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Sequence and expression of C-type lectin receptors in Atlantic salmon (Salmo salar)

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Abstract

The diverse receptors of the C-type lectin superfamily play key roles in innate immunity. In mammals, cell surface receptors with C-type lectin domains are involved in pathogen recognition and in immune response, and in some cases are exploited by pathogens to gain entry into cells. This study reports on sequence and expression analysis of three paralogous group II C-type lectins from the teleost fish Atlantic salmon (Salmo salar). Each of the receptors showed similarity to immune-relevant mammalian receptors in terms of amino acid sequence and overall organization within the C-type lectin-like domain (CTLD). Two of the three have cytoplasmic motifs consistent with the immunoreceptor tyrosine-based activation motifs (ITAM), which are known to modulate downstream functions in leukocytes. All three C-type lectin receptors were expressed in multiple tissues of healthy fish, including peripheral blood leukocytes and salmon head kidney cells (SHK-1). Each receptor was up-regulated in salmon liver in response to infection by Aeromonas salmonicida and one receptor was substantially up-regulated in cultured SHK-1 cells in response to lipopolysaccharide (LPS). Putative binding sites for the CAAT-enhancer-binding protein (C/EBP) family of transcription factors in the regulatory regions of these C-type lectin genes may mediate their response to bacteria and LPS in salmon leukocytes. The identification of these types of receptors in distinct populations of cells within the immune system will provide important markers for identifying and categorizing the state of differentiation or activation of these cells and lead to further understanding of the interaction between the salmon host and multiple pathogens.

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References

  • Apostolopoulos V, McKenzie IF (2001) Role of the mannose receptor in the immune response. Curr Mol Med 1:469–474

    CAS  PubMed  Google Scholar 

  • Ariizumi K, Shen GL, Shikano S, Ritter R III, Zubas P, Edelbaum D, Morita A, Takashima A (2000) Cloning of a second dendritic cell-associated C-type lectin (dectin-2) and its alternatively spliced isoforms. J Biol Chem 275:11957–11963

    Article  CAS  PubMed  Google Scholar 

  • Ariizumi K, Shen GL, Ritter R III, Kumanoto T, Edelbaum D, Morita A, Bergstresser PR, Takashima A (2001) Identification of a human homologue of the dendritic cell-associated C-type lectin-1, dectin-1. Gene 272:51–60

    Article  PubMed  Google Scholar 

  • Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392:245–2522

    Article  CAS  PubMed  Google Scholar 

  • Bashirova AA, Geijtenbeek TBH, van Duijnhoven GCF, van Vliet SJ, Eilering JBG, Martin MP, Wu L, Martin TD, Viebig N, Knolle PA, KewalRamani VN, van Kooyk Y, Carrington M (2001) A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection. J Exp Med 193:671–678

    Article  CAS  PubMed  Google Scholar 

  • Bashirova AA, Wu L, Cheng J, Martin TD, Martin MP, Benveniste RE, Lifson JD, KewalRamani VN, Hughes A, Carrington M (2003) Novel member of the CD209 (DC-SIGN) gene family in primates. J Virol 77:217–227

    Article  CAS  PubMed  Google Scholar 

  • Bayne CJ, Gerwick L, Fujiki K, Nakao M, Yano T (2001) Immune-relevant (including acute phase) genes identified in the livers of rainbow trout, Oncorhynchus mykiss, by means of suppression subtractive hybridization. Dev Comp Immunol 25:205–2177

    Article  CAS  PubMed  Google Scholar 

  • Billadeau DD, Leibson PJ (2002) ITAMs versus ITIMs: striking a balance during cell regulation. J Clin Invest 109:161–168

    Article  CAS  PubMed  Google Scholar 

  • Bradley MN, Zhou L, Smale ST (2003) C/EBPbeta regulation in lipopolysaccharide-stimulated macrophages. Mol Cell Biol 23:4841–4858

    Article  CAS  PubMed  Google Scholar 

  • Berger B, Wilson DB, Wolf E, Tonchev T, Milla M, Kim PS (1995) Predicting coiled-coils by use of pairwise residue correlations. Proc Natl Acad Sci USA 92:8259–8263

    CAS  PubMed  Google Scholar 

  • Cambi A, Figdor CG (2003) Dual function of C-type lectin-like receptors in the immune system. Curr Opin Cell Biol 15:539–546

    Article  CAS  PubMed  Google Scholar 

  • Colonna M, Samaridis J, Angman L (2000) Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendrictic cells. Eur J Immunol 30:697–704

    Article  CAS  PubMed  Google Scholar 

  • Dannevig BH, Brudeseth BE, Gjoen T, Rode M, Wergeland HI, Evensen, O, McL Press C (1997) Characterization of a long-term cell line (SHK-1) developed from the head kidney of Atlantic salmon (Salmo salar). Fish Shellfish Immunol 7:213–226

