Salmonids have an extraordinary complex type I IFN system: Characterization of the IFN locus in rainbow trout oncorhynchus mykiss reveals two novel IFN subgroups

Journal of Immunology

Volumn 193, Issue 5, 2014, Pages 2273-2286

  Zou, Jun ^a   Gorgoglione, Bartolomeo ^a,b,h   Taylor, Nicholas G H ^b   Summathed, Thitiya ^a   Lee, Po Tsang ^a   Panigrahi, Akshaya ^a   Genet, Carine ^c   Chen, Young Mao ^d   Chen, Tzong Yueh ^d   Ul Hassan, Mahmood ^e   Mughal, Sharif M ^f   Boudinot, Pierre ^g   Secombes, Christopher J ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b CENTRE FOR ENVIRONMENT   (United Kingdom)

^c UMR1313 GÉNÉTIQUE ANIMALE ET BIOLOGIE INTÉGRATIVE   (France)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^e GC UNIVERSITY   (Pakistan)

^f UNIVERSITY OF VETERINARY AND ANIMAL SCIENCES   (Pakistan)

^g INRA Institut National de la Recherche Agronomique   (France)

^h UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERFERON A; INTERFERON B; INTERFERON C; INTERFERON D; INTERFERON E; INTERFERON F; POLYINOSINIC POLYCYTIDYLIC ACID; RESIQUIMOD; UNCLASSIFIED DRUG; FISH PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BROWN TROUT; CONTROLLED STUDY; GENE EXPRESSION; GENE IDENTIFICATION; HEAD KIDNEY; INTERFERON INDUCTION; KIDNEY; LEUKOCYTE; MARKER GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; RAINBOW TROUT; REGULATORY SEQUENCE; SEQUENCE ANALYSIS; SPLEEN; VIRAL HEMORRHAGIC SEPTICEMIA; VIRUS LOAD; ANIMAL; ANTIBODY SPECIFICITY; GENE LOCUS; GENETICS; IMMUNOLOGY; MOLECULAR GENETICS; PHYSIOLOGY;

ANIMALS; BASE SEQUENCE; FISH PROTEINS; GENETIC LOCI; INTERFERON TYPE I; MOLECULAR SEQUENCE DATA; ONCORHYNCHUS MYKISS; ORGAN SPECIFICITY;

EID: 84907033620     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301796     Document Type: Article

References (54)

