Amino Acid Sequence; Animals; Base Sequence; Cell Line; Cloning, Molecular; Fish Diseases/immunology/virology; Gene Expression Regulation; Interleukin-10/genetics; Molecular Sequence Data; Oncorhynchus mykiss/genetics/immunology; Primary Cell Culture; Protein Structure, Tertiary; Receptors, Cytokine/biosynthesis/genetics; Sequence Analysis, DNA; Cell lines; Class 2 cytokine receptor family (CRF2); Head kidney leucocytes; In vitro stimulation; Oncorhynchus mykiss; Viral infection; Antimicrobial peptides; Cohabitation; Cytokines; Intraperitoneal injection; Non-lethal sampling; Yersinia ruckeri
Abstract :
[en] The interleukin (IL)-10 cytokine family includes IL-10, IL-19, IL-20, IL-22, IL-24, IL-26 and the lambda/type III interferons. They are highly pleiotropic and mediate a variety of activities, including immune suppression and antibacterial immunity. To exert their functions they signal through a heterodimeric receptor composed of a subunit with a long intracellular domain (R1 type receptors; IL-10R1, IL-20R1 or IL-22R1) and a subunit with a short intracellular domain (R2 type receptors; IL-10R2 or IL-20R2). In this study we report the identification of three R1 type receptors (named IL-10R1/CRFB7, IL-20R1a/CRFB8a and IL-20R1b/CRFB8b) and one R2 type receptor (named IL-10R2/CRFB4) in rainbow trout. The nomenclature of the receptors was supported by homology analysis, conserved motifs and phylogenetic tree analysis, confirming they belong to the piscine class 2 cytokine receptor family. For instance, they all displayed the presence of characteristic features, such as conserved fibronectin type-III domains. Expression analysis in tissues collected from healthy fish revealed different patterns of expression for each receptor, suggesting their potential involvement in different types of immune responses. When studying the modulation of the genes in cell lines and primary cultures, a greater effect was observed in the cell lines, where the expression of most receptors was affected by incubation with microbial mimics (LPS and PolyI:C) or the pro-inflammatory cytokine rIFN-gamma. In addition, expression of the four receptors was modulated by viral infection, suggesting a potential involvement of such receptors and their ligands in antiviral defence.
Aggad, D., Stein, C., Sieger, D., Mazel, M., Boudinot, P., Herbomel, P., In vivo analysis of IFN-γ1 and IFN-γ2 signalling in zebrafish (2010) J. Immunol, 185, pp. 6774-6782
Aggad, D., Mazel, M., Boudinot, P., Mogensen, K.E., Hamming, O.J., Hartman, R., The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains (2009) J. Immunol, 183, pp. 3924-3931
Bazan, J.F., Structural design and molecular evolution of a cytokine receptor superfamily (1990) Proc. Natl. Acad. Sci. U. S. A., 87, p. 6934
Blumberg, H., Conklin, D., Xu, W.F., Grossmann, A., Brender, T., Carollo, S., Interleukin 20: discovery, receptor identification, and role in epidermal function (2001) Cell, 104, pp. 9-19
Bols, N., Barlian, A., Chirino-Trejo, M., Caldwell, S., Goegan, P., Lee, L., Development of a cell line from primary cultures of rainbow trout, Oncorhynchus mykiss (Walbaum), gills (1994) J. Fish Dis, 17, pp. 601-611
Booth, D., George, J., Loss of function of the new interferon IFN-l4 may confer protection from hepatitis C (2013) Nat. Genet, 45, pp. 119-120
Campanella, J.J., Bitincka, L., Smalley, J., MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences (2003) BMC Bioinformatics, 4, p. 4
Campbell, S., McBeath, A., Secombes, C., Snow, M., Collet, B., Interferon response following infection with genetically similar isolates of viral haemorrhagic septicaemia virus (VHSV) exhibiting contrasting virulence in rainbow trout (2011) Fish Shellfish Immunol, 31, pp. 287-294
Chang, M.-C., Zou, J., Nie, P., Huan, B., Yu, Z., Collet, B., Intracellular interferons in fish: a unique means to combat viral infection (2013) PLoS Pathog, 9, p. e1003736
Chaudhry, A., Samstein, R., Treuting, P., Liang, Y., Pils, M.C., Heinrich, J.M., Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation (2011) Immunity, 34, pp. 566-578
Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G., Multiple sequence alignment with the clustal series of programs (2003) Nucleic Acids Res, 31, pp. 3497-3500