    Article  Google Scholar 

  • Douglas SE, Tsoi SCM, Penny S, Melville K, Reith ME, Ewart KV (2003) Expressed sequence tags—a snapshot of the fish genome. In: Shimizu N, Aoki T, Hirono I, Takashima F (eds) Aquatic Genomics, steps toward a great future. Springer-Verlag, New York Heidelberg Berlin, pp 115–127

    Google Scholar 

  • Drickamer K (1993) Evolution of Ca(2+)-dependent animal lectins. Prog Nucleic Acid Res Mol Biol 45:207–232

    CAS  PubMed  Google Scholar 

  • Drickamer K (1999) C-type lectin-like domains. Curr Opin Struct Biol 9:585–590

    Article  CAS  PubMed  Google Scholar 

  • Drickamer K, Fadden AJ (2002) Genomic analysis of C-type lectins. Biochem Soc Symp 69:59–72

    CAS  PubMed  Google Scholar 

  • Fadden AJ, Holt OJ, Drickamer K (2003) Molecular characterization of the rat Kupffer cell glycoprotein receptor. Glycobiology 13:529–5377

    Article  CAS  PubMed  Google Scholar 

  • Feinberg H, Mitchell DA, Drickamer K, Weis WI (2001) Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 294:2163–2166

    Article  CAS  PubMed  Google Scholar 

  • Gantner BN, Simmons RM, Canavera SJ, Akira S, Underhill DM (2003) Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J Exp Med 197:1107–1119

    Article  CAS  PubMed  Google Scholar 

  • Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y (2000) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100:491–494

    Article  PubMed  Google Scholar 

  • Giga Y, Ikai A, Takahashi K (1987) The complete amino acid sequence of echinoidin, a lectin from the coelomic fluid of the sea urchin Anthocidaris crassispina: homologies with mammalian and insect lectins. J Biol Chem 262:6197–6203

    CAS  PubMed  Google Scholar 

  • Holmskov U, Thiel S, Jensenius JC (2003) Collectins and ficolins: humoral lectins of the innate immune defence. Annu Rev Immunol 21:547–578

    Article  CAS  PubMed  Google Scholar 

  • Hoyle GW, Hill RL (1991) Structure of the gene for a carbohydrate-binding receptor unique to rat Kupffer cells. J Biol Chem 266:1850–1857

    CAS  PubMed  Google Scholar 

  • Iobst ST, Drickamer K (1994) Binding of sugar ligands to Ca2+-dependent animal lectins II. Generation of high-affinity galactose binding by site-directed mutagenesis. J Biol Chem 269:15512–15519

    CAS  PubMed  Google Scholar 

  • Kolatkar AR, Weis WI (1996) Structural basis of galactose recognition by C-type animal lectins. J Biol Chem 271:6679–6685

    Article  CAS  PubMed  Google Scholar 

  • Kwon DS, Gregorio G, Bitton N, Hendrickson WA, Littman DR (2002) DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity 16:135–1444

    Article  CAS  PubMed  Google Scholar 

  • Lanier LL, Corliss BC, Wu J, Leong C, Phillips JH (1998) Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391:703–707

    Article  CAS  PubMed  Google Scholar 

  • Lee SJ, Evers S, Roeder D, Parlow AF, Risteli J, Risteli L, Lee YC, Feizi T, Langen H, Nussenzweig MC (2002) Mannose receptor-mediated regulation of serum glycoprotein homeostasis. Science 295:1898–1901

    Article  CAS  PubMed  Google Scholar 

  • Ley K (2001) Pathways and bottlenecks in the web of inflammatory adhesion molecules and chemoattractants. Immunol Res 24:87–95

    Article  CAS  PubMed  Google Scholar 

  • Leyrer S, Bitzer M, Lauer U, Kramer J, Neubert W, Sedlmeier R (1998) Sendai virus-like particles devoid of haemagglutinin-neuraminidase protein infect cells via the human asialoglycoprotein receptor. J Gen Virol 79:683–687

    CAS  PubMed  Google Scholar 

  • Lopez-Rodriguez C, Botella L, Corbi AL (1997) CCAAT-enhancer-binding proteins (C/EBP) regulate the tissue specific activity of the CD11c integrin gene promoter through functional interactions with Sp1 proteins. J Biol Chem 272:29120–29126

    Article  CAS  PubMed  Google Scholar 

  • Mann K, Weiss IM, Andre S, Gaius H, Fritz M (2000) The amino-acid sequence of the abalone (Haliotis Laevigata) nacre protein perlucin. Eur J Biochem 267:5257–5264

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto M, Tanaka T, Kaisho T, Sanjo H, Copeland NG, Gilbert DJ, Jenkins NA, Akira S (1999) A novel LPS-inducible C-type lectin is a transcriptional target of NF-IL6 in macrophages. J Immunol 163:5039–5048

