Innate immune responses of salmonid fish to viral infections

Developmental and Comparative Immunology

Volumn 43, Issue 2, 2014, Pages 160-173

  Collet, Bertrand ^a  

^a MARINE LABORATORY   (United Kingdom)

Author keywords

Innate immunity; Interferon; Mx; Salmonidae; Viral infection; Virus

Indexed keywords

ACUTE PHASE PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 8; MANNAN BINDING LECTIN; MYELOID DIFFERENTIATION FACTOR 88; MYXOVIRUS RESISTANCE PROTEIN; PATTERN RECOGNITION RECEPTOR; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN KINASE R; ANTIMICROBIAL CATIONIC PEPTIDE;

ADAPTIVE IMMUNITY; APOPTOSIS; CELLULAR IMMUNITY; COMPLEMENT SYSTEM; DENDRITIC CELL; ENVIRONMENTAL PARAMETERS; FISH DISEASE; GENE; GENE INDUCTION; HOST RESISTANCE; HUMORAL IMMUNITY; IMMUNE EVASION; IMMUNOCOMPETENT CELL; INFLAMMATION; INNATE IMMUNITY; INTERFERON GENE; ISG15 GENE; MACROPHAGE; MX GENE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PKR GENE; PRIORITY JOURNAL; REVIEW; SALMONID; SIGNAL TRANSDUCTION; TRIM GENE; VIG 1 GENE; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS REPLICATION; ANIMAL; GENETICS; IMMUNOLOGY; METABOLISM;

ONCORHYNCHUS MYKISS; SALMO SALAR; SALMONIDAE;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; APOPTOSIS; IMMUNITY, INNATE; INFLAMMATION; INTERFERON TYPE I; SALMONIDAE; VIRUS DISEASES;

EID: 84891829101     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.08.017     Document Type: Review

References (300)

1. Aamelfot M., Dale O.B., Weli S.W., Koppang E.O., Falk K. Expression of the ISAV receptor on Atlantic salmon endothelial cells correlates with cell tropism of the virus. J. Virol. 2012, 86:10571-10578.
2. Acosta F., Collet B., Lorenzen N., Ellis A.E. Expression of the glycoprotein of viral haemorrhagic septicaemia virus (VHSV) on the surface of the fish cell line RTG-P1 induces type 1 interferon expression in neighbouring cells. Fish Shellfish Immunol. 2006, 21:272-278.
3. Alcorn S.W., Murray A.L., Pascho R.J. Effects of rearing temperature on immune functions in sockeye salmon (Oncorhynchus nerka). Fish Shellfish Immunol. 2002, 12:303-334.
4. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738.
5. Altmann S.M., Mellon M.T., Distel D.L., Kim C.H. Molecular and functional analysis of an interferon gene from the zebrafish, Danio rerio. J. Virol. 2003, 77:1992-2002.
6. Amend D.F., Smith L. Pathophysiology of infectious hematopoietic necrosis virus disease in rainbow trout: haematological and blood chemical changes in moribund fish. Infect. Immun. 1975, 11:171-179.
7. Ammayappan A., Vakharia V.N. Nonvirion protein of novirhabdovirus suppresses apoptosis at the early stage of virus infection. J. Virol. 2011, 85:8393-8402.
8. Ammayappan A., Kurath G., Thompson T.M., Vakharia V.N. A reverse genetics system for the Great Lakes strain of viral hemorrhagic septicemia virus: the NV gene is required for pathogenicity. Mar. Biotechnol. 2011, 13:672-683.
9. Ananko E.A., Kondrakhin Y.V., Merkulova T.I., Kolchanov N.A. Recognition of interferon-inducible sites, promoters, and enhancers. BMC Bioinformatics 2007, 8:56.
10. Andersen L., Hodneland K., Nylund A. No influence of oxygen levels on pathogenesis and virus shedding in Salmonid alphavirus (SAV)-challenged Atlantic salmon (Salmo salar L.). Virol. J. 2010, 7:198.
11. Aoki, T., Hikima, J.-I., Hwang, S.D, Jung, T.-S., in press. Innate immunity of finfish: Primordial conservation and function of viral RNA sensors in teleosts. Fish Shellfish Immunol.
12. Asselin-Paturel C., Boonstra A., Dalod M., Durand I., Yessaad N., Dezutter-Dambuyant C., Vicari A., O'Garra A., Biron C., Briere F., Trinchieri G. Mouse type I IFN-producing cells are immature APCs with plasmacytoid. Morphology 2007, 2:1144-1150.
13. Avtalion R.R., Wojdani A., Malik Z., Shahrabani R., Duczyminer M. Influence of environmental temperature on the immune response in fish. Curr. Top. Microbiol. Immunol. 1973, 61:1-35.
14. Baggiolini M., Dewald B., Moser B. Interleukin-8 and related chemotactic cytokines: CXC and CC chemokines. Adv. Immunol. 1994, 55:97-179.
15. Baggiolini M., Dewald B., Moser B. Human chemokines: an update. Annu. Rev. Immunol. 1997, 15:675-705.
16. Ballesteros N.A., Saint-Jean S.S., Encinas P.A., Perez-Prieto S.I., Coll J.M. Oral immunization of rainbow trout to infectious pancreatic necrosis virus (IPNV) induces different immune gene expression profiles in head kidney and pyloric ceca. Fish Shellfish Immunol. 2012, 33:174-185.
17. Banchereau J., Briere F., Caux C., Davoust J., Lebecque S., Liu Y.-J., Pulendran B., Palucka K. Immunobiology of dendritic cells. Annu. Rev. Immunol. 2000, 2000(18):767-811.
18. Barton B.A. Salmonid fishes differ in their cortisol and glucose responses to handling and transport stress. North Am. J. Aquac. 2000, 62:12-18.
19. Barton B.A., Iwama G.K. Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Ann. Rev. Fish Dis. 1991, 1:3-26.
20. Bassity E., Clark T.G. Functional identification of dendritic cells in the teleost model, rainbow trout (Oncorhynchus mykiss). PLoS One 2012, 7:33196.
21. Benedict C.A., Norris P.S., Ware C.F. To kill or be killed: viral evasion of apoptosis. Nat. Immunol. 2002, 3:1013-1018.
22. Bergan V., Steinsvik S., Xu H., Kileng Ø., Robertsen B. Promoters of type I interferon genes from Atlantic salmon contain two main regulatory regions. FEBS J. 2006, 273:3893-3906.
23. Bergan V., Kileng Ø., Sun B., Robertsen B. Regulation and function of interferon regulatory factors of Atlantic salmon. Mol. Immunol. 2010, 47:2005-2014.
24. Bhoj V.J., Sun Q., Bhoj E.J., Somers C., Chen X., Torres J.-P., Mejias A., Gomez A.M., Jafri H., Ramilo O., Chen Z.J. MAVS and MyD88 are essential for innate immunity but not cytotoxic T lymphocyte response against respiratory syncytial virus. Proc. Natl. Acad. Sci. USA 2008, 105:14046-14051.
25. Biacchesi S. The reverse genetics applied to fish RNA viruses. Vet. Res. 2011, 42:12.
26. Biacchesi S., LeBerre M., Lamoureux A., Louise Y., Lauret E., Boudinot P., Brémont M. Mitochondrial antiviral signaling protein plays a major role in induction of the fish innate immune response against RNA and DNA viruses. J. Virol. 2009, 83:7815-7827.
27. Biron C.A., Nguyen K.B., Pien G.C., Cousens L.P., Salazar-Mather T.P. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 1999, 17:189-220.
28. Blue C.E., Spiller O.B., Blackbourn D.J. The relevance of complement to virus biology. Virology 2004, 319:176-184.
29. Bonga S.E.W. The stress response in fish. Physiol. Rev. 1997, 77:591-625.
30. Boudinot P., Massin P., Blanco M., Riffault S., Benmansour A. Vig-1, a new fish gene induced by the rhabdovirus glycoprotein, has a virus-induced homologue in humans and shares conserved motifs with the MoaA family. J. Virol. 1999, 73:1846-1852.
31. 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. Fish Shellfish Immunol. 2011, 30:287-294.
32. Casadei E., Wang T., Zou J., Vecino J.L.G., Wadsworth S., Secombes C.J. Characterization of three novel b-defensin antimicrobial peptides in rainbow trout (Oncorhynchus mykiss). Mol. Immunol. 2009, 46:3358-3366.
33. Chang C.I., Pleguezuelos O., Zhang Y.-A., Zou J., Secombes C.J. Identification of a novel cathelicidin gene in the rainbow trout, Oncorhynchus mykiss. Infect. Immun. 2005, 73:5053-5064.
34. Chang M., Nie P., Collet B., Secombes C.J., Zou J. 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 2009, 61:315-325.
