Skip to main content
SpringerLink
Log in

Toll-like receptor 3 and TICAM genes in catfish: species-specific expression profiles following infection with Edwardsiella ictaluri

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

Abstract

Toll-like receptors (TLRs) are a family of transmembrane proteins that recognize specific pathogen-associated molecular patterns and use conserved signaling pathways to activate proinflammatory cytokines and type-1 interferons to fight infection. TLR3 in mammals is best known for its recognition of dsRNA as ligand and its MyD88-independent signaling. TLR3, upon recognition of dsRNA, recruits and binds its adaptor protein TIR domain-containing adapter molecule (TICAM) 1. Here we report the genomic sequences and structures of TLR3 and a TICAM adaptor from channel catfish (Ictalurus punctatus). Whereas a partial TLR3 cDNA sequence has been reported from channel catfish, and complete TLR3 genes are known from other teleost fish species, a complete TICAM sequence has not been previously reported from a nonmammalian species. Analysis of catfish TLR3 and TICAM expression after infection with Edwardsiella ictaluri, the causative agent of enteric septicemia of catfish (ESC), suggested a conserved TLR3-TICAM receptor–adaptor relation in catfish. Comparison of TLR3 and TICAM expression profiles in channel catfish with those from the closely related blue catfish species (Ictalurus furcatus), which exhibits strong resistance to ESC, revealed a striking pattern of species-specific expression. A dramatic downregulation of TLR3 and TICAM gene expression was observed in blue catfish head kidney and spleen, which we speculate may be the result of maturation and migration of different cell types to and from the lymphoid tissues following infection.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511

    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 

  • Bao B, Peatman E, Li P, He C, Liu ZJ (2005) Catfish hepcidin gene is expressed in a wide range of tissues and exhibits tissue-specific upregulation after bacterial infection. Dev Comp Immunol 29:939–950

    Article  PubMed  CAS  Google Scholar 

  • Bao B, Peatman E, Xu P, Li P, Zeng H, He C, Liu Z (2006) The catfish liver-expressed antimicrobial peptide 2 (LEAP-2) gene is expressed in a wide range of tissues and developmentally regulated. Mol Immunol 43:367–377

    Article  PubMed  CAS  Google Scholar 

  • Baoprasertkul P, Peatman E, Chen L, He C, Kucuktas H, Li P, Simmons M, Liu Z (2004) Sequence analysis and expression of a CXC chemokine in resistant and susceptible catfish after infection of Edwardsiella ictaluri. Dev Comp Immunol 28:769–780

    Article  PubMed  CAS  Google Scholar 

  • Baoprasertkul P, He C, Peatman E, Zhang S, Li P, Liu Z (2005) Constitutive expression of three novel catfish CXC chemokines: homeostatic chemokines in teleost fish. Mol Immunol 42:1355–1366

    Article  PubMed  CAS  Google Scholar 

  • Baoprasertkul P, Peatman E, Abernathy J, Liu Z (2006) Structural characterization and expression analysis of Toll-like receptor 2 gene from catfish. Fish Shellfish Immunol (in press). DOI 10.1016/j.fsi.2006.04.005

  • Bell JK, Botos I, Hall PR, Askins J, Shiloach J, Segal DM, Davies DR (2005) The molecular structure of the Toll-like receptor 3 ligand-binding domain. Proc Natl Acad Sci USA 102:10976–10980

    Article  PubMed  CAS  Google Scholar 

  • Belvin MP, Anderson KV (1996) A conserved signaling pathway: the Drosophila toll–dorsal pathway. Annu Rev Cell Dev Biol 12:393–416

    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 

  • Bilodeau AL, Peterson BC, Bosworth BG (2006) Response of Toll-like receptors, lysozyme, and IGF-I in back-cross hybrid (F1 male (blue × channel) × female channel) catfish challenged with virulent Edwardsiella ictaluri. Fish Shellfish Immunol 20:29–39