1. Robertsen, B. 2006. The interferon system of teleost fish. Fish Shellfish Immunol. 20: 172-191.
2. Zou, J., and C. J. Secombes. 2011. Teleost fish interferons and their role in immunity. Dev. Comp. Immunol. 35: 1376-1387.
3. Zhang, Y. B., and J. F. Gui. 2012. Molecular regulation of interferon antiviral response in fish. Dev. Comp. Immunol. 38: 193-202.
4. Robertsen, B., V. Bergan, T. Røkenes, R. Larsen, and A. Albuquerque. 2003. Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J. Interferon Cytokine Res. 23: 601-612.
5. Sun, B., B. Robertsen, Z. Wang, and B. Liu. 2009. Identification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Dev. Comp. Immunol. 33: 547-558.
6. Kitao, Y., T. Kono, H. Korenaga, T. Iizasa, K. Nakamura, R. Savan, and M. Sakai. 2009. Characterization and expression analysis of type I interferon in common carp Cyprinus carpio L. Mol. Immunol. 46: 2548-2556.
7. Long, S., I. Milev-Milovanovic, M. Wilson, E. Bengten, L. W. Clem, N. W. Miller, and V. G. Chinchar. 2006. Identification and expression analysis of cDNAs encoding channel catfish type I interferons. Fish Shellfish Immunol. 21: 42-59.
8. Lutfalla, G., H. Roest Crollius, N. Stange-Thomann, O. Jaillon, K. Mogensen, and D. Monneron. 2003. 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. BMC Genomics 4: 29.
9. Yu, F. F., Y. B. Zhang, T. K. Liu, Y. Liu, F. Sun, J. Jiang, and J. F. Gui. 2010. Fish virus-induced interferon exerts antiviral function through Stat1 pathway. Mol. Immunol. 47: 2330-2341.
10. Casani, D., E. Randelli, S. Costantini, A. M. Facchiano, J. Zou, S. Martin, C. J. Secombes, G. Scapigliati, and F. Buonocore. 2009. Molecular characterisation and structural analysis of an interferon homologue in sea bass (Dicentrarchus labrax L.). Mol. Immunol. 46: 943-952.
11. Chang, M., P. Nie, B. Collet, C. J. Secombes, and J. Zou. 2009. Identification of an additional two-cysteine containing type I interferon in rainbow trout Oncorhynchus mykiss provides evidence of a major gene duplication event within this gene family in teleosts. Immunogenetics 61: 315-325.
12. Zou, J., C. Tafalla, J. Truckle, and C. J. Secombes. 2007. Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J. Immunol. 179: 3859-3871.
13. Altmann, S. M., M. T. Mellon, D. L. Distel, and C. H. Kim. 2003. Molecular and functional analysis of an interferon gene from the zebrafish, Danio rerio. J. Virol. 77: 1992-2002.
14. Stein, C., M. Caccamo, G. Laird, and M. Leptin. 2007. Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish. Genome Biol. 8: R251.
15. Aggad, D., M. Mazel, P. Boudinot, K. E. Mogensen, O. J. Hamming, R. Hartmann, S. Kotenko, P. Herbomel, G. Lutfalla, and J. P. Levraud. 2009. The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains. J. Immunol. 183: 3924-3931.
16. Qi, Z., P. Nie, C. J. Secombes, and J. Zou. 2010. Intron-containing type I and type III IFN coexist in amphibians: refuting the concept that a retroposition event gave rise to type I IFNs. J. Immunol. 184: 5038-5046.
17. Hamming, O. J., G. Lutfalla, J. P. Levraud, and R. Hartmann. 2011. Crystal structure of Zebrafish interferons I and II reveals conservation of type I interferon structure in vertebrates. J. Virol. 85: 8181-8187.
18. Pestka, S., C. D. Krause, and M. R. Walter. 2004. Interferons, interferon-like cytokines, and their receptors. Immunol. Rev. 202: 8-32.
19. Svingerud, T., T. Solstad, B. Sun, M. L. Nyrud, Ø. Kileng, L. Greiner-Tollersrud, and B. Robertsen. 2012. Atlantic salmon type I IFN subtypes show differences in antiviral activity and cell-dependent expression: evidence for high IFNb/IFNcproducing cells in fish lymphoid tissues. J. Immunol. 189: 5912-5923.