35. Chang M., Collet B., Nie P., Lester K., Campbell S., Secombes C.J., Zou J. Expression and functional characterization of the RIG-I-like receptors MDA5 and LGP2 in rainbow trout (Oncorhynchus mykiss). J. Virol. 2011, 85:8403-8412.
36. Chaves-Pozo E., Montero J., Cuesta A., Tafalla C. Viral hemorrhagic septicaemia and infectious pancreatic necrosis viruses replicate differently in rainbow trout gonad and induce different chemokine transcription profiles. Dev. Comp. Immunol. 2010, 34:648-658.
37. Chaves-Pozo E., Zou J., Secombes C.J., Cuesta A., Tafalla C. The rainbow trout (Oncorhynchus mykiss) interferon response in the ovary. Mol. Immunol. 2010, 47:1757-1764.
38. Chawla-Sarkar M., Lindner D.J., Liu Y.-F., Williams B.R., Sen G.C., Silverman R.H., Borden E.C. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 2003, 8:237-249.
39. Chill J.H., Quadt S.R., Levy R., Schreiber G., Anglister J. The human type I interferon receptor: NMR structure reveals the molecular basis of ligand binding. Structure 2003, 11:791-802.
40. Chinchar V.G., Bryan L., Silphadaung U., Noga E., Wade D., Rollins-Smith L. Inactivation of viruses infecting ectothermic animals by amphibian and piscine antimicrobial peptides. Virology 2004, 323:268-275.
41. Chiou P.P., Kim C.H., Ormonde P., Leong J.A. Infectious hematopoietic necrosis virus matrix protein inhibits host-directed gene expression and induces morphological changes of apoptosis in cell cultures. J. Virol. 2000, 74:7619-7627.
42. Chiou P.P., Lina C.-M., Bols N.C., Chen T.T. Characterization of virus/double-stranded RNA-dependent induction of antimicrobial peptide hepcidin in trout macrophages. Dev. Comp. Immunol. 2007, 31:1297-1309.
43. Choi M.K., Moon C.H., Ko M.S., Lee U.-H., Cho W.J., Cha S.J., Do J.W., Heo G.J., Jeong S.G., Hahm Y.S., Harmache A., Bremont M., Kurath G., Park J.W. A nuclear localization of the infectious haematopoietic necrosis virus NV protein is necessary for optimal viral growth. PLoS One 2011, 6:22362.
44. Chilmonczyk S., Monge D. Flow cytometry as a tool for assessment of the fish cellular immune response to pathogens. Fish Shellfish Immunol. 1999, 9:319-333.
45. Clark H.F., Soriano E.Z. Fish rhabdovirus replication in non-piscine cell culture: new system for the study of rhabdovirus-cell interaction in which the virus and cell have different temperature optima. Infect. Immun. 1974, 10:180-188.
46. Collet B., Secombes C.J. The rainbow trout Mx1 promoter: structural and functional characterisation. Eur. J. Biochem. 2001, 286:1577-1584.
47. Collet B., Secombes C.J. Type I interferon signalling in fish. Fish Shellfish Immunol. 2002, 12:389-397.
48. Collet B., Hovens G.C.J., Mazzoni D., Hirono I., Aoki T., Secombes C.J. Cloning and expression analysis of rainbow trout Oncorhynchus mykiss interferon regulatory factor 1 and 2 (IRF-1 and IRF-2). Dev. Comp. Immunol. 2003, 27:111-126.
49. Collet B., Boudinot P., Benmansour A., Secombes C.J. A luciferase reporter system based on Mx1 promoter to study interferon pathways in rainbow trout. Dev. Comp. Immunol. 2004, 28:793-801.
50. Collet B., Munro E.S., Gahlawat S., Acosta F., Garcia J., Roemelt C., Zou J., Secombes C.J., Ellis A.E. Infectious pancreatic necrosis virus suppresses type i interferon signalling in rainbow trout gonad cell line but not in Atlantic salmon macrophages. Fish Shellfish Immunol. 2007, 22:44-56.
51. Collet B., Bain N., Prevost S., Besinque G., McBeath A., Snow M., Collins C. Atlantic salmon Salmo salar signal transducer and activator of transcription STAT-1: a contrasting kinetics of expression upon ISAV or IPNV infection. Fish Shellfish Immunol. 2008, 25:861-867.
52. Collet B., Ganne G., Bird S., Collins C. Isolation and expression profile of a gene encoding for the Signal Transducer and Activator of Transcription STAT-2 in Atlantic salmon (Salmo salar). Dev. Comp. Immunol. 2009, 33:821-829.
53. Collet B., Urquhart K., Noguera P., Larsen K., Lester K., Smail D., Bruno D. A method to measure an indicator of viraemia in Atlantic salmon using a reporter cell line. J. Virol. Methods 2013, 191:113-117.
54. Congleton J., Sun B. Interferon-like activity produced by anterior kidney leucocytes of rainbow trout stimulated in vitro by infectious hematopoietic necrosis virus or poly I:C. Dis. Aquat. Org. 1996, 25:185-195.
55. Crane M., Hyatt A. Viruses of fish: an overview of significant pathogens. Viruses 2011, 3:2025-2046.
56. Cuesta A., Tafalla C. Transcription of immune genes upon challenge with viral hemorrhagic septicaemia virus (VHSV) in DNA vaccinated rainbow trout (Oncorhynchus mykiss). Vaccine 2009, 27:280-289.
57. Cuesta, A., Meseguer, J., Esteban, M.A., 2011. Immunotoxicological effects of environmental contaminants. In: Stoytcheva, M. (Ed.), Teleost Fish Reared for Aquaculture, Pesticides in the Modern World - Risks and Benefits. pp 242-266.
58. Cummings K.L., Waggoner S.N., Tacke R., Hahn Y.S. Role of complement in immune regulation and its exploitation by virus. Viral Immunol. 2007, 20:505-524.
59. Dabo S., Meurs E.F. DsRNA-dependent protein kinase PKR and its role in stress, signaling and HCV infection. Viruses 2012, 4:2598-2635.
60. Danion M., LeFloch S., Castric J., Lamour F., Cabon J., Quentel C. Effect of chronic exposure to pendimethalin on the susceptibility of rainbow trout, Oncorhynchus mykiss L., to viral hemorrhagic septicaemia virus (VHSV). Ecotoxicol. Environ. Safety 2012, 79:28-34.
61. Das B.K., Collet B., Snow M., Ellis A.E. Expression of interferon type I and II, Mx and gIP genes in the kidney of Atlantic salmon, Salmo salar, is induced during smelting. Fish Shellfish Immunol. 2007, 23:514-520.
62. Das B.K., Nayak K.K., Fourrier M., Collet B., Snow M., Ellis A.E. Expression of Mx protein in tissues of Atlantic salmon post-smolts - an immunohistochemical study. Fish Shellfish Immunol. 2007, 23:1209-1217.
63. Das B.K., Ellis A.E., Collet B. Induction and persistence of Mx protein in tissues, blood and plasma of Atlantic salmon parr, Salmo salar, injected with poly I:C. Fish Shellfish Immunol. 2009, 26:40-48.
64. David M., Romeroll G., Zhang Z.-Y., Dixon J.E., Larner A.C. In Vitro activation of the transcription factor ISGFb3y interferon ar involves a membrane-associated tyrosine phosphatase and tyrosine kinase. J. Biol. Chem. 1993, 268:6593-6599.
65. de Kinkelin P., Dorson M. Interferon production in rainbow trout (Salmo gairdneri) experimentally infected with egtved virus. J. Gen. Virol. 1973, 19:125-127.
66. Desvignes L., Quentel C., Lamour F., le V.A. Pathogenesis and immune response in Atlantic salmon (Salmo salar L.) parr experimentally infected with salmon pancreas disease virus (SPDV). Fish Shellfish Immunol. 2002, 12:77-95.
67. de Weerd N.A., Samarajiwa S.A., Hertzog P.J. Type I interferon receptors: biochemistry and biological functions. J. Biol. Chem. 2007, 282:20053-20057.
68. Dorson M., Touchy C. The influence of fish age and water temperature on mortalities of rainbow trout, Salmo gairdneri Richardson, caused by a European strain of infectious pancreatic necrosis virus. J. Fish Dis. 1981, 4:213-221.
69. Eaton W.D. Anti-viral activity in four species of salmonids following exposure to poly inosinic:cytidylic acid. Dis. Aquat. Org. 1990, 9:193-198.
70. Einer-Jensen K., Delgado L., Lorenzen E., Bovo G., Evensen Ø., Lapatra S., Lorenzen N. Dual DNA vaccination of rainbow trout (Oncorhynchus mykiss) against two different rhabdoviruses, VHSV and IHNV, induces specific divalent protection. Vaccine 2009, 27:1248-1253.