    CAS  PubMed  Google Scholar 

  • Matsuo MY, Asakawa S, Shimizu N, Kimura H, Nonaka M (2002) Nucleotide sequence of the MHC class I genomic region of a teleost, the medaka (Oryzias latipes). Immunogenetics 53:930–940

    Article  CAS  PubMed  Google Scholar 

  • Mistry AC, Honda S, Hirose S (2001) Structure, properties and enhanced expression of galactose-binding C-type lectins in mucous cells of gills from freshwater Japanese eels (Anguilla japonica). Biochem J 360:107–115

    Article  CAS  PubMed  Google Scholar 

  • Mummidi S, Catano G, Lam L, Hoefle A, Telles V, Begum K, Jimenez F, Ahuja SS, Ahuja SK (2001) Extensive repertoire of membrane-bound and soluble dendritic cell-specific ICAM-3-grabbing nonintegrin 1 (DC-SIGN1) and DC-SIGN2 isoforms. Inter-individual variation in expression of DC-SIGN transcripts. J Biol Chem 276:33196–33212

    Article  CAS  PubMed  Google Scholar 

  • Nakamura K, Funakoshi H, Miyamoto K, Tokunaga F, Nakamura T (2001) Molecular cloning and functional characterization of a human scavenger receptor with C-type lectin (SRCL), a novel member of a scavenger receptor family. Biochem Biophys Res Commun 280:1028–1035

    Article  CAS  PubMed  Google Scholar 

  • Ohmori H, Makita Y, Funamizu M, Chiba S, Ohtani K, Suzuki Y, Wakamiya N, Hata A (2003) Haplotype analysis of the human collectin placenta 1 (hCL-P1) gene. J Hum Genet 48:82–85

    Article  CAS  PubMed  Google Scholar 

  • Ohtani K, Suzuki Y, Eda S, Kawai T, Kase T, Keshi H, Sakai Y, Fukuoh A, Sakamoto T, Itabe H, Suzutani T, Ogasawara M, Yoshida I, Wakamiya N (2001) The membrane-type collectin CL-P1 is a scavenger receptor on vascular endothelial cells. J Biol Chem 276:44222–44228

    Article  CAS  PubMed  Google Scholar 

  • Plevy SE, Gemberling JH, Hsu S, Dorner AJ, Smale ST (1997) Multiple control elements mediate activation of the murine and human interleukin 12 p40 promoters: evidence of functional synergy between C/EBP and Rel proteins. Mol Cell Biol 17:4572–4588

    CAS  PubMed  Google Scholar 

  • Pohlmann S, Baribaud F, Lee B, Leslie GJ, Sanchez MD, Hiebenthal-Millow K, Munch J, Kirchhoff F, Doms RW (2001) DC-SIGN interactions with human immunodeficiency virus type 1 and 2 and simian immunodeficiency virus. J Virol 7:4664–4672

    Article  Google Scholar 

  • Poli V (1998) The role of C/EBP isoforms in the control of inflammatory and native immunity functions. J Biol Chem 273:29279–29282

    Article  CAS  PubMed  Google Scholar 

  • Quandt K, Frech K, Karas H, Wingender E, Werner T (1995) MatInd and MatInspector—New fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23:4878–4884

    CAS  PubMed  Google Scholar 

  • Quesenberry MS, Drickamer K (1992) Role of conserved and non-conserved residues in the Ca(2+)-dependent carbohydrate-recognition domain of a rat mannose-binding protein. Analysis by random cassette mutagenesis. J Biol Chem 267:10831–10841

    CAS  PubMed  Google Scholar 

  • Radaev S, Sun PD (2003) Structure and function of natural killer cell surface receptors. Annu Rev Biophys Biomol Struct 32:93–114

    Article  CAS  PubMed  Google Scholar 

  • Rauch U, Grimpe B, Kulbe G, Arnold-Ammer I, Beier D, Faessler R (1995) Structure and chromosomal localization of the mouse neurocan gene. Genomics 28:405–410

    Article  CAS  PubMed  Google Scholar 

  • Richards RC, Hudson DM, Thibault P, Ewart KV (2003) Cloning and characterization of the Atlantic salmon serum lectin, a long-form C-type lectin expressed in kidney. Biochim Biophys Acta 1621:110–115

    Article  CAS  PubMed  Google Scholar 

  • Sato A, Mayer WE, Overath P, Klein J (2003) Genes encoding putative natural killer cell C-type lectin receptors in teleostean fishes. Proc Natl Acad Sci USA 100:7779–7784

    Article  CAS  PubMed  Google Scholar 

  • Soilleux EJ, Barten R, Trowsdale J (2000) DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13. J Immunol 165:2937–2942