    Article  PubMed  CAS  Google Scholar 

  • Camp KL, Wolters WR, Rice CD (2000) Survivability and immune responses after challenge with Edwardsiella ictaluri in susceptible and resistant families of channel catfish, Ictalurus punctatus. Fish Shellfish Immunol 10:475–487

    Article  PubMed  CAS  Google Scholar 

  • Cao D, Kocabas A, Ju Z, Karsi A, Li P, Patterson A, Liu Z (2001) Transcriptome of channel catfish (Ictalurus punctatus): initial analysis of genes and expression profiles of the head kidney. Anim Genet 32:169–188

    Article  PubMed  CAS  Google Scholar 

  • Chen L, He C, Baoprasertkul P, Xu P, Li P, Serapion J, Waldbieser G, Wolters W, Liu Z (2005) Analysis of a catfish gene resembling interleukin-8: cDNA cloning, gene structure, and expression after infection with Edwardsiella ictaluri. Dev Comp Immunol 29:135–142

    Article  PubMed  CAS  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 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Ferreon JC, Ferreon AC, Li K, Lemon SM (2005) Molecular determinants of TRIF proteolysis mediated by the hepatitis C virus NS3/4A protease. J Biol Chem 280:20483–20492

    Article  PubMed  CAS  Google Scholar 

  • Fitzgerald KA, Rowe DC, Barnes BJ, Caffrey DR, Visintin A, Latz E, Monks B, Pitha PM, Golenbock DT (2003) LPS–TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J Exp Med 198:1043–1055

    Article  PubMed  CAS  Google Scholar 

  • Hardy MP, McGGettrick AF, O’Neill LA (2004) Transcriptional regulation of the human TRIF (TIR domain-containing adaptor protein inducing interferon beta) gene. Biochem J 380:83–93

    Article  PubMed  CAS  Google Scholar 

  • He C, Chen L, Simmons M, Li P, Kim S, Liu ZJ (2003) Putative SNP discovery in interspecific hybrids of catfish by comparative EST analysis. Anim Genet 34:445–448

    Article  PubMed  CAS  Google Scholar 

  • Heinz S, Haehnel V, Karaghiosoff M, Schwarzfischer L, Muller M, Krause SW, Rehli M (2003) Species-specific regulation of Toll-like receptor 3 genes in men and mice. J Biol Chem 278:21502–21509

    Article  PubMed  CAS  Google Scholar 

  • Iliev DB, Roach JC, Mackenzie S, Planas JV, Goetz FW (2005) Endotoxin recognition: in fish or not in fish? FEBS Lett 579:6519–6528

    Article  PubMed  CAS  Google Scholar 

  • Ishii KJ, Coban C, Akiral S (2005) Manifold mechanisms of Toll-like receptor–ligand recognition. J Clin Immunol 25:511–521

    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 

  • Ju Z, Karsi A, Kocabas A, Patterson A, Li P, Cao D, Dunham R, Liu Z (2000) Transcriptome analysis of channel catfish (Ictalurus punctatus): genes and expression profile from the brain. Gene 261:373–382

    Article  PubMed  CAS  Google Scholar 

  • Kadowaki N, Ho S, Antonenko S, Malefyt RW, Kastelein RA, Bazan F, Liu YJ (2001) Subsets of human dendritic cell precursors express different Toll-like receptors and respond to different microbial antigens. J Exp Med 194:863–869

    Article  PubMed  CAS  Google Scholar 

  • Karsi A, Cao D, Li P, Patterson A, Kocabas A, Feng J, Ju Z, Mickett KD, Liu Z (2002) Transcriptome analysis of channel catfish (Ictalurus punctatus): initial analysis of gene expression and microsatellite-containing cDNAs in the skin. Gene 285:157–168

    Article  PubMed  CAS  Google Scholar 

  • Kocabas AM, Li P, Cao D, Karsi A, He C, Patterson A, Ju Z, Dunham RA, Liu Z (2002) Expression profile of the channel catfish spleen: analysis of genes involved in immune functions. Mar Biotechnol 4:526–536