71. Ellis A.E. Innate host defense mechanisms of fish against viruses and bacteria. Dev. Comp. Immunol. 2001, 25:827-839.
72. Ellis A.E., Cavaco A., Petrie A., Lockhart K., Snow M., Collet B. A sequential histopathological, immunocytochemical and quantitative RT-PCR analysis of Atlantic salmon post-smolts following infection with IPNV. J. Fish Dis. 2010, 33:803-818.
73. Esteban M.A. An overview of the immunological defenses in fish skin. ISRN Immunol. 2012, 853470.
74. Evans D.L., Jaso-Friedmann L. Nonspecific cytotoxic cells as effectors of immunity in fish. Ann. Rev. Fish Dis. 1992, 2:109-121.
75. Everett R.D., Chelbi-Alix M.K. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 2007, 89:819-830.
76. FAO yearbook. Fishery and Aquaculture Statistics, 2010.
77. Falco A., Mas V., Tafalla C., Perez L., Coll J.M., Estepa A. Dual antiviral activity of human alpha-defensin-1 against viral haemorrhagic septicaemia rhabdovirus (VHSV): inactivation of virus particles and induction of a type I interferon-related response. Antiviral Res. 2007, 76:111-123.
78. Falco A., Brocal I., Pérez L., Coll J.M., Estepa A., Tafalla C. In vivo modulation of the rainbow trout (Oncorhynchus mykiss) immune response by the human alpha defensin 1, HNP1. Fish Shellfish Immunol. 2008, 24:102-112.
79. Falco A., Chico V., Marroqui L., Perez L., Coll J.M., Estepa A. Expression and antiviral activity of a β-defensin-like peptide identified in the rainbow trout (Oncorhynchus mykiss) EST sequences. Mol. Immunol. 2008, 45:757-765.
80. Falco A., Ortega-Villaizan M., Chico V., Brocal I., Perez L., Coll J.M., Estepa A. Antimicrobial peptides as model molecules for the development of novel antiviral agents in aquaculture. Mini Rev. Med. Chem. 2009, 9:1159-1164.
81. Falk K., Press C.M., Landsverk T., Dannevig B.H. Spleen and kidney of Atlantic salmon (Salmo salar L.) show histochemical changes early in the course of experimentally induced infectious salmon anaemia (ISA). Vet. Immunol. Immunopathol. 1995, 49:115-126.
82. Fast M.D., Sims D.E., Burka J.F., Mustafa A., Ross N.W. Skin morphology and humoral non-specific defence parameters of mucus and plasma in rainbow trout, coho and Atlantic salmon. Comp. Biochem. Physiol. A 2002, 132:645-657.
83. Favoreel H.W., Van de Walle G.R., Nauwynck H.J., Pensaert M.B. Virus complement evasion strategies. J. Gen. Virol. 2003, 84:1-15.
84. Forlenza M., Fink I.R., Raes G., Wiegertjes G.F. Heterogeneity of macrophage activation in fish. Dev. Comp. Immunol. 2011, 35:1246-1255.
85. Fitzgerald K.A. The interferon inducible gene: viperin. J. Interferon Cytokine Res. 2011, 31:131-135.
86. Fourrier M.C.F., Arnold M.F.F., Collet B., Munro E.S. The effect of sub-culturing on the basal level of type I interferon (IFN) gene expression in the Salmon Head Kidney (SHK-1) cell line. Fish Shellfish Immunol. 2009, 27:535-538.
87. Fu X.Y., Kessler D.S., Veals S.A., Levy D.E., Darnell J.E. ISGF3, the transcriptional activator induced by interferon a, consists of multiple interacting polypeptide chains. Proc. Natl. Acad. Sci. USA 1990, 87:8555-8559.
88. Fujiki K., Gauley J., Bols N.C., Dixon B. Genomic cloning of novel isotypes of the rainbow trout interleukin-8. Immunogenetics 2003, 55:126-131.
89. Gadan K., Marjara I.S., Sundh H., Sundell K., Evensen Ø. Slow release cortisol implants result in impaired innate immune responses and higher infection prevalence following experimental challenge with infectious pancreatic necrosis virus in Atlantic salmon (Salmo salar) parr. Fish Shellfish Immunol. 2012, 32:637-644.
90. Gadan K., Sandtrø A., Marjara I.S., Santi N., Munang'andu H.M., Evensen O. Stress-induced reversion to virulence of infectious pancreatic necrosis virus in naïve fry of Atlantic salmon (Salmo salar L.). PLoS One 2013, 8:54656.
91. García-Rosadoa E., Markussen T., Kileng O., Baekkevold E.S., Robertsen B., Mjaalanda S., Rimstad E. Molecular and functional characterization of two infectious salmon anaemia virus (ISAV) proteins with type I interferon antagonizing activity. Virus Res. 2008, 133:228-238.
92. Gerwick L., Steinhauer R., Lapatra S., Sandell T., Ortuno J., Hajiseyedjavadi N., Bayne C.J. The acute phase response of rainbow trout (Oncorhynchus mykiss) plasma proteins to viral, bacterial and fungal inflammatory agents. Fish Shellfish Immunol. 2002, 12:229-242.
93. Gombart A.F. The vitamin D-antimicrobial peptide pathway and its role in protection against infection. Fut. Microbiol. 2009, 4:1151.
94. Goodbourn S., Didcock L., Randall R.E. Interferons: cell signalling, immune modulation, antiviral responses and virus countermeasures. J. Gen. Virol. 2000, 81:2341-2364.
95. Gordon S. The macrophage: past, present and future. Eur. J. Immunol. 2007, 37:9-17.
96. Gordon S., Taylor P.R. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 2005, 5:953-964.
97. Gordon Y.J., Romanowski E.G., McDermott A.M. A review of antimicrobial peptides and their therapeutic potential as anti-infective drugs. Curr. Eye Res. 2005, 30:505-515.
98. Grove S., Austbø L., Hodneland K., Frost P., Løvoll M., McLoughlin M., Thim H.L., Braaen S., König M., Syed M., Jørgensen J.B., Rimstad E. Immune parameters correlating with reduced susceptibility to pancreas disease in experimentally challenged Atlantic salmon (Salmo salar). Fish Shellfish Immunol. 2013, 34:789-798.
99. Guarda G., Braun M., Staehli F., Tardivel A., Mattmann C., Förster I., Farlik M., Decker T., Du Pasquier R.A., Romero P., Tschopp J. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 2011, 34:213-223.
100. Gupta K., Cooper C. A review of the role of CpG oligodeoxynucleotides as toll-like receptor 9 agonists in prophylactic and therapeutic vaccine development in infectious diseases. Drugs R&D 2008, 9:137-145.
101. Haller O., Kochs G., Weber F. Interferon, Mx, and viral countermeasures. Cytokine Growth Fact. Rev. 2007, 18:425-433.
102. Harmache A., LeBerre M., Droineau S., Giovannini M., Bremont M. Bioluminescence imaging of live infected salmonids reveals that the fin bases are the major portal of entry for novirhabdovirus. J. Virol. 2006, 80:3655-3659.
103. Harper C., Wolf J.C. Morphologic effects of the stress response in fish. ILAR J. 2009, 50:387-396.
104. Hart S., Wrathmell A.B., Harris J.E., Grayson T.H. Gut immunology in fish: a review. Dev. Comp. Immunol. 1988, 12:453-480.
105. Haugarvoll E., Bjerkås I., Nowak B.F., Hordvik I., Koppang E.O. Identification and characterization of a novel intraepithelial lymphoid tissue in the gills of Atlantic salmon. J. Anat. 2008, 213:202-209.
106. Herath T.K., Bron J.E., Thompson K.D., Taggart J.B., Adams A., Ireland J.H., Richards R.H. Transcriptomic analysis of the host response to early stage salmonid alphavirus (SAV-1) infection in Atlantic salmon Salmo salar L. Fish Shellfish Immunol. 2012, 32:796-807.
107. Hirsch R.L. The complement system: its importance in the host response to viral infection. Microbiol. Rev. 1982, 46:71-85.
108. Hjalmarsson A., Everitt E. Identification of IPNV-specified components released from productively infected RTG-2 cells following massive cytopathic effect. Arch. Virol. 1999, 144:1487-1501.
109. Holland M.C.H., Lambris J.D. The complement system in teleosts. Fish Shellfish Immunol. 2002, 12:399-420.
110. Holland J.H., Bird S., Williamson B., Woudstra E., Akhlaghi M., Wang T., Zou J., Blaney S.C., Collet B., Secombes C.J. Molecular characterization of IRF3 and IRF7 in rainbow trout, Oncorhynchus mykiss: functional analysis and transcriptional modulation. Mol. Immunol. 2008, 46:269-285.