20. López-Muñoz, A., F. J. Roca, J. Meseguer, and V. Mulero. 2009. New insights into the evolution of IFNs: zebrafish group II IFNs induce a rapid and transient expression of IFN-dependent genes and display powerful antiviral activities. J. Immunol. 182: 3440-3449.
21. Sun, B., I. Skjæveland, T. Svingerud, J. Zou, J. Jørgensen, and B. Robertsen. 2011. Antiviral activity of salmonid gamma interferon against infectious pancreatic necrosis virus and salmonid alphavirus and its dependency on type I interferon. J. Virol. 85: 9188-9198.
22. Xu, C., T. C. Guo, S. Mutoloki, Ø. Haugland, I. S. Marjara, and Ø. Evensen. 2010. Alpha interferon and not gamma interferon inhibits salmonid alphavirus subtype 3 replication in vitro. J. Virol. 84: 8903-8912.
23. Palti, Y., S. A. Gahr, J. D. Hansen, and C. E. Rexroad, III. 2004. Characterization of a new BAC library for rainbow trout: evidence for multi-locus duplication. Anim. Genet. 35: 130-133.
24. Campanella, J. J., L. Bitincka, and J. Smalley. 2003. MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 4: 29.
25. Wang, T., B. Gorgoglione, T. Maehr, J. W. Holland, J. L. Vecino, S. Wadsworth, and C. J. Secombes. 2011. Fish Suppressors of Cytokine Signaling (SOCS): Gene Discovery, Modulation of Expression and Function. J. Signal Transduct. 2011: 905813.
26. Stone, D. M., H. W. Ferguson, P. A. Tyson, J. Savage, G. Wood, M. J. Dodge, G. Woolford, P. F. Dixon, S. W. Feist, and K. Way. 2008. The first report of viral haemorrhagic septicaemia in farmed rainbow trout, Oncorhynchus mykiss (Walbaum), in the United Kingdom. J. Fish Dis. 31: 775-784.
27. Pham, P. H., J. Jung, and N. C. Bols. 2011. Using 96-well tissue culture polystyrene plates and a fluorescence plate reader as tools to study the survival and inactivation of viruses on surfaces. Cytotechnology 63: 385-397.
28. Cutrín, J. M., J. G. Olveira, I. Bandín, and C. P. Dopazo. 2009. Validation of real time RT-PCR applied to cell culture for diagnosis of any known genotype of viral haemorrhagic septicaemia virus. J. Virol. Methods 162: 155-162.
29. Klaus, W., B. Gsell, A. M. Labhardt, B. Wipf, and H. Senn. 1997. The threedimensional high resolution structure of human interferon alpha-2a determined by heteronuclear NMR spectroscopy in solution. J. Mol. Biol. 274: 661-675.
30. Radhakrishnan, R., L. J. Walter, A. Hruza, P. Reichert, P. P. Trotta, T. L. Nagabhushan, and M. R. Walter. 1996. Zinc mediated dimer of human interferon-alpha 2b revealed by X-ray crystallography. Structure 4: 1453-1463.
31. Thomas, C., I. Moraga, D. Levin, P. O. Krutzik, Y. Podoplelova, A. Trejo, C. Lee, G. Yarden, S. E. Vleck, J. S. Glenn, et al. 2011. Structural linkage between ligand discrimination and receptor activation by type I interferons. Cell 146: 621-632.
32. Akabayov, S. R., Z. Biron, P. Lamken, J. Piehler, and J. Anglister. 2010. NMR mapping of the IFNAR1-EC binding site on IFNalpha2 reveals allosteric changes in the IFNAR2-EC binding site. Biochemistry 49: 687-695.
33. Volff, J. N. 2005. Genome evolution and biodiversity in teleost fish. Heredity (Edinb) 94: 280-294.
34. Wan, Q., W. D. Wicramaarachchi, I. Whang, B. S. Lim, M. J. Oh, S. J. Jung, H. C. Kim, S. Y. Yeo, and J. Lee. 2012. Molecular cloning and functional characterization of two duplicated two-cysteine containing type I interferon genes in rock bream Oplegnathus fasciatus. Fish Shellfish Immunol. 33: 886-898.
35. Near, T. J., R. I. Eytan, A. Dornburg, K. L. Kuhn, J. A. Moore, M. P. Davis, P. C. Wainwright, M. Friedman, and W. L. Smith. 2012. Resolution of ray-finned fish phylogeny and timing of diversification. Proc. Natl. Acad. Sci. USA 109: 13698-13703.