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto M, Kikkawa S, Kohase M, Miyake K, Seya T (2002) Establishment of a monoclonal antibody against human Toll-like receptor 3 that blocks double-stranded RNA-mediated signaling. Biochem Biophys Res Commun 293:1364–1369

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov R, Janeway C Jr (2000) Innate immune recognition: mechanisms and pathways. Immunol Rev 173:89–97

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov R, Preston-Hurlburt P, Janeway CA Jr (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, Ewa Snaar-Jagalska B, Spaink HP (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 

  • Muzio M, Polentarutti N, Bosisio D, Manoj Kumar PP, Mantovani A (2000) Toll-like receptor family and signalling pathway. Biochem Soc Trans 28:563–566

    PubMed  CAS  Google Scholar 

  • O’Neill LA, Fitzgerald KA, Bowie AG (2003) The Toll-IL-1 receptor adaptor family grows to five members. Trends Immunol 24:286–290

    Article  PubMed  Google Scholar 

  • Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T (2003a) TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol 4:161–167

    Article  PubMed  CAS  Google Scholar 

  • Oshiumi H, Sasai M, Shida K, Fujita T, Matsumoto M, Seya T (2003b) TIR-containing adapter molecule (TICAM)-2, a bridging adapter recruiting to Toll-like receptor 4 TICAM-1 that induces interferon-beta. J Biol Chem 278:49751–49762

    Article  PubMed  CAS  Google Scholar 

  • Oshiumi H, Tsujita T, Shida K, Matsumoto M, Ikeo K, Seya T (2003c) 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 

  • Peatman E, Bao B, Baoprasertkul P, Liu Z (2005) In silico identification and expression analysis of 12 novel CC chemokines in catfish. Immunogenetics 57:409–419

    Article  PubMed  CAS  Google Scholar 

  • Peatman E, Bao B, Peng X, Baoprasertkul P, Brady Y, Liu Z (2006) Catfish CC chemokines: genomic clustering, duplications, and expression after bacterial infection with Edwardsiella ictaluri. Mol Genet Genomics 275:297–309

    Article  PubMed  CAS  Google Scholar 

  • Peterson BC, Bosworth BG, Bilodeau AL (2005) Differential gene expression of IGF-I, IGF-II, and Toll-like receptors 3 and 5 during embryogenesis in hybrid (channel × blue) and channel catfish. Comp Biochem Physiol A Mol Integr Physiol 141:42–47

    Article  PubMed  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36

    Article  PubMed  Google Scholar 

  • Phelan PE, Mellon MT, Kim CH (2005) Functional characterization of full-length TLR3, IRAK-4, and TRAF6 in zebrafish (Danio rerio). Mol Immunol 42:1057–1071

    Article  PubMed  CAS  Google Scholar 

  • Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, Hood LE, Aderem A (2005) The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci USA 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 

  • Ross MT, LaBrie S, McPherson J, Stanton VP Jr (1999) Screening large-insert libraries by hybridization. In: Boyl A (ed) Current protocols in human genetics. Wiley, New York, pp 5.6.1–5.6.52

    Google Scholar 

  • Ruckdeschel K, Pfaffinger G, Haase R, Sing A, Weighardt H, Hacker G, Holzmann B, Heesemann J (2004) Signaling of apoptosis through TLRs critically involves toll/IL-1 receptor domain-containing adapter inducing IFN-beta, but not MyD88, in bacteria-infected murine macrophages. J Immunol 173:3320–3328

    PubMed  CAS  Google Scholar 

  • Rzhetsky A, Nei M (1992) Statistical properties of the ordinary least-squares, generalized least-squares, and minimum-evolution methods of phylogenetic inference. J Mol Evol 35:367–375

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Frisch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Serapion J, Kucuktas H, Feng J, Liu Z (2004) Bioinformatic mining of type I microsatellites from expressed sequence tags of channel catfish (Ictalurus punctatus). Mar Biotechnol (NY) 6:364–377