111. Holland J.W., Karim A., Wang T., Alnabulsi A., Collet B., Mughal M.S., Secombes C.J., Bird S. Molecular cloning and characterization of interferon regulatory factors 4 and 8 (IRF-4 and IRF-8) in rainbow trout, Oncorhynchus mykiss. Fish Shellfish Immunol. 2010, 29:157-166.
112. Honda K., Taniguchi T. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 2006, 6:644-658.
113. Hong J.R., Gong H.-Y., Wu J.-L. IPNV VP5, a novel anti-apoptosis gene of the Bcl-2 family, regulates Mcl-1 and viral protein expression. Virology 2002, 295:217-229.
114. Hong J.R., Wu J.L. Induction of apoptotic death in cells via Bad gene expression by infectious pancreatic necrosis virus infection. Cell Death Differ. 2002, 9:113-124.
115. Hong J.R., Lin T.L., Hsu Y.L., Wu J.L. Apoptosis precedes necrosis of fish cell line with infectious pancreatic necrosis virus infection. Virology 1998, 250:76-84.
116. Hong J.R., Hsu Y.L., Wu J.L. Infectious pancreatic necrosis virus induces apoptosis due to down-regulation of survival factor MCL-1 protein expression in a fish cell line. Virus Res. 1999, 63:75-83.
117. Husain M., Bird S., van Zwieten R., Secombes C.J., Wang T. Cloning of the IL-1b3 gene and IL-1b4 pseudogene in salmonids uncovers a second type of IL-1b gene in teleost fish. Dev. Comp. Immunol. 2012, 38:431-446.
118. Hussell T., Goulding J. Structured regulation of inflammation during respiratory viral infection. Lancet Infect. Dis. 2010, 10:360-366.
119. Ingerslev H.C., Rønneseth A., Pettersen E.F., Wergeland H.I. Differential expression of immune genes in Atlantic salmon (Salmo salar L.) challenged intraperitoneally or by cohabitation with IPNV. Scand. J. Immunol. 2009, 69:90-98.
120. Ingram G.I. Substances involved in the natural resistance of fish to infection - a review. J. Fish Biol. 1980, 16:23-60.
121. Iliev D.B., Skjæveland I., Jørgensen J.B. CpG oligonucleotides bind TLR9 and RRM-containing proteins in Atlantic Salmon (Salmo salar). BMC Immunol. 2013, 14:12.
122. Iliev D.B., Sobhkhez M., Fremmerlid K., Jørgensen J.B. MyD88 interacts with interferon regulatory factor (IRF) 3 and IRF7 in Atlantic salmon (Salmo salar): transgenic SsMyD88 modulates the IRF-induced type I interferon response and accumulates in aggresomes. J. Biol. Chem. 2011, 286:42715-42724.
123. Jensen S., Thomsen A.R. Sensing of RNA viruses: a review of innate immune receptors involved in recognizing RNA virus invasion. J. Virol. 2012, 86:2900-2910.
124. Johansson P., Corripio-Miyar Y., Wang T., Collet B., Secombes C.J., Zou J. Characterisation and expression analysis of the rainbow trout (Oncorhynchusmykiss) homologue of the human dendritic cell marker CD208/lysosomal associated membrane protein 3. Dev. Comp. Immunol. 2012, 37:402-413.
125. Jørgensen J.B., Johansen L.-H., Steiro K., Johansen A. CpG DNA induces protective antiviral immune responses in Atlantic salmon (Salmo salar L.). J. Virol. 2003, 77:11471-11479.
126. Jørgensen J.B., Johansen A., Hegseth M.N., Zou J., Robertsen B., Collet B., Secombes C.J. A recombinant CHSE-214 cell line expressing an Mx1 promoter-reporter system responds to both interferon type I and type II from salmonids and represents a versatile tool to study the IFN-system in teleost fish. Fish Shellfish Immunol. 2007, 23:1294-1303.
127. Jørgensen S.M., Hetland D.L., Press C.M., Grimholt U., Gjøen T. Effect of early infectious salmon anaemia virus (ISAV) infection on expression of MHC pathway genes and type I and II interferon in Atlantic salmon (Salmo salar L.) tissues. Fish Shellfish Immunol. 2007, 23:576-588.
128. Jørgensen S.M., Afanasyev S., Krasnov A. Gene expression analyses in Atlantic salmon challenged with infectious salmon anaemia virus reveal differences between individuals with early, intermediate and late mortality. BMC Genomics 2008, 9:179.
129. Jørgensen H.B., Sørensen P., Cooper G.A., Lorenzen E., Lorenzen N., Hansen M.H., Koop B.F., Henryon M. General and family-specific gene expression responses to viral hemorrhagic septicaemia virus infection in rainbow trout (Oncorhynchus mykiss). Mol. Immunol. 2011, 48:1046-1058.
130. Joseph T., Cepica A., Brown L., Ikede B.O., Kibenge F.S.B. Mechanism of cell death during infectious salmon anemia virus infection is cell type-specific. J. Gen. Virol. 2004, 85:3027-3036.
131. Hamming O.J., Lutfalla G., Levraud J.-P., Hartmann R. Crystal structure of zebrafish interferons I and II reveals conservation of type I interferon structure in vertebrates. J. Virol. 2011, 85:8181-8187.
132. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., Ishii K.J., Yamaguchi O., Otsu K., Tsujimura T., Koh C.-S., Reis e Sousa C., Matsuura Y., Fujita T., Akira S. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441:101-105.
133. Kawai T., Akira S. Innate immune recognition of viral infection. Nat. Immunol. 2006, 7:131-137.
134. Kessler D.S., Levy D.E., Darnell J.E. Two interferon-induced nuclear factors bind a single promoter element in interferon-stimulated genes. Proc. Natl. Acad. Sci. USA 1988, 85:8521-8525.
135. Kessler D.S., Veals S.A., Fu X.-Y., Levy D.E. Interferon-alpha regulates nuclear translocation and DNA-binding affinity of ISGF3, a multimeric transcriptional activator. Gene Dev. 1990, 4:1753-1765.
136. Kibenge M.J.T., Munir K., Kibenge F.S.B. Constitutive expression of Atlantic salmon Mx1 protein in CHSE-214 cells confers resistance to Infectious Salmon Anaemia virus. Virol. J. 2005, 2:75.
137. Kileng Ø., Brundtland M.I., Robertsen B. Infectious salmon anaemia virus is a powerful inducer of key genes of the type I interferon system of Atlantic salmon, but is not inhibited by interferon. Fish Shellfish Immunol. 2007, 23:378-389.
138. Kim C.H., Johnson M.C., Drennan J.D., Simon B.E., Thomann E., Leong J.A. DNA vaccines encoding viral glycoproteins induce nonspecific immunity and Mx protein synthesis in fish. J. Virol. 2000, 74:7048-7054.
139. Kochs G., García-Sastre A., Martínez-Sobrido L. Multiple anti-interferon actions of the influenza A virus NS1 protein. J. Virol. 2007, 81:7011-7021.
140. Koppang E.O., Fischer U., Moore L., Tranulis M.A., Dijkstra J.M., Köllner B., Aune L., Jirillo E., Hordvik I. Salmonid T cells assemble in the thymus, spleen and in novel interbranchial lymphoid tissue. J. Anat. 2010, 217:728-739.
141. Koyama S., Ishii K.J., Coban C., Akira S. Innate immune response to viral infection. Cytokine 2008, 43:336-341.
142. Kumar V., Sharma A. Neutrophils: Cinderella of innate immune system. Int. Immunopharmacol. 2010, 10:1325-1334.
143. Kvamme B.O., Gadan K., Finne-Fridell F., Niklasson L., Sundh H., Sundell K., Taranger G.L., Evensen Ø. Modulation of innate immune responses in Atlantic salmon by chronic hypoxia-induced stress. Fish Shellfish Immunol. 2013, 34:55-65.
144. Lachmann P.J., Davies A. Complement and immunity to viruses. Immunol. Rev. 1997, 159:69-77.
145. Laing K., Secombes C.J. Chemokines. Dev. Comp. Immunol. 2004, 28:443-460.
146. Laing K.J., Zou J.J., Wang T., Bols N., Hirono I., Aoki I., Secombes C.J. Identification and analysis of an interleukin-8 like molecule in rainbow trout Oncorhynchus mykiss. Dev. Comp. Immunol. 2002, 23:433-444.
147. Larsen R., Rokenes T.P., Robertsen B. Inhibition of infectious pancreatic necrosis virus replication by Atlantic salmon Mx1 protein. J. Virol. 2004, 78:7938-7944.
148. Lauksund S., Svingerud T., Bergan V., Robertsen B. Atlantic salmon IPS-1 mediates induction of IFNa1 and activation of NF-kappaB and localizes to mitochondria. Dev. Comp. Immunol. 2009, 33:1196-1204.
