Cloning and characterization of rainbow trout interleukin-17A/F2 (IL-17A/F2) and IL-17 receptor A: expression during infection and bioactivity of recombinant IL-17A/F2.
Mira Monte, Milena; Wang, Tiehui; Holland, Jason W.et al.
2013 • In Infection and Immunity, 81 (1), p. 340-53
[en] Lower vertebrates have been found to possess genes that have similar homology to both interleukin (IL)-17A and IL-17F, which have been termed IL-17A/F. In fish species, several of these genes can be present, but, to date, very little is known about their functional activity. This article describes the discovery and sequence analysis of a rainbow trout (Oncorhynchus mykiss) IL-17A/F2 molecule and an IL-17RA receptor. In addition, the bioactivity of the trout IL-17A/F2 is investigated for the first time in any species. The predicted IL-17A/F2 and IL-17RA proteins consist of 146 and 966 amino acids (aa), respectively, with both molecules containing conserved family motifs. Expression analysis revealed high constitutive expression of trout IL-17A/F2 in mucosal tissues from healthy fish, suggesting a potential role in mucosal immunity. When the modulation of IL-17A/F2 and IL-17RA in vitro was analyzed, it was observed that the two molecules were similarly affected. The expression of IL-17A/F2 was also induced in head kidney during bacterial, parasitic, and viral infections, revealing a possible function in defense against such pathogens. However, downregulation of IL-17RA was seen in some tissues and infections. The recombinant IL-17A/F2 protein was produced in Escherichia coli and was found to affect the expression of an antimicrobial peptide and the proinflammatory cytokines IL-6 and IL-8 in splenocytes. Consistent with mammalian IL-17 homologues, our expression and bioactivity results imply that trout IL-17A/F2 plays an important role in promoting inflammatory and host innate immune responses directed against different pathogen groups.
Cloning and characterization of rainbow trout interleukin-17A/F2 (IL-17A/F2) and IL-17 receptor A: expression during infection and bioactivity of recombinant IL-17A/F2.
Publication date :
2013
Journal title :
Infection and Immunity
ISSN :
0019-9567
eISSN :
1098-5522
Publisher :
American Society for Microbiology, Washington, United States - District of Columbia
Aggarwal, S., Gurney, A.L., IL-17: prototype member of an emerging cytokine family (2002) J. Leukoc. Biol., 71, pp. 1-8
Kolls, J.K., Lindén, A., Interleukin-17 family members and inflammation (2004) Immunity, 21, pp. 467-476
Yao, Z., Painter, S.L., Fanslow, W.C., Ulrich, D., Macduff, B.M., Spriggs, M.K., Armitage, R.J., Human IL-17: a novel cytokine derived from T cells (1995) J. Immunol., 155, pp. 5483-5486
Harrington, L.E., Hatton, R.D., Mangan, P.R., Turner, H., Murphy, T.L., Murphy, K.M., Weaver, C.T., Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages (2005) Nat. Immunol., 6, pp. 1123-1132
Langrish, C.L., Chen, Y., Blumenschein, W.M., Mattson, J., Basham, B., Sedgwick, J.D., McClanahan, T., Cua, D.J., IL-23 drives a pathogenic T cell population that induces autoimmune inflammation (2005) J. Exp. Med., 201, pp. 233-240
Park, H., Li, Z., Yang, X.O., Chang, S.H., Nurieva, R., Wang, Y.H., Wang, Y., Dong, C., A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17 (2005) Nat. Immunol., 6, pp. 1133-1141
Yao, Z., Fanslow, W.C., Seldin, M.F., Rousseau, A.M., Painter, S.L., Comeau, M.R., Cohen, J.I., Spriggs, M.K., Herpesvirus saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor (1995) Immunity, 3, pp. 811-821