    Article  CAS  Google Scholar 

  • Seya T, Oshiumi H, Sasai M, Akazawa T, Matsumoto M (2005) TICAM-1 and TICAM-2: Toll-like receptor adapters that participate in induction of type 1 interferons. Int J Biochem Cell Biol 37:524–529

    Article  PubMed  CAS  Google Scholar 

  • Shoemaker CA, Klesius PH, Plumb JA (1997) Killing of Edwardsiella ictaluri by macrophages from channel catfish immune and susceptible to enteric septicemia of catfish. Vet Immunol Immunopathol 58:181–190

    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 

  • Tosi MF (2005) Innate immune responses to infection. J Allergy Clin Immunol 116:241–249

    Article  PubMed  CAS  Google Scholar 

  • Visintin A, Mazzoni A, Spitzer JH, Wyllie DH, Dower SK, Segal DM (2001) Regulation of Toll-like receptors in human monocytes and dendritic cells. J Immunol 166:249–255

    PubMed  CAS  Google Scholar 

  • Wang Q, Bao B, Wang Y, Peatman E, Liu Z (2006a) Characterization of a NK-lysin antimicrobial peptide gene from channel catfish. Fish Shellfish Immunol 20:419–426

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Wang Q, Baoprasertkul P, Peatman E, Liu Z (2006b) Genomic organization, gene duplication, and expression analysis of interleukin-1beta in channel catfish (Ictalurus punctatus). Mol Immunol 43:1653–1664

    Article  PubMed  CAS  Google Scholar 

  • Wolters WR, Wise DJ, Klesius PH (1996) Survival and antibody response of channel catfish, blue catfish and hybrids of female channel catfish and male blue catfish following exposure to Edwardsiella ictaluri. J Aquat Anim Health 8:249–254

    Article  Google Scholar 

  • Xu P, Bao B, He Q, Peatman E, He C, Liu ZJ (2005) Characterization and expression analysis of bactericidal permeability-increasing protein (BPI) antimicrobial peptide gene from channel catfish Ictalurus punctatus. Dev Comp Immunol 29:865–878

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto M, Sato S, Mori K, Hoshino K, Takeuchi O, Takeda K, Akira S (2002) Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J Immunol 169:6668–6672

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This project was supported by a grant from USDA NRI Animal Genome Tools and Resources Program (award no. 2006-35616-16685) and in part by a Specific Cooperative Agreement with USDA ARS Aquatic Animal Health Laboratory under contract no. 58-6420-5-030. We are grateful for an equipment grant from the National Research Initiative Competitive (grant no. 2005-35206-15274) from the USDA Cooperative State Research, Education, and Extension Service. We thank Renee Beam, Esau Arana, and Randell Goodman for their excellence in the production and maintenance of fish used in this study, and their assistance during challenge experiments. The authors are grateful to Dr. Sandra Ewald for a number of valuable discussions with her in the Department of Pathobiology at Auburn University. The senior author of the paper was supported by a scholarship from the Royal Thai Government.

Author information

Authors and Affiliations

  1. The Fish Molecular Genetics and Biotechnology Laboratory, Department of Fisheries and Allied Aquacultures and Program of Cell and Molecular Biosciences, Aquatic Genomics Unit, Auburn University, Auburn, AL 36849, USA

    Puttharat Baoprasertkul, Eric Peatman, Benjaporn Somridhivej & Zhanjiang Liu

Authors
  1. Puttharat Baoprasertkul
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eric Peatman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Benjaporn Somridhivej
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhanjiang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhanjiang Liu.

Additional information

Puttharat Baoprasertkul and Eric Peatman contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(PDF 93 kb)

Table S2

(PDF 93 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baoprasertkul, P., Peatman, E., Somridhivej, B. et al. Toll-like receptor 3 and TICAM genes in catfish: species-specific expression profiles following infection with Edwardsiella ictaluri . Immunogenetics 58, 817–830 (2006). https://doi.org/10.1007/s00251-006-0144-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-006-0144-z

Keywords

Search

Navigation