149. Leong J.C., Trobridge G.D., Kim C.H., Johnson M., Simon B. Interferon-inducible Mx proteins in fish. Immunol. Rev. 1998, 166:349-363.
150. Leong J.S., Jantzen S.G., von Schalburg K.R., Cooper G.A., Messmer A.M., Liao N.Y., Munro S., Moore R., Holt R.A., Jones S.J., Davidson W.S., Koop B.F. Salmo salar and Esox lucius full-length cDNA sequences reveal changes in evolutionary pressures on a post-tetraploidization genome. BMC Genomics 2010, 11:279.
151. LeBlanc F., Laflamme M., Gagné N. Genetic markers of the immune response of Atlantic salmon (Salmo salar) to infectious salmon anaemia virus (ISAV). Fish Shellfish Immunol. 2010, 29:217-232.
152. LeBlanc F., Arseneau J.R., Leadbeater S., Glebe B., Laflamme M., Gagné N. Transcriptional response of Atlantic salmon (Salmo salar) after primary versus secondary exposure to infectious salmon anaemia virus (ISAV). Mol. Immunol. 2012, 51:197-209.
153. Lee S.-H., Vidal S.M. Functional diversity of Mx proteins: variations on a theme of host resistance to infection. Genome Res. 2002, 12:527-530.
154. Lenschow D.J. Antiviral properties of ISG15. Viruses 2010, 2:2154-2168.
155. Lester K., Urquhart K., Hall M., Gahlawat S., Collet B. Development of an in vitro system to measure the sensitivity to the antiviral Mx protein of fish viruses. J. Virol. Methods 2012, 182:1-8.
156. Levraud J.-P., Boudinot P., Colin I., Benmansour A., Peyrieras N., Herbomel P., Lutfalla G. Identification of the Zebrafish IFN receptor: implications for the origin of the vertebrate IFN system. J. Immunol. 2007, 178:4385-4394.
157. Liu Y.-J. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 2005, 23:275-306.
158. Liu G., Yang H. Modulation of macrophage activation and programming in immunity. J. Cell Physiol. 2013, 228:502-512.
159. Lockhart K., McBeath A.J.A., Collet B., Snow M., Ellis A.E. Expression of Mx mRNA following infection with IPNV is greater in IPN-susceptible Atlantic salmon post-smolts than in IPN-resistant Atlantic salmon parr. Fish Shellfish Immunol. 2007, 22:151-156.
160. Lorenzen N., Olesen N.J., Koch C. Immunity to VHS virus in rainbow trout. Aquaculture 1999, 172:41-61.
161. Lorenzen N., Lorenzen E., Einer-Jensen K., LaPatra S.E. DNA vaccines as a tool for analysing the protective immune response against rhabdoviruses in rainbow trout. Fish Shellfish Immunol. 2002, 12:439-453.
162. Lorenzen E., Einer-Jensen K., Rasmussen J.S., Kjaer T.E., Collet B., Secombes C.J., Lorenzen N. The protective mechanisms induced by a fish rhabdovirus DNA vaccine depend on temperature. Vaccine 2009, 27:3870-3880.
163. Lovy J., Savidant G.P., Speare D.J., Wright G.M. Langerin/CD207 positive dendritic like cells in the haemopoietic tissues of salmonids. Fish Shellfish Immunol. 2009, 27:365-368.
164. MacKenzie S., Balasch J.C., Novoa B., Ribas L., Roher N., Krasnov A., Figueras A. Comparative analysis of the acute response of the trout, O. mykiss, head kidney to in vivo challenge with virulent and attenuated infectious hematopoietic necrosis virus and LPS-induced inflammation. BMC Genomics 2008, 9:141.
165. Martin S.A.M., Taggart J.B., Seear P., Bron J.E., Talbot R., Teale A.J., Sweeney G.E., Høyheim B., Houlihan D.F., Tocher D.R., Zou J., Secombes C.J. Interferon type I and type II responses in an Atlantic salmon (Salmo salar) SHK-1 cell line by the salmon TRAITS/SGP microarray. Physiol. Genomics 2007, 32:33-44.
166. Martinez-Alonso S., Martinez-Lopez A., Estepa A., Cuesta A., Tafalla C. The introduction of multi-copy CpG motifs into an antiviral DNA vaccine strongly up-regulates its immunogenicity in fish. Vaccine 2011, 29:1289-1296.
167. Martinez-Alonso S., Vakharia V.N., Saint-Jean S.R., Pérez-Prieto S., Tafalla C. Immune responses elicited in rainbow trout through the administration of infectious pancreatic necrosis virus-like particles. Dev. Comp. Immunol. 2012, 36:378-384.
168. Matejusova, I., Lester, K., Li, Z., Bravo, J., Bland, F., Collet, B., in press. Comparative genotypic and phenotypic analysis of two salmon pancreas disease virus (SPDV) isolates in salmonid cell lines. Arch. Virol.
169. McBeath A.J.A., Collet B., Paley R., Duraffour S., Aspehaug V., Biering E., Secombes C.J., Snow M. Identification of an interferon antagonist protein encoded by segment 7 of infectious salmon anaemia virus. Virus Res. 2006, 115:176-184.
170. McBeath A.J.A., Snow M., Secombes C.J., Ellis A.E., Collet B. Expression kinetics of interferon and interferon-induced genes in Atlantic salmon (Salmo salar) following infection with Infectious Pancreatic Necrosis Virus and Infectious Salmon Anaemia Virus. Fish Shellfish Immunol. 2007, 22:230-241.
171. McLauchlan P.E., Collet B., Ingerslev E., Secombes C.J., Lorenzen N., Ellis A.E. DNA vaccination against viral haemorrhagic septicaemia (VHS) in rainbow trout: size, dose, route of injection and duration of protection - early protection correlates with Mx expression. Fish Shellfish Immunol. 2003, 15:39-50.
172. Mikalsen A.B., Haugland O., Rode M., Solbakk I.T., Evensen O. Atlantic salmon reovirus infection causes a CD8 T cell myocarditis in Atlantic salmon (Salmo salar L.). PLoS One 2012, 7:37269.
173. Miller N., Wilson M., Bfufltén E., Stuge T., Warr G., Clem W. Functional and molecular characterization of teleost leukocytes. Immunol. Rev. 1998, 166:187-197.
174. Moneke E.E., Kibenge M.J.T., Groman D., Johnson G.R., Ikede B.O., Kibenge F.S.B. Experimentally infected with infectious salmon anemia virus infectious salmon anaemia virus RNA in fish cell cultures and in tissue sections of Atlantic salmon. J. Vet. Diagn. Invest. 2003, 15:407.
175. Montero J., Estepa A., Coll J., Tafalla C. Regulation of rainbow trout (Oncorhynchus mykiss) interleukin-8 receptor (IL-8R) gene transcription in response to viral hemorrhagic septicemia virus (VHSV), DNA vaccination and chemokines. Fish Shellfish Immunol. 2008, 25:271-280.
176. Montero J., Coll J., Sevilla N., Cuesta A., Bols N.C., Tafalla C. Interleukin 8 and CK-6 chemokines specifically attract rainbow trout (Oncorhynchus mykiss) RTS11 monocyte-macrophage cells and have variable effects on their immune functions. Dev. Comp. Immunol. 2008, 32:1374-1384.
177. Montero J., Chaves-Pozo E., Cuesta A., Tafalla C. Chemokine transcription in rainbow trout (Oncorhynchus mykiss) is differently modulated in response to viral hemorrhagic septicaemia virus (VHSV) or infectious pancreatic necrosis virus (IPNV). Fish Shellfish Immunol. 2009, 27:661-669.
178. Montero J., Garcia J., Ordas M.C., Casanova I., Gonzalez A., Villena A., Coll J., Tafalla C. Specific regulation of the chemokine response to viral hemorrhagic septicaemia virus at the entry site. J. Virol. 2011, 85:4046-4056.
179. Moody C.E., Serreze D.V., Reno P.W. Non-specific cytotoxicity activity of teleosts leukocytes. Dev. Comp. Immunol. 1985, 9:51-64.
180. Munro E.S., Gahlawat S.K., Acosta F., Ellis A.E. In infectious pancreatic necrosis virus carrier Atlantic salmon, Salmo salar L., post-smolts, almost all kidney macrophages ex vivo contain a low level of non-replicating virus. J. Fish Dis. 2006, 29:43-48.
181. Nagarajan U.M. Induction and function of IFNβ during viral and bacterial infection. Crit. Rev. Immunol. 2011, 31:459-474.
182. Nygaard R., Husgard S., Sommer A.I., Leong J.A., Robertsen B. Induction of Mx protein by interferon and double-stranded RNA in salmonid cells. Fish Shellfish Immunol. 2000, 10:435-450.