    CAS  PubMed  Google Scholar 

  • Spiess M (1990) The asialoglycoprotein receptor: a model for endocytic transport receptors. Biochem 29:10009–10018

    CAS  Google Scholar 

  • Takamatsu N, Takeda T, Kojima M, Heishi M., Muramoto K, Kamiya H, Shiba T (1993) Acorn barnacle Megabalanus rosa lectin (BRA-3): cDNA cloning, gene structure and seasonal changes of mRNA and protein levels. Gene 128:251–255

    Article  CAS  PubMed  Google Scholar 

  • Tang X, Davies JE, Davies SJ (2003) Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J Neurosci Res 71:427–444

    Article  CAS  PubMed  Google Scholar 

  • Tasumi S, Ohira T, Kawazoe I, Suetake H, Suzuki Y, Aida, K (2002) Primary structure and characteristics of a lectin from skin mucus of the Japanese eel, Anguilla japonica. J Biol Chem 277:27305–27311

    Article  CAS  PubMed  Google Scholar 

  • Tsoi SCM, Ewart KV, Penny S, Melville K, Liebscher RS, Brown LL, Douglas SE (2004) Identification of immune-relevant genes from Atlantic salmon using suppression subtractive hybridization. Mar Biotechnol (NY) (in press)

  • Tusnády GE, Simon I (1998) Principles governing amino acid composition of integral membrane proteins: applications to topology prediction. J Mol Biol 283:489–506

    Article  CAS  PubMed  Google Scholar 

  • Tusnády GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849–850

    Article  CAS  PubMed  Google Scholar 

  • Valladeau J, Ravel O, Dezutter-Dambuyant C, Moore K, Kleijmeer M, Liu Y, Duvert-Frances V, Vincent C, Schmitt D, Davoust J, Caux C, Lebecque S, Saeland S (2000) Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 12:71–81

    Article  CAS  PubMed  Google Scholar 

  • Vitved L, Holmskov U, Koch C, Teisner B, Hansen S, Skjodt K (2000) The homologue of mannose-binding lectin in the carp family Cyprinidae is expressed at high level in spleen, and the deduced primary structure predicts affinity for galactose. Immunogenetics 51:955–964

    Article  CAS  PubMed  Google Scholar 

  • Weis WI, Drickamer K, Hendrickson WA (1992) Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature 360:127–1344

    Article  CAS  PubMed  Google Scholar 

  • Weis WI, Taylor ME, Drickamer K (1998) The C-type superfamily in the immune system. Immuno Rev 163:19–34

    CAS  Google Scholar 

  • Wingender E, Chen X, Hehl R, Karas H, Liebich I, Matys V, Meinhardt T, Prüβ M, Reuter I, Schacherer F (2000) TRANSFAC: an integrated system for gene expression regulation. Nucleic Acids Res 28:316–319

    Article  CAS  PubMed  Google Scholar 

  • Yoder JA, Mueller MG, Nichols KM, Ristow SS, Thorgaard GH, Ota T, Litman GW (2002) Cloning novel immune-type inhibitory receptors from the rainbow trout, Oncorhynchus mykiss. Immunogenetics 54:662–6700

    Article  CAS  PubMed  Google Scholar 

  • Yokota K, Takashima A, Bergstresser PR, Ariisumi K (2001) Identification of a human homologue of the dendritic cell-associted C-type lectin-1, dectin-1. Gene 272:51–60

    Article  PubMed  Google Scholar 

  • Zhang H, Robison B, Thorgaard GH and Ristow SS (2000) Cloning and mapping genomic organisation of a fish C-type lectin gene from homozygous clones of rainbow trout (Oncorhynchus mykiss). Biochim Biophys Acta 1492:14–22

    Google Scholar 

  • Zhang H, Nichols K, Thorgaard GH and Ristow SS (2001) Identification, mapping and genomic structural analysis of an immunoreceptor tyrosine-based inhibition motif-bearing C-type lectin from homozygous clones of rainbow trout (Oncorhynchus mykiss). Immunogenetics 53:751–759

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Krista Melville, Sandra Sperker and Laura Brown [all NRC Institute for Marine Biosciences (IMB)] for salmon liver samples from previous infection studies and Mark Fast (Dalhousie University and Microtek) for the gift of RNA samples from control and LPS-treated SHK-1 cells. We are grateful to J.C. Achenbach (Dalhousie University) for technical assistance and helpful discussion. We also thank Neil Ross (NRC IBM) for review of the manuscript. This work was supported by the NRC IMB, and the NRC Genomics and Health Initiative (GHI). This is NRC publication number 42363.

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Soanes, K.H., Figuereido, K., Richards, R.C. et al. Sequence and expression of C-type lectin receptors in Atlantic salmon (Salmo salar). Immunogenetics 56, 572–584 (2004). https://doi.org/10.1007/s00251-004-0719-5

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