in fish lymphoid tissues. J Immunol 189:5912–5923

    Article  PubMed  CAS  Google Scholar 

  • Tabeta K, Georgel P, Janssen E, Du X, Hoebe K et al (2004) Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc Natl Acad Sci U S A 101:3516–3521

    Article  PubMed  CAS  Google Scholar 

  • Takano T, Kondo H, Hirono I, Endo M, Saito-Taki T et al (2007) Molecular cloning and characterization of Toll-like receptor 9 in Japanese flounder, Paralichthys olivaceus. Mol Immunol 44:1845–1853

    Article  PubMed  CAS  Google Scholar 

  • Takano T, Don HS, Kondo H, Hirono I, Aoki T et al (2010) Evidence of molecular Toll-like receptor mechanisms in teleosts. Fish Pathol 45:1–16

    Article  Google Scholar 

  • Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17:1–14

    Article  PubMed  CAS  Google Scholar 

  • Takeda K, Kaisho T, Akira S (2003) Toll-like receptors. Annu Rev Immunol 21:335–376

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140:805–820

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Tine M, Kuhl H, Beck A, Bargelloni L, Reinhardt R (2011) Comparative analysis of intronless genes in teleost fish genomes: insights into their evolution and molecular function. Mar Genomics 4:109–119

    Article  PubMed  Google Scholar 

  • Tsoi S, Park KC, Kay HH, O’Brien TJ, Podor E et al (2006) Identification of a transcript encoding a soluble form of toll-like receptor 5 (TLR5) in Atlantic salmon during Aeromonas salmonicida infection. Vet Immunol Immunopathol 109:183–187

    Article  PubMed  CAS  Google Scholar 

  • Tsujita T, Tsukada H, Nakao M, Oshiumi H, Matsumoto M et al (2004) Sensing bacterial flagellin by membrane and soluble orthologs of Toll-like receptor 5 in rainbow trout (Onchorhynchus mykiss). J Biol Chem 279:48588–48597

    Article  PubMed  CAS  Google Scholar 

  • Tsujita T, Ishii A, Tsukada H, Matsumoto M, Che F-S et al (2006) Fish soluble Toll-like receptor (TLR)5 amplifies human TLR5 response via physical binding to flagellin. Vaccine 24:2193–2199

    Article  PubMed  CAS  Google Scholar 

  • Wei T, Gong J, Jamitzky F, Heckl WM, Stark RW et al (2008) LRRML: a conformational database and an XML description of leucine-rich repeats (LRRs). BMC Struct Biol 8:47

    Article  PubMed  CAS  Google Scholar 

  • Wei YC, Pan TS, Chang MX, Huang B, Xu Z et al (2011) Cloning and expression of Toll-like receptors 1 and 2 from a teleost fish, the orange-spotted grouper Epinephelus coioides. Vet Immunol Immunopathol 141:173–182

    Article  PubMed  CAS  Google Scholar 

  • Wu X-Y, Xiang L-X, Huang L, Jin Y, Shao J-Z (2008) Characterization, expression and evolution analysis of Toll-like receptor 1 gene in pufferfish (Tetraodon nigroviridis). Int J Immunogenet 35:215–225

    Article  PubMed  CAS  Google Scholar 

  • Xiao X, Qin Q, Chen X (2011) 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 30:224–233

    Article  PubMed  CAS  Google Scholar 

  • Xu Y, Tao X, Shen B, Horng T, Medzhitov R et al (2000) Structural basis for signal transduction by the Toll/interleukin-1 receptor domains. Nature 408:111–115

    Article  PubMed  CAS  Google Scholar 

  • Yang C, Su J (2010) Molecular identification and expression analysis of Toll-like receptor 3 in common carp Cyprinus carpio. J Fish Biol 76:1926–1939

    Article  PubMed  CAS  Google Scholar 

  • Yang C, Su J, Zhang R, Peng L, Li Q (2012) Identification and expression profiles of grass carp Ctenopharyngodon idella tlr7 in responses to double-stranded RNA and virus infection. J Fish Biol 80:2605–2622

    Article  PubMed  CAS  Google Scholar 

  • Yao C-L, Kong P, Wang Z-Y, Ji P-F, Cai M-Y et al (2008) Cloning and expression analysis of two alternative splicing toll-like receptor 9 isoforms A and B in large yellow croaker, Pseudosciaena crocea. Fish Shellfish Immunol 25:648–656

    Article  PubMed  CAS  Google Scholar 

  • Yilmaz A, Shen S, Adelson DL, Xavier S, Zhu JJ (2005) Identification and sequence analysis of chicken Toll-like receptors. Immunogenetics 56:743–753

    Article  PubMed  CAS  Google Scholar 

  • Yoon S, Kurnasov O, Natarajan V, Hong M, Gudkov AV et al (2012) Structural basis of TLR5-flagellin recognition and signaling. Science 335:859–864

    Article  PubMed  CAS  Google Scholar 

  • Yu Y, Zhong Q, Li C, Jiang L, Yan F et al (2009) Isolation and characterization of Toll-like receptor 9 in half-smooth tongue sole Cynoglossus semilaevis. Fish Shellfish Immunol 26:492–499

    Article  PubMed  CAS  Google Scholar 

  • Zhang D, Zhang G, Hayden MS, Greenblatt MB, Bussey C et al (2004) A toll-like receptor that prevents infection by uropathogenic bacteria. Science 303:1522–1526

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Liu S, Rajendran KV, Sun L, Zhang Y, Sun F, Kucuktas H, Liu H, Liu Z (2013) Pathogen recognition receptors in channel catfish: III. Phylogeny and expression analysis of Toll-like receptors. Dev Comp Immunol. doi:10.1016/j.dci.2013.01.009

Download references

Acknowledgments

The authors thank Thishya Perera for technical support.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sylvie M. A. Quiniou.

Additional information

Note added in proof: During processing of this paper, another article about catfish TLRs was published by Zhang et al. (2013).

Electronic supplementary material

ESM 1

(DOC 94 kb)

ESM 2

(DOCX 125 kb)

ESM 3

(DOCX 173 kb)

ESM 4

(DOCX 147 kb)

ESM 5

(DOCX 78 kb)

ESM 6

(DOCX 122 kb)

ESM 7

(DOCX 103 kb)

ESM 8

(DOCX 125 kb)

ESM 9

(DOCX 168 kb)

ESM 10

(DOCX 113 kb)

ESM 11

(DOCX 80 kb)

ESM 12

(DOCX 82 kb)

ESM 13

(DOCX 96 kb)

ESM 14

(DOCX 143 kb)

ESM 15

(DOCX 84 kb)

ESM 16

(XLSX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Quiniou, S.M.A., Boudinot, P. & Bengtén, E. Comprehensive survey and genomic characterization of Toll-like receptors (TLRs) in channel catfish, Ictalurus punctatus: identification of novel fish TLRs. Immunogenetics 65, 511–530 (2013). https://doi.org/10.1007/s00251-013-0694-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-013-0694-9

Keywords

Navigation