183. O'Brien V. Viruses and apoptosis. J. Gen. Virol. 1998, 79:1833-1845.
184. O'Farrell C., Vaghefi N., Cantonnet M., Buteau B., Boudinot P., Benmansour A. Survey of transcript expression in rainbow trout leukocytes reveals a major contribution of interferon-responsive genes in the early response to a rhabdovirus infection. J. Virol. 2002, 76:8040-8049.
185. Ohta H., Kai C., Yoshikawa Y., Yamanouchi K. Activation of chicken alternative complement pathway by fowlpox virus-infected cells. Infect. Immun. 1983, 42:721-727.
186. Ohta Y., Landis E., Boulay T., Phillips R.B., Collet B., Secombes C.J., Flajnik M.F., Hansen J.D. Homologs of CD83 from elasmobranch and teleost fish. J. Immunol. 2004, 173:4553-4560.
187. OIE Manual of Diagnostic Tests for Aquatic Animals 2012, Office International des Epizooties, Paris. sixth ed.
188. Onomoto K., Jogi M., Yoo J.-S., Narita R., Morimoto S., Takemura A., Sambhara S., Kawaguchi A., Osari S., Nagata K., Matsumiya T., Namiki H., Yoneyama M., Fujita T. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS One 2012, 7:43031.
189. Ooi E.L., Verjan N., Haraguchi I., Oshima T., Kondo H., Hirono I., Aoki T., Kiyono H., Yuki Y. Innate immunomodulation with recombinant interferon-alpha enhances resistance of rainbow trout (Oncorhynchus mykiss) to infectious hematopoietic necrosis virus. Dev. Comp. Immunol. 2008, 32:1211-1220.
190. Ordás M.C., Cuesta A., Mercado L., Bols N.C., Tafalla C. Viral hemorrhagic septicaemia virus (VHSV) up-regulates the cytotoxic activity and the perforin/granzyme pathway in the rainbow trout RTS11 cell line. Fish Shellfish Immunol. 2011, 31:252-259.
191. Ortega-Villaizan M., Chico V., Falco A., Perez L., Coll J.M., Estepa A. The rainbow trout TLR9 gene and its role in the immune responses elicited by a plasmid encoding the glycoprotein G of the viral haemorrhagic septicaemia rhabdovirus (VHSV). Mol. Immunol. 2009, 46:1710-1717.
192. Overturf K., LaPatra S. Quantitative expression (Walbaum) of immunological factors in rainbow trout, Oncorhynchus mykiss (Walbaum), after infection with either Flavobacterium psychrophilum, Aeromonas salmonicida, or infectious haematopoietic necrosis virus. J. Fish Dis. 2006, 29:215-224.
193. Ozato K., Shin D.-M., Chang T.-H., Morse H.-C. TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 2008, 8:849-860.
194. Palti Y., Gahr S.A., Purcell M.K., Hadidi S., Rexroad C.E., Wiens G.D. Identification, characterization and genetic mapping of TLR7, TLR8a1 and TLR8a2 genes in rainbow trout (Oncorhynchus mykiss). Dev. Comp. Immunol. 2010, 34:219-233.
195. Paulmann D., Magulski T., Schwarz R., Heitmann L., Flehmig B., Vallbracht A., Dotzauer A. Hepatitis A virus protein 2B suppresses beta interferon (IFN) gene transcription by interfering with IFN regulatory factor 3 activation. J. Gen. Virol. 2008, 89:1593-1604.
196. Peddie S., McLaughlan P., Ellis A.E., Secombes C.J. Effect of intraperitoneally administered IL1β-derived peptides on resistance to Viral Haemorrhagic Septicaemia in rainbow trout Oncorhynchus mykiss. Dis. Aquat. Org. 2003, 56:195-200.
197. Peñaranda M.M., Purcell M.K., Kurath G. Differential virulence mechanisms of infectious hematopoietic necrosis virus in rainbow trout (Oncorhynchus mykiss) include host entry and virus replication kinetics. J. Gen. Virol. 2009, 90:2172-2182.
198. Peñaranda M.M., Lapatra S.E., Kurath G. Specificity of DNA vaccines against the U and M genogroups of infectious hematopoietic necrosis virus (IHNV) in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 2011, 31:43-51.
199. Pestka S., Krause C.D., Walter M.R. Interferons, interferon-like cytokines, and their receptors. Immunol. Rev. 2004, 202:8-32.
200. Pindel A., Sadler A. The role of protein kinase R in the interferon response. J. Interferon Cytokine Res. 2011, 31:59-70.
201. Pirhonen J., Sareneva T., Kurimoto M., Julkunen I., Matikainen S. Virus infection activates IL-1b and IL-18 production in human macrophages by a caspase-1-dependent pathway. J. Immunol. 1999, 162:7322-7329.
202. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 2005, 5:375-386.
203. Pottinger T.G., Carrick T.R. Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. Gen. Comp. Endocrinol. 1999, 116:122-132.
204. Prechtel A.T., Steinkasserer A. CD83: an update on functions and prospects of the maturation marker of dendritic cells. Arch. Dermatol. Res. 2007, 299:59-69.
205. Purcell M.K., Kurath G., Garver K.A., Herwig R.P., Winton J.R. Quantitative expression profiling of immune response genes in rainbow trout following infectious haematopoietic necrosis virus (IHNV) infection or DNA vaccination. Fish Shellfish Immunol. 2004, 17:447-462.
206. Purcell M.K., Smith K.D., Hood L., Winton J.R., Roach J.C. Conservation of toll-like receptor signalling pathways in teleost fish. Comp. Biochem. Physiol. D Genomics Proteomics 2006, 1:77-88.
207. Purcell M.K., Garver K.A., Conway C., Elliott D.G., Kurath G. Infectious haematopoietic necrosis virus genogroup-specific virulence mechanisms in sockeye salmon, Oncorhynchus nerka (Walbaum), from Redfish Lake, Idaho. J. Fish Dis. 2009, 32:619-631.
208. Purcell M.K., Laing K.J., Woodson J.C., Thorgaard G.H., Hansen J.D. Characterization of the interferon genes in homozygous rainbow trout reveals two novel genes, alternate splicing and differential regulation of duplicated genes. Fish Shellfish Immunol. 2009, 26:293-304.
209. Purcell M.K., Lapatra S.E., Woodson J.C., Kurath G., Winton J.R. Early viral replication and induced or constitutive immunity in rainbow trout families with differential resistance to Infectious hematopoietic necrosis virus (IHNV). Fish Shellfish Immunol. 2010, 28:98-105.
210. Purcell M.K., Marjara I.S., Batts W., Kurath G., Hansen J.D. Transcriptome analysis of rainbow trout infected with high and low virulence strains of infectious hematopoietic necrosis virus. Fish Shellfish Immunol. 2010, 30:84-93.
211. Purcell M.K., Laing K.J., Winton J.R. Immunity to Fish Rhabdoviruses. Viruses 2012, 4:140-166.
212. Rajanbabu V., Chen J.Y. Applications of antimicrobial peptides from fish and perspectives for the future. Peptides 2011, 32:415-420.
213. Randall R.E., Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 2008, 89:1-47.
214. Rebl A., Goldammer T., Seyfert H.-M. Toll-like receptor signalling in bony fish. Vet. Immunol. Immunopathol. 2010, 134:139-150.
215. Reid A., Young K.M., Lumsden J.S. Rainbow trout Oncorhynchus mykiss ladderlectin, but not intelectin, binds viral hemorrhagic septicemia virus IVb. Dis. Aquat. Organ. 2011, 95:137-143.
216. Reintamm T., Kuusksalu A., Metsis M., Päri M., Vallmann K., Lopp A., Justesen J., Kelve M. Sponge OAS has a distinct genomic structure within the 2-5A synthetase family. Mol. Genet. Genomics 2008, 280:453-466.
217. Reite O.B., Evensen O. Inflammatory cells of teleostean fish: a review focusing on mast cells/eosinophilic granule cells and rodlet cells. Fish Shellfish Immunol. 2006, 20:192-208.
218. Renault T., Torchy C., de Kinkelin P. Spectrophotometric method for titration of trout interferon, and its application to rainbow trout fry experimentally infected with viral haemorrhagic septicaemia virus. Dis. Aquat. Org. 1991, 10:23-29.
219. Reyes-Cerpa S., Reyes-López F.E., Toro-Ascuy D., Ibañez J., Maisey K., Sandino A.M., Imarai M. IPNV modulation of pro and anti-inflammatory cytokine expression in Atlantic salmon might help the establishment of infection and persistence. Fish Shellfish Immunol. 2012, 32:291-300.
220. Rimstad E. Examples of emerging virus diseases in salmonid aquaculture. Aquat. Res. 2010, 42:86-89.
221. Robertsen B. Can we get the upper hand on viral diseases in aquaculture of Atlantic salmon?. Aqua. Res. 2011, 42:125-131.