36. von Schalburg, K. R., R. Yazawa, J. de Boer, K. P. Lubieniecki, B. Goh, C. A. Straub, M. R. Beetz-Sargent, A. Robb, W. S. Davidson, R. H. Devlin, and B. F. Koop. 2008. Isolation, characterization and comparison of Atlantic and Chinook salmon growth hormone 1 and 2. BMC Genomics 9: 522.
37. Nei, M., and A. P. Rooney. 2005. Concerted and birth-and-death evolution of multigene families. Annu. Rev. Genet. 39: 121-152.
38. Roberts, R. J., and M. D. Pearson. 2005. Infectious pancreatic necrosis in Atlantic salmon, Salmo salar L. J. Fish Dis. 28: 383-390.
39. Bjornsson, B. T., S. O. Stefansson, and S. D. McCormick. 2011. Environmental endocrinology of salmon smoltification. Gen. Comp. Endocrinol. 170: 290-298.
40. Ludigs, K., V. Parfenov, R. A. Du Pasquier, and G. Guarda. 2012. Type I IFNmediated regulation of IL-1 production in inflammatory disorders. Cell Mol. Life Sci. 69: 3395-3418.
41. Chang, M. X., J. Zou, P. Nie, B. Huang, Z. Yu, B. Collet, and C. J. Secombes. 2013. Intracellular interferons in fish: a unique means to combat viral infection. PLoS Pathog. 9: e1003736.
42. Purcell, M. K., K. J. Laing, J. C. Woodson, G. H. Thorgaard, and J. D. Hansen. 2009. Characterization of the interferon genes in homozygous rainbow trout reveals two novel genes, alternate splicing and differential regulation of duplicated genes. Fish Shellfish Immunol. 26: 293-304.
43. Pettersen, E. F., H. C. Ingerslev, V. Stavang, M. Egenberg, and H. I. Wergeland. 2008. A highly phagocytic cell line TO from Atlantic salmon is CD83 positive and M-CSFR negative, indicating a dendritic-like cell type. Fish Shellfish Immunol. 25: 809-819.
44. Matsuo, A., H. Oshiumi, T. Tsujita, H. Mitani, H. Kasai, M. Yoshimizu, M. Matsumoto, and T. Seya. 2008. Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from birnaviruses. J. Immunol. 181: 3474-3485.
45. Chang, M., B. Collet, P. Nie, K. Lester, S. Campbell, C. J. Secombes, and J. Zou. 2011. Expression and functional characterization of the RIG-I-like receptors MDA5 and LGP2 in Rainbow trout (Oncorhynchus mykiss). J. Virol. 85: 8403-8412.
46. Biacchesi, S., M. LeBerre, A. Lamoureux, Y. Louise, E. Lauret, P. Boudinot, and M. Brémont. 2009. Mitochondrial antiviral signaling protein plays a major role in induction of the fish innate immune response against RNA and DNA viruses. J. Virol. 83: 7815-7827.
47. Zou, J., M. Chang, P. Nie, and C. J. Secombes. 2009. Origin and evolution of the RIG-I like RNA helicase gene family. BMC Evol. Biol. 9: 85.
48. Sato, M., H. Suemori, N. Hata, M. Asagiri, K. Ogasawara, K. Nakao, T. Nakaya, M. Katsuki, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-αlpha/beta gene induction. Immunity 13: 539-548.
49. Marié, I., J. E. Durbin, and D. E. Levy. 1998. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 17: 6660-6669.
50. Holland, J. W., S. Bird, B. Williamson, C. Woudstra, A. Mustafa, T. Wang, J. Zou, S. C. Blaney, B. Collet, and C. J. Secombes. 2008. Molecular characterization of IRF3 and IRF7 in rainbow trout, Oncorhynchus mykiss: functional analysis and transcriptional modulation. Mol. Immunol. 46: 269-285.
51. Sun, F., Y. B. Zhang, T. K. Liu, L. Gan, F. F. Yu, Y. Liu, and J. F. Gui. 2010. Characterization of fish IRF3 as an IFN-inducible protein reveals evolving regulation of IFN response in vertebrates. J. Immunol. 185: 7573-7582.
52. Bergan, V., Ø. Kileng, B. Sun, and B. Robertsen. 2010. Regulation and function of interferon regulatory factors of Atlantic salmon. Mol. Immunol. 47: 2005-2014.
53. Kileng, O., V. Bergan, S. T. Workenhe, and B. Robertsen. 2009. Structural and functional studies of an IRF-7-like gene from Atlantic salmon. Dev. Comp. Immunol. 33: 18-27.
54. Skjesol, A., T. Hansen, C. Y. Shi, H. L. Thim, and J. B. Jørgensen. 2010. Structural and functional studies of STAT1 from Atlantic salmon (Salmo salar). BMC Immunol. 11: 17.