Dumoutier, L., Leemans, C., Lejeune, D., Kotenko, S.V., Renauld, J.C., Cutting edge: STAT activation by IL-19, IL-20 and mda-7 through IL-20 receptor complexes of two types (2001) J. Immunol, 167, pp. 3545-3549
Gibbs, V.C., Pennica, D., CRF2-4: isolation of cDNA clones encoding the human and mouse proteins (1997) Gene, 186, pp. 97-101
Grayfer, L., Belosevic, M., Identification and molecular characterization of the interleukin-10 receptor 1 of the zebrafish (Danio rerio) and the goldfish (Carassius auratus L (2012) Dev. Comp. Immunol, 36, pp. 408-417
Gupta, R., Jung, E., Brunak, S., (2004), Prediction of N-glycosylation sites in human proteins, NetGlycate 1.0 Server
Harun, N.O., Costa, M.M., Secombes, C.J., Wang, T., Sequencing of a second interleukin-10 gene in rainbow trout Oncorhynchus mykiss and comparative investigation of the expression and modulation of the paralogues invitro and invivo (2011) Fish Shellfish Immunol, 31, pp. 107-117
Ho, A., Liu, Y., Khan, T.A., Hsu, D.H., Bazan, J.F., Moore, K.W., A receptor for interleukin 10 is related to interferon receptors (1993) Proc. Natl. Acad. Sci. U. S. A., 90, pp. 11267-11271
Hofmann, K., Stoffel, W., TMbase - a database of membrane spanning proteins segments (1993) Biol. Chem. Hoppe-Seyler, 374, p. 166
Igawa, D., Sakai, M., Savan, R., An unexpected discovery of two interferon gamma-like genes along with interleukin (IL)-22 and -26 from teleost: IL-22 and -26 genes have been described for the first time outside mammals (2006) Mol. Immunol, 43, pp. 999-1009
Josephson, K., Logsdon, N.J., Walter, M.R., Crystal structure of the IL-10/IL-10R1 complex reveals a shared receptor binding site (2001) Immunity, 15, pp. 35-46
Koop, B.F., von Schalburg, K.R., Leong, J., Walker, N., Lieph, R., Cooper, G.A., A salmonid EST genomic study: genes, duplications, phylogeny and microarrays (2008) BMC Genomics, 9, p. 545
Kotenko, S.V., Langer, J.A., Full house: 12 receptors for 27 cytokines (2004) Int. Immunopharmacol, 4, pp. 593-608
Kotenko, S.V., Krause, C.D., Izotova, L.S., Pollack, B.P., Wu, W., Pestka, S., Identification and functional characterization of a second chain of the interleukin-10 receptor complex (1997) EMBO J., 16, pp. 5894-5903
Kotenko, S.V., Izotova, L.S., Mirochnitchenko, O.V., Esterova, E., Dickensheets, H., Donnelly, R.P., Identification of the functional interleukin-22 (IL-22) receptor complex (2001) J. Biol. Chem, 276, pp. 2725-2732
Krause, C.D., Pestka, S., Evolution of the class 2 cytokines and receptors, and discovery of new friends and relatives (2005) Pharmacol. Ther, 106, pp. 299-346
Langer, J.A., Cutrone, E.C., Kotenko, S., The class II cytokine receptor (CRF2) family: overview and patterns of receptor-ligand interactions (2004) Cytokine Growth Factor Rev, 15, pp. 33-48
Lee, L.E.J., Clemons, J.H., Bechtel, D.G., Caldwell, S.J., Han, K.B., Pasitschniak-Arts, M., Development and characterization of a rainbow trout liver cell line expressing cytochrome P450-dependent monooxygenase activity (1993) Cell Biol. Toxicol, 9, pp. 279-294
Letunic, I., Doerks, T., Bork, P., SMART 6: recent updates and new developments (2008) Nucleic Acids Res, 37, pp. 229-232
Levraud, J.P., Boudinot, P., Colin, I., Benmansour, A., Peyrieras, N., Herbomel, P., Identification of the zebrafish IFN receptor: implications for the origin of the vertebrate IFN system (2007) J. Immunol, 178, pp. 4385-4394
Liu, Y., Wei, S., Ho, A., de Waal Malefyt, R., Moore, K.W., Expression cloning and characterization of a human IL-10 receptor (1994) J. Immunol, 152, pp. 1821-1829
Lutfalla, G., Gardiner, K., Uzé, G., A new member of the cytokine receptor gene family maps on chromosome 21 at less than 35 kb from IFNAR (1993) Genomics, 16, pp. 366-373
Lutfalla, G., Roest Crollius, H., Stange-Thomann, N., Jaillon, O., Mogensen, K., Monneron, D., Comparative genomic analysis reveals independent expansion of a lineage-specific gene family in vertebrates: the class II cytokine receptors and their ligands in mammals and fish (2003) BMC Genomics, 4, pp. 1-15
Martin, S.A., Zou, J., Houlihan, D.F., Secombes, C.J., Directional responses following recombinant cytokine stimulation of rainbow trout (Oncorhynchus mykiss) RTS-11 macrophage cells as revealed by transcriptome profiling (2007) BMC Genomics, 8, p. 150