222. Robertsen B. Expression of interferon and interferon-induced genes in salmonids in response to virus infection, interferon-inducing compounds and vaccination. Fish Shellfish Immunol. 2008, 25:351-357.
223. Robertsen B. The interferon system of teleost fish. Fish Shellfish Immunol. 2006, 20:172-191.
224. Robertsen B., Trobridge G., Leong J.A. Molecular cloning of double-stranded RNA inducible Mx genes from Atlantic salmon (Salmo salar L.). Dev. Comp. Immunol. 1997, 21:397-412.
225. Robertsen B., Bergan V., Røkenes T., Larsen R., Albuquerque A. Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J. Interferon Cytokine Res. 2003, 23:601-612.
226. Rodriguez M.F., Wiens G.D., Purcell M.K., Palti Y. Characterization of Toll-like receptor 3 gene in rainbow trout (Oncorhynchus mykiss). Immunogenetics 2005, 57:510-519.
227. Rogel-Gaillard C., Chilmonczyk S., de Kinkelin P. In vitro induction of interferon-like activity from rainbow trout leucocytes stimulated by Egtved virus. Fish Shellfish Immunol. 1993, 3:383-394.
228. Røkenes T.P., Larsen R., Robertsen B. Atlantic salmon ISG15: expression and conjugation to cellular proteins in response to interferon, double-stranded RNA and virus infections. Mol. Immunol. 2007, 44:950-959.
229. Romero A., Dios S., Bremont M., Figueras A., Novoa B. Interaction of the attenuated recombinant rIHNV-Gvhsv GFP virus with macrophages from rainbow trout (Oncorhynchus mykiss). Vet. Immunol. Immunopathol. 2011, 140:119-129.
230. Rønneseth A., Pettersen E.F., Wergeland H.I. Neutrophils and B-cells in blood and head kidney of Atlantic salmon (Salmo salar L.) challenged with infectious pancreatic necrosis virus (IPNV). Fish Shellfish Immunol. 2006, 20:610-620.
231. Roulston A., Marcellus R.C., Branton P.E. Virus and apoptosis. Annu. Rev. Microbiol. 1999, 53:577-628.
232. Saint-Jean S.R., Pérez-Prieto S.I. Interferon mediated antiviral activity against salmonid fish viruses in BF-2 and other cell lines. Vet. Immunol. Immunopathol. 2006, 110:1-10.
233. Saint-Jean R.S., de las Heras A.I., Pérez-Prieto S.I. The persistence of infectious pancreatic necrosis virus and its influence on the early immune response. Vet. Immunol. Immunopathol. 2010, 136:81-91.
234. Salinas I., Lockhart K., Bowden T.J., Collet B., Secombes C.J., Ellis A.E. An assessment of immunostimulants as Mx inducers in Atlantic salmon (Salmo salar L.) parr. Effect of temperature on the kinetics of Mx responses. Fish Shellfish Immunol. 2004, 17:159-170.
235. Salaun B., de Saint-Vis B., Pacheco N., Pacheco Y., Riesler A., Isaac S., Leroux C., Clair-Moninot V., Pin J.-J., Griffith J., Treilleux I., Goddard S., Davoust J., Kleijmeer M., Lebecque S. CD208/dendritic cell-lysosomal associated membrane protein is a marker of normal and transformed type II pneumocytes. Am. J. Pathol. 2004, 164:861-871.
236. Salinas I., Zhang Y.A., Sunyer J.O. Mucosal immunoglobulins and B cells of teleost fish. Dev. Comp. Immunol. 2011, 35:1346-1365.
237. Sangrador-Vegas A., Lennington J.B., Smith T.J. Molecular cloning of an IL-8-like CXC chemokine and tissue factor in rainbow trout (Oncorhynchus mykiss) by use of suppression subtractive hybridization. Cytokine 2002, 17:66-70.
238. Santana P., Palacios C., Narváez E., Guzmán F., Gallardo J.A., Mercado L. Anti-peptide antibodies: a tool for detecting IL-8 in salmonids. Elect. J. Biotechnol. 2012, 15:15.
239. Sasaki Y., Maita M., Okamoto N. Rainbow trout neutrophils are responsible for non-specific cytotoxicity. Fish Shellfish Immunol. 2002, 12:243-252.
240. Schindler C., Levy D.E., Decker T. JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 2007, 282:20059-20063.
241. Schiøtz B.L., Jørgensen S.M., Rexroad C., Gjøena T., Krasnov A. Transcriptomic analysis of responses to infectious salmon anemia virus infection in macrophage-like cells. Virus Res. 2008, 136:65-74.
242. Schiøtz B.L., Bækkevold E.S., Poulsen L.C., Mjaaland S., Gjøen T. Analysis of host- and strain-dependent cell death responses during infectious salmon anemia virus infection in vitro. Virol. J. 2009, 6:91.
243. Schmeisser H., Mejido J., Balinsky C.A., Morrow A.N., Clark C.R., Zhao T., Zoon K.C. Identification of alpha interferon-induced genes associated with antiviral activity in daudi cells and characterization of IFIT3 as a novel antiviral gene. J. Virol. 2010, 84:10671-10680.
244. Schmid S., Mordstein M., Kochs G., García-Sastre A., tenOever B.R. Transcription factor redundancy ensures induction of the antiviral state. J. Biol. Chem. 2010, 285:42013-42022.
245. Seo J.Y., Yaneva R., Cresswell P. Viperin: a multifunctional, interferon-inducible protein that regulates virus replication. Cell Host Microbe 2011, 10:534-539.
246. Sepulcre M.O., Muñoz I., Roca F.J., López-Muñoz A., Mulero V. Molecular strategies used by fish pathogens to interfere with host-programmed cell death. Dev. Comp. Immunol. 2010, 34:603-610.
247. Shau H., Gupta R.K., Golub S.H. Identification of a natural killer enhancing factor (NKEF) from human erythroid cells. Cell. Immunol. 1993, 147:1-11.
248. Siegal F.P., Kadowaki N., Shodell M., Fitzgerald-Bocarsly P.A., Shah K., Ho S., Antonenko S., Liu Y.J. The nature of the principal type 1 interferon-producing cells in human blood. Science 1999, 284:1835-1837.
249. Silverman R.H. Synthetase and RNase L during the interferon antiviral response. J. Virol. 2007, 81:12720-12729.
250. Sissons J.G., Oldstone M.B., Schreiber R.D. Antibody-independent activation of the alternative complement pathway by measles virus-infected cells. PNAS 1980, 77:559-562.
251. Skaug B., Chen Z.J. Emerging role of ISG15 in antiviral immunity. Cell 2010, 143:187-190.
252. Skjaeveland I., Iliev D.B., Zou J., Jorgensen T., Jorgensen J.B. A TLR9 homolog that is up-regulated by IFN-gamma in Atlantic salmon (Salmo salar). Dev. Comp. Immunol. 2008, 32:603-607.
253. Skjesol A., Hansen T., Shi C.-Y., Thim H.L., Jørgensen J.B. Structural and functional studies of STAT1 from Atlantic salmon (Salmo salar). BMC Immunol. 2010, 11:17.
254. Skjesol A., Skjæveland I., Elnæs M., Timmerhaus G., Fredriksen B.N., Jørgensen S.M., Krasnov A., Jørgensen J.B. IPNV with high and low virulence: host immune responses and viral mutations during infection. Virol. J. 2011, 10:396.
255. Smail D.A., Munro A.L.S. Infectious pancreatic necrosis virus persistence in farmed Atlantic salmon (Salmo salar). Fish and Shellfish Pathology 1985, 277-288. Academic Press, New York, NY. A.E. Ellis (Ed.).
256. Smith V.J., Fernandes J.M.O. Non-specific antimicrobial proteins of the innate system. Fish Defences 2009, 241-275. Science Publishers, Enfield. G. Zaccone, J. Masseguer, A. García-Ayala, B.G. Kapoor (Eds.).
257. Smith V.J., Desbois A.P., Dyrynda E.A. Conventional and unconventional antimicrobials from fish, marine invertebrates and micro-algae. Mar. Drugs 2010, 8:1213-1262.
258. Staeheli P., Yu Y.X., Grob R., Haller O. A double-stranded RNA-inducible fish gene homologous to the murine influenza virus resistance gene Mx. Mol. Cell. Biol. 1989, 9:3117-3121.
259. Subramanian S., MacKinnon S.L., Ross N.W. A comparative study on innate immune parameters in the epidermal mucus of various fish species. Comp. Biochem. Physiol. B 2007, 148:256-263.
260. Sun B., Skjæveland I., Svingerud T., Zou J., Jørgensen J., Robertsen B. Antiviral activity of salmonid gamma interferon against infectious pancreatic necrosis virus and salmonid alphavirus and its dependency on type I interferon. J. Virol. 2011, 85:9188-9198.