Ivanov, I.I., McKenzie, B.S., Zhou, L., Tadokoro, C.E., Lepelley, A., Lafaille, J.J., Cua, D., Littman, D.R., The orphan nuclear receptor RORγt directs the differentiation program of proinflammatory IL-17 T helper cells (2006), 126, pp. 1121-1133
Ye, P., Garvey, P.B., Zhang, P., Nelson, S., Bagby, G., Summer, W.R., Schwarzenberger, P., Kolls, J.K., Interleukin-17 and lung host defense against Klebsiella pneumoniae infection (2001) Am. J. Respir. Cell Mol. Biol., 25, pp. 335-340
Liang, S.C., Tan, X.Y., Luxenberg, D.P., Karim, R., Dunussi-Joannopoulos, K., Collins, M., Fouser, L.A., Interleukin (IL)-22 and IL-17 are coex-pressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides (2006) J. Exp. Med., 203, pp. 2271-2279
Eyerich, S., Eyerich, K., Cavani, A., Schmidt-Weber, C., IL-17 and IL-22: siblings, not twins (2010) Trends Immunol., 31, pp. 354-361
Weaver, C.T., Hatton, R.D., Mangan, P.R., Harrington, L.E., IL-17 family cytokines and the expanding diversity of effector T cell lineages (2007) Annu. Rev. Immunol., 25, pp. 821-852
Hymowitz, S.G., Filvaroff, E.H., Yin, J.P., Lee, J., Cai, L., Risser, P., Maruoka, M., Starovasnik, M.A., IL-17s adopt a cystine knot fold: structure and activity of a novel cytokine, IL-17F, and implications for receptor binding (2001) EMBO J., 20, pp. 5332-5341
Starnes, T., Robertson, M.J., Sledge, G., Kelich, S., Nakshatri, H., Broxmeyer, H.E., Hromas, R., Cutting edge: IL-17F, a novel cytokine selectively expressed in activated T cells and monocytes, regulates angiogenesis and endothelial cell cytokine production (2001) J. Immunol., 167, pp. 4137-4140
Chang, S.H., Dong, C., A novel heterodimeric cytokine consisting of IL-17 and IL-17F regulates inflammatory responses (2007) Cell Res., 17, pp. 435-440
Gunimaladevi, I., Savan, R., Sakai, M., Identification, cloning and characterization of interleukin-17 and its family from zebrafish (2006) Fish Shellfish Immunol., 21, pp. 393-403
Korenaga, H., Kono, T., Sakai, M., Isolation of seven IL-17 family genes from the Japanese pufferfish Takifugu rubripes (2010) Fish Shellfish Immunol., 28, pp. 809-818
Kono, T., Korenaga, H., Sakai, M., Genomics of fish IL-17 ligand and receptors: a review (2011) Fish Shellfish Immunol., 31, pp. 635-643
Secombes, C.J., Wang, T., Bird, S., The interleukins of fish (2011) Dev. Comp. Immunol., 35, pp. 1336-1345
McAllister, F., Henry, A., Kreindler, J.L., Dubin, P.J., Ulrich, L., Steele, C., Finder, J.D., Kolls, J.K., Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis (2005) J. Immunol., 175, pp. 404-412
Kramer, J.M., Yi, L., Shen, F., Maitra, A., Jiao, X., Jin, T., Gaffen, S.L., Cutting edge: evidence for ligand-independent multimerization of the IL-17 receptor (2006) J. Immunol., 176, pp. 711-715
Toy, D., Kugler, D., Wolfson, M., Vandel Bos, T., Gurgel, J., Derry, J., Tocker, J., Peschon, J., Cutting edge: interleukin 17 signals through a heteromeric receptor complex (2006) J. Immunol., 177, pp. 36-39
Kuestner, R.E., Taft, D.W., Haran, A., Brandt, C.S., Brender, T., Lum, K., Harder, B., Levin, S.D., Identification of the IL-17 receptor related molecule IL-17RC as the receptor for IL-17F (2007) J. Immunol., 179, pp. 5462-5473
Gaffen, S.L., Structure and signalling in the IL-17 receptor family (2009) Nat. Rev. Immunol., 9, pp. 556-567
Wu, B., Jin, M., Zhang, Y., Wei, T., Bai, Z., Evolution of the IL17 receptor family in chordates: a new subfamily IL17REL (2011) Immunogenetics, 63, pp. 835-845