Monte, M.M., Zou, J., Wang, T., Carrington, A., Secombes, C.J., Cloning, expression analysis and bioactivity studies of rainbow trout (Oncorhynchus mykiss) interleukin-22 (2011) Cytokine, 55, pp. 62-73
Monte, M.M., Wang, T., Holland, J., Zou, J., Secombes, C.J., Cloning and characterization of rainbow trout interleukin-17A/F2 (IL-17A/F2) and IL-17 receptor A: expression during infection and bioactivity analysis of recombinant IL-17A/F2 (2013) Infect. Immun, 81, pp. 340-353
Petersen, T.N., Brunak, S., von Heijne, G., Nielsen, H., SignalP 4.0: discriminating signal peptides from transmembrane regions (2011) Nat. Methods, 8, pp. 785-786
Saitou, F., Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees (1987) Mol. Biol. Evol, 4, pp. 406-425
Sheikh, F., Baurin, V.V., Lewis-Antes, A., Shah, N.K., Smirnov, S.V., Anantha, S., Cutting edge: IL-26 signals through a novel receptor complex composed of IL-20 receptor 1 and IL-10 receptor 2 (2004) J. Immunol, 1724, pp. 2006-2010
Stein, C., Caccamo, M., Laird, G., Leptin, M., Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish (2007) Genome Biol, 8, p. 23
Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., MEGA6: molecular evolutionary genetics analysis version 6.0 (2013) Mol. Biol. Evol, 30, pp. 2725-2729
Trivella, D.B.B., Ferreira-Júnior, J.R., Dumoutier, L., Renauld, J.C., Polikarpov, I., Structure and function of interleukin-22 and other members of the interleukin-10 family (2010) Cell. Mol. Life Sci, 67, pp. 2909-2935
Wang, M., Tan, Z., Zhang, R., Kotenko, S.V., Liang, P., Interleukin 24 (MDA-7/MOB-5) signals through two heterodimeric receptors, IL-22R1/IL-20R2 and IL-20R1/IL-20R2 (2002) J. Biol. Chem, 277, p. 7341
Wang, T., Secombes, C.J., Complete sequencing and expression of three complement components, C1r, C4 and C1 inhibitor, of the classical activation pathway of the complement system in rainbow trout Oncorhynchus mykiss (2003) Immunogenetics, 55, pp. 615-628
Wang, T., Holland, J.W., Bols, N., Secombes, C.J., Cloning and expression of the first nonmammalian interleukin-11 gene in rainbow trout Oncorhynchus mykiss (2005) FEBS J., 272, pp. 1136-1147
Wang, T., Díaz-Rosales, P., Martin, S.A.M., Secombes, C.J., Cloning of a novel interleukin (IL)-20-like gene in rainbow trout Oncorhynchus mykiss gives an insight into the evolution of the IL-10 family (2010) Dev. Comp. Immunol, 34, pp. 158-167
Wang, T., Huang, W., Costa, M.M., Martin, S.A.M., Secombes, C.J., Two copies of the genes encoding the subunits of putative interleukin (IL)-4/IL-13 receptors, IL- 4Rα, IL-13Rα1 and IL-13Rα2, have been identified in rainbow trout (Oncorhynchus mykiss) and have complex patterns of expression and modulation (2011) Immunogenetics, 63, pp. 235-253
Wei, H., Wang, S., Qin, L., Wang, X., Zhou, H., Molecular characterization, 3D modelling of grass carp interleukin-10 receptor 1 (IL10R1) (2013) Engineering, 5, pp. 214-219
Wei, H., Wang, X., Zhang, A., Du, L., Zhou, H., Identification of grass carp IL-10 receptor subunits: functional evidence for IL-10 signaling in teleost immunity (2014) Dev. Comp. Immunol, 45, pp. 259-268
Wolf, K., Quimby, M.C., Established eurythermic line of fish cells in vitro (1962) Science, 135, pp. 1065-1066
Wolk, K., Kunz, S., Asadullah, K., Sabat, R., Cutting edge: immune cells as sources and targets of the IL-10 family members? (2002) J. Immunol, 168, pp. 5397-5402
Wolk, K., Kunz, S., Witte, E., Friedrich, M., Asadullah, K., Sabat, R., IL-22 increases the innate immunity of tissues (2004) Immunity, 21, pp. 241-254
Xie, M.H., Aggarwal, S., Ho, W.H., Foster, J., Zhang, Z., Stinson, J., Interleukin (IL)-22, a novel human cytokine that signals through the interferon receptor-related proteins CRF2-4 and IL-22R (2000) J. Biol. Chem, 275, pp. 31335-31339
Xu, W., Presnell, S.R., Parrish-Novak, J., Kindsvogel, W., Jaspers, S., Chen, Z., A soluble class II cytokine receptor, IL-22RA2, is a naturally occurring IL-22 antagonist (2001) Proc. Natl. Acad. Sci. U. S. A., 98, pp. 9511-9516
Zou, J., Secombes, C.J., Teleost fish interferons and their role in immunity (2011) Dev. Comp. Immunol, 35, pp. 1376-1387
Zou, J., Carrington, A., Collet, B., Dijkstra, J.M., Yoshiura, Y., Bols, N., Identification and bioactivities of IFN-γ in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish (2005) J. Immunol, 175, pp. 2484-2494