Novatchkova, M., Leibbrandt, A., Werzowa, J., Neubüser, A., Eisenhaber, F., The STIR-domain superfamily in signal transduction, development and immunity (2003) Trends Biochem. Sci., 28, pp. 226-229
Gaffen, S.L., An overview of IL-17 function and signaling (2008) Cytokine, 43, pp. 402-407
Yao, Z., Spriggs, M.K., Derry, J.M., Strockbine, L., Park, L.S., VandenBos, T., Zappone, J.D., Armitage, R.J., Molecular characterization of the human interleukin (IL)-17 receptor (1997) Cytokine, 9, pp. 794-80
Laan, M., Cui, Z.H., Hoshino, H., Lötvall, J., Sjöstrand, M., Gruenert, D.C., Skoogh, B.E., Lindén, A., Neutrophil recruitment by human IL-17 via CXC chemokine release in the airways (1999) J. Immunol., 162, pp. 2347-2352
Kawaguchi, M., Adachi, M., Oda, N., Kokubu, F., Huang, S.K., IL-17 cytokine family (2004) J. Allergy Clin. Immunol., 114, pp. 1265-1273
Aujla, S.J., Chan, Y.R., Zheng, M., Fei, M., Askew, D.J., Pociask, D.A., Reinhart, T.A., Kolls, J.K., IL-22 mediates mucosal host defense against gram-negative bacterial pneumonia (2008) Nat. Med., 14, pp. 275-281
Ouyang, W., Kolls, J.K., Zheng, Y., The biological functions of T helper 17 cell effector cytokines in inflammation (2008) Immunity, 28, pp. 454-467
Kao, C.Y., Chen, Y., Thai, P., Wachi, S., Huang, F., Kim, C., Harper, R.W., Wu, R., IL-17 markedly up-regulates beta-defensin-2 expression in human airway epithelium via JAK and NF-kappaB signaling pathways (2004) J. Immunol., 173, pp. 3482-3491
Wilson, N.J., Boniface, K., Chan, J.R., McKenzie, B.S., Blumenschein, W.M., Mattson, J.D., Basham, B., de Waal Malefyt, R., Development, cytokine profile and function of human interleukin 17-producing helper T cells (2007) Nat. Immunol., 8, pp. 950-957
Ishigame, H., Kakuta, S., Nagai, T., Kadoki, M., Nambu, A., Komiyama, Y., Fujikado, N., Iwakura, Y., Differential roles of interleukin-17A and-17F in host defense against mucoepithelial bacterial infection and allergic responses (2009) Immunity, 30, pp. 108-119
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
Casadei, E., Wang, T., Zou, J., González Vecino, J.L., Wadsworth, S., Secombes, C.J., Characterization of three novel beta-defensin antimicrobial peptides in rainbow trout (Oncorhynchus mykiss) (2009) Mol. Immunol., 46, pp. 3358-3366
Komatsu, K., Tsutsui, S., Hino, K., Araki, K., Yoshiura, Y., Yamamoto, A., Nakamura, O., Watanabe, T., Expression profiles of cytokines released in intestinal epithelial cells of the rainbow trout, Oncorhynchus mykiss, in response to bacterial infection (2009) Dev. Comp. Immunol., 33, pp. 499-506
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
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs (1997) Nucleic Acids Res., 25, pp. 3389-3402
Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G., Thompson, J.D., Multiple sequence alignment with the clustal series of programs (2003) Nucleic Acids Res., 31, pp. 3497-3500
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
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. 29
Tamura, K., Dudley, J., Nei, M., Kumar, S., MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0 (2007) Mol. Biol. Evol., 24, pp. 1596-1599
Letunic, I., Doerks, T., Bork, P., SMART 6: recent updates and new developments (2009) Nucleic Acids Res., 37, pp. D229 -D232. , (Database issue)
Marsden, R.L., McGuffin, L.J., Jones, D.T., Rapid protein domain assignment from amino acid sequence using predicted secondary structure (2002) Protein Sci., 11, pp. 2814-2814
Wang, T., Díaz-Rosales Costa, M.M., Campbell, S., Snow, M., Collet, B., Martin, S.A., Secombes, C.J., Functional characterization of a non-mammalian IL-21: rainbow trout Oncorhynchus mykiss IL-21 upregulates the expression of the Th cell signature cytokines IFN-gamma, IL-10, and IL-22 (2011) J. Immunol., 186, pp. 708-721
Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT-PCR (2001) Nucleic Acids Res., 29, pp. e45
Harun, N.O., Wang, T., Secombes, C.J., Gene expression profiling in naïve and vaccinated rainbow trout after Yersinia ruckeri infection: insights into the mechanisms of protection seen in vaccinated fish (2011) Vaccine, 29, pp. 4388-4399
Tobback, E., Decostere, A., Hermans, K., Ryckaert, J., Duchateau, L., Haesebrouck, F., Chiers, K., Route of entry and tissue distribution of Yersinia ruckeri in experimentally infected rainbow trout Oncorhynchus mykiss (2009) Dis. Aquat. Organ., 84, pp. 219-228
Wang, T., Holland, J.W., Martin, S.A.M., Secombes, C.J., Sequence and expression analysis of two T helper master transcription factors, T-bet and GATA3, in rainbow trout Oncorhynchus mykiss and analysis of their expression during bacterial and parasitic infection (2010) Fish Shellfish Immunol, 29, pp. 705-715
Clifton-Hadley, R.S., Bucke, D., Richards, R.H., A study of the sequential clinical and pathological changes during proliferative kidney disease in rainbow trout (1987) J. Fish Dis., 10, pp. 335-352. , Salmo gairdneri Richardson
Campbell, S., McBeath, A., Secombes, C., Snow, M., Collet, B., Inter-feron response following infection with genetically similar isolates of viral haemorrhagic septicaemia virus (VHSV) exhibiting contrasting virulence in rainbow trout (2011) Fish Shellfish Immunol, 30, pp. 287-294
Zou, J., Carrington, A., Collet, B., Dijkstra, J.M., Yoshiura, Y., Bols, N., Secombes, C., Identification and bioactivities of IFN-gamma in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish (2005) J. Immunol., 175, pp. 2484-2494
Laing, K.J., Wang, T., Zou, J., Holland, J., Hong, S., Bols, N., Hirono, I., Secombes, C.J., Cloning and expression analysis of rainbow trout Oncorhynchus mykiss tumour necrosis factor-alpha (2001) Eur. J. Biochem., 268, pp. 1315-1322
Iliev, D.B., Castellana, B., MacKenzie, S., Planas, J.V., Goetz, F.W., Cloning and expression analysis of an IL-6 homolog in rainbow trout (Oncorhynchus mykiss) (2007) Mol. Immunol., 44, pp. 1803-1807
Laing, K.J., Zou, J.J., Wang, T., Bols, N., Hirono, I., Aoki, T., Secombes, C.J., Identification and analysis of an interleukin 8-like molecule in rainbow trout Oncorhynchus mykiss (2002) Dev. Comp. Immunol., 26, pp. 433-444
Morris, D.R., Geballe, A.P., Upstream open reading frames as regulators of mRNA translation (2000) Mol. Cell. Biol., 20, pp. 8635-8642
Tobback, E., Decostere, A., Hermans, K., Haesebrouck, F., Chiers, K., Yersinia ruckeri infections in Salmonid fish (2007) J. Fish Dis., 30, pp. 257-268
Okamura, B., Hartikainen, H., Schmidt-Posthaus, H., Wahli, T., Life cycle complexity, environmental change and the emerging status of salmonid proliferative kidney disease (2011) Freshwater Biol., 56, pp. 735-753
Tafalla, C., Coll, J., Secombes, C., Expression of genes related to the early immune response in rainbow trout (Oncorhynchus mykiss) after viral haemorrhagic septicemia virus (VHSV) infection (2005) Dev. Comp. Immunol., 29, pp. 615-626
Wang, T., Martin, S.A.M., Secombes, C.J., Two interleukin-17C-like genes exist in rainbow trout Oncorhynchus mykiss that are differentially expressed and modulated (2010) Dev. Comp. Immunol., 34, pp. 491-500
Rouvier, E., Luciani, M., Mattei, M., Denizot, F., Golstein, P., CTLA-8, cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a herpesvirus saimiri gene (1993) J. Immunol., 150, pp. 5445-5456
Ely, L.K., Fischer, S., Garcia, K.C., Structural basis of receptor sharing by interleukin 17 cytokines (2009) Nat. Immunol., 10, pp. 1245-1251
Molet, S., Hamid, Q., Davoine, F., Nutku, E., Taha, R., Pagé, N., Olivenstein, R., Chakir, J., IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines (2001) J. Allergy Clin. Immunol., 108, pp. 430-438
Wang, T., Díaz-Rosales Martin, S.A., 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
Fernández, L., Méndez, J., Guijarro, J.A., Molecular virulence mechanisms of the fish pathogen Yersinia ruckeri (2007) Vet. Microbiol., 125, pp. 1-10
Ye, P., Rodriguez, F.H., Kanaly, S., Stocking, K.L., Schurr, J., Schwarzenberger, P., Oliver, P., Kolls, J.K., Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense (2001) J. Exp. Med., 194, pp. 519-527
Matsuzaki, G., Umemura, M., Interleukin-17 as an effector molecule of innate and acquired immunity against infections (2007) Microbiol. Immunol., 51, pp. 1139-1147
Ribeiro, C.M.S., Pontes, M.J.S.L., Bird, S., Chadzinska, M., Scheer, M., Kemenade, B.M.L.V., Savelkoul, H.F.J., Wiegertjes, G.F., Trypanosomiasis-induced Th17-like immune responses in carp (2010) PLoS One, 5. , e13012. doi: 10.1371/journal.pone.0013012
Skall, H.F., Olesen, N.J., Mellergaard, S., Viral haemorrhagic septicaemia virus in marine fish and its implications for fish farming-a review (2005) J. Fish Dis., 28, pp. 509-529
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
Falco, A., Chico, V., Marroqui, L., Perez, L., Coll, J., Estepa, A., Expression and antiviral activity of a beta-defensin-like peptide identified in the rainbow trout (Oncorhynchus mykiss) EST sequences (2008) Mol. Immunol., 45, pp. 757-765
Kawaguchi, M., Kokubu, F., Kuga, H., Matsukura, S., Hoshino, H., Ieki, K., Imai, T., Huang, S.K., Modulation of bronchial epithelial cells by IL-17 (2001) J. Allergy Clin. Immunol., 108, pp. 804-809
Ammit, A.J., Lazaar, A.L., Irani, C., O'Neill, G.M., Gordon, N.D., Amrani, Y., Penn, R.B., Panettieri Jr., R.A., Tumor necrosis factor-alpha-induced secretion of RANTES and interleukin-6 from human airway smooth muscle cells: modulation by glucocorticoids and beta-agonists (2002) Am. J. Respir. Cell Mol. Biol., 26, pp. 465-474
Bergamaschi, A., Corsi, M., Garnier, M.J., Synergistic effects of cAMP-dependent signalling pathways and IL-1 on IL-6 production by H19-7/ IGF-IR neuronal cells (2006) Cell Signal, 18, pp. 1679-1684
Costa, M.M., Maehr, T., Díaz-Rosales, P., Secombes, C.J., Wang, T., Bioactivity studies of rainbow trout (Oncorhynchus mykiss) interleukin-6: effects on macrophage growth and antimicrobial peptide gene expression (2011) Mol. Immunol., 48, pp. 1903-1916
Raida, M.K., Buchmann, K., Innate immune response in rainbow trout (Oncorhynchus mykiss) against primary and secondary infections with Yersinia ruckeri O1 (2009) Dev. Comp. Immunol., 33, pp. 35-45
Harun, N.O., Zou, J., Zhang, Y.A., Nie, P., Secombes, C.J., The biological effects of rainbow trout (Oncorhynchus mykiss) recombinant interleukin-8 (2008) Dev. Comp. Immunol., 32, pp. 673-681