261. Sun B., Robertsen B., Wang Z., Liu B. Identification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Dev. Comp. Immunol. 2009, 33:547-558.
262. Svingerud T., Solstad T., Sun B., Nyrud M.L.J., Kileng O., Greiner-Tollersrud L., Robertsen B. Atlantic salmon type I IFN subtypes show differences in antiviral activity and cell-dependent expression: evidence for high IFNb/IFNc-producing cells in fish lymphoid tissues. J. Immunol. 2012, 189:5912-5923.
263. Tafalla C., Coll J., Secombes C.J. Expression of genes related to the early immune response in rainbow trout (Oncorhynchus mykiss) after viral haemorrhagic septicaemia virus (VHSV) infection. Dev. Comp. Immunol. 2005, 29:615-626.
264. Tafalla C., Chico V., Perez L., Coll J.M., Estepa A. In vitro and in vivo differential expression of rainbow trout (Oncorhynchus mykiss) Mx isoforms in response to viral haemorrhagic septicaemia virus (VHSV) G gene, poly I:C and VHSV. Fish Shellfish Immunol. 2007, 23:210-221.
265. Tafalla C., Sanchez E., Lorenzen N., DeWitte-Orr S.J., Bols N.C. Effects of viral hemorrhagic septicaemia virus (VHSV) on the rainbow trout (Oncorhynchus mykiss) monocyte cell line RTS-11. Mol. Immunol. 2008, 45:1439-1448.
266. Takeuchi O., Akira S. Innate immunity to virus infection. Immunol. Rev. 2009, 227:75-86.
267. Taksdal T., Olsen A.B., Bjerkås I., Hjortaas M.J., Dannevig B.H., Graham D.A., McLoughlin M.F. Pancreas disease in farmed Atlantic salmon, Salmo salar L., and rainbow trout, Oncorhynchus mykiss(Walbaum), in Norway. J. Fish Dis. 2007, 30:545-558.
268. Tamura T., Yanai H., Savitsky D., Taniguchi T. The IRF family transcription factors in immunity and oncogenesis. Annu. Rev. Immunol. 2008, 26:535-584.
269. Teles M., Mackenzie S., Boltaña S., Callol A., Tort L. Gene expression and TNFalpha secretion profile in rainbow trout macrophages following exposures to immunotoxicological effects of environmental contaminants in teleost fish reared for aquaculture copper and bacterial lipopolysaccharide. Fish Shellfish Immunol. 2011, 30:340-346.
270. Timmerhaus G., Krasnov A., Nilsen P., Alarcon M., Afanasyev S., Rode M., Takle H., Jørgensen S.M. Transcriptome profiling of immune responses to cardiomyopathy syndrome (CMS) in Atlantic salmon. BMC Genomics 2011, 12:459.
271. Thomas C., Moraga I., Levin D., Krutzik P.O., Podoplelova Y., Trejo A., Lee C., Yarden G., Vleck E.S., Glenn J.S., Nolan G.P., Piehler J., Schreiber G., Garcia K.C. Structural linkage between ligand discrimination and receptor activation by type I interferons. Cell 2011, 146:621-632.
272. Tort L., Balasch J.C., MacKenzie S. Fish health challenge after stress. Indicators of immunocompetence. Contrib. Sci. 2004, 2:443-454.
273. Trinchieri G. Type I interferon: friend or foe?. J. Exp. Med. 2010, 207:2053-2063.
274. Trobridge G.D., Leong J.A. Characterization of a rainbow trout Mx gene. J. Interferon Cytokine Res. 1995, 15:691-702.
275. Trobridge G.D., Chiou P.P., Leong J.C. Cloning of the rainbow trout (Oncorhynchus mykiss) Mx2 and Mx3 cDNAs and characterization of trout Mx protein expression in salmon cells. J. Virol. 1997, 71:5304-5311.
276. Underhill D.M. Mini-review toll-like receptors: networking for success. Eur. J. Immunol. 2003, 33:1767-1775.
277. Utke K., Kock H., Schuetze H., Bergmann S.M., Lorenzen N., Einer-Jensen K., Köllner B., Dalmo R.A., Vesely T., Ototake M., Fischer U. Cell-mediated immune responses in rainbow trout after DNA immunization against the viral hemorrhagicsepticemia virus. Dev. Comp. Immunol. 2008, 32:239-252.
278. Van Compernolle S.E., Taylor R.J., Oswald-Richter K., Jiang J., Youree B.E., Bowie J.H., Tyler M.J., Conlon J.M., Wade D., Aiken C., Dermody T.S., KewalRamani V.N., Rollins-Smith L.A., Unutmaz D. Antimicrobial peptides from amphibian skin potently inhibit human immunodeficiency virus infection and transfer of virus from dendritic cells to T cells. J. Virol. 2005, 79:11598-11606.
279. van der Aa L.M., Chadzinska M., Tijhaar E., Boudinot P., Verburg-van Kemenade B.M.L. CXCL8 chemokines in teleost fish: two lineages with distinct expression profiles during early phases of inflammation. PLoS One 2010, 5:e12384.
280. van der Aa L.M., Levraud J.P., Yahmi M., Lauret E., Briolat V., Herbomel P., Benmansour A., Boudinot P. A large new subset of TRIM genes highly diversified by duplication and positive selection in teleost fish. BMC Biol. 2009, 7:7.
281. Verjan N., Ooi E.L., Nochi T., Kondo H., Hirono I., Aoki T., Kiyono H., Yuki Y. A soluble non-glycosylated recombinant infectious hematopoietic necrosis virus (IHNV) G-protein induces IFNs in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 2008, 25:170-180.
282. Verrier E.R., Langevin C., Tohry C., Houel A., Ducrocq V., Benmansour A., Quillet E., Boudinot P. Genetic resistance to rhabdovirus infection in teleost fish is paralleled to the derived cell resistance status. PLoS One 2012, 7:33935.
283. Waddell S.J., Popper S.J., Rubins K.H., Griffiths M.J., Brown P.O., Levin M., Relman D.A. Dissecting interferon-induced transcriptional programs in human peripheral. Blood Cells. PLoS One 2010, 5:9753.
284. Wang T., Ward M., Grabowski P., Secombes C.J. Molecular cloning, gene organization and expression of rainbow trout (Oncorhynchus mykiss) inducible nitric oxide synthase (iNOS) gene. Biochem. J. 2001, 358:747-755.
285. Wargo A.R., Kell A.M., Scott R.J., Thorgaard G.H., Kurath G. Analysis of host genetic diversity and viral entry as sources of between-host variation in viral load. Virus Res. 2012, 165:71-80.
286. Weli S.C., Aamelfot M., Dale O.B., Koppang E.O., Falk K. Infectious salmon anaemia virus infection of Atlantic salmon gill epithelial cells. Virol. J. 2013, 10:5.
287. Workenhe S.T., Wadowska D.W., Wright G.M., Kibenge M.J.T., Kibenge F.S.B. Demonstration of infectious salmon anaemia virus (ISAV) endocytosis in erythrocytes of Atlantic salmon. Virol. J. 2007, 4:13.
288. Workenhe S.T., Kibenge M.J., Wright G.M., Wadowska D.W., Groman D.B., Kibenge F.S. Infectious salmon anaemia virus replication and induction of alpha interferon in Atlantic salmon erythrocytes. Virol. J. 2008, 5:36.
289. Workenhe S.T., Hori T.S., Rise M.L., Kibenge M.J., Kibenge F.S. Infectious salmon anaemia virus (ISAV) isolates induce distinct gene expression responses in the Atlantic salmon (Salmo salar) macrophage/dendritic-like cell line TO, assessed using genomic techniques. Mol. Immunol. 2009, 46:2955-2974.
290. Xagorari A., Chlichlia K. Toll-like receptors and viruses: induction of innate antiviral immune responses. Open Microbiol. J. 2008, 2:49-59.
291. Xu C., Guo T.-C., Mutoloki S., Haugland O., Marjara I.S., Evensen O. Alpha interferon and not gamma interferon inhibits salmonid alphavirus subtype 3 replication in vitro. J. Virol. 2010, 84:8903-8912.
292. Xu C., Guo T.-C., Mutoloki S., Haugland O., Evensen O. Gene expression studies of host response to Salmonid alphavirus subtype 3 experimental infections in Atlantic salmon. Vet. Res. 2012, 43:78.
293. Yano T. The nonspecific immune system: humoral defense. The Fish Immune System: Organism, Pathogen, and Environment 1996, 105-157. Academic Press, San Diego. G. Iwama, T. Nakanishi (Eds.).
294. Yoshinaga K., Okamoto N., Kurata O., Ikeda Y. Individual variation of natural killer activity of rainbow trout leukocytes against IPN-virus infected and uninfected RTG-2 cells. Fish Pathol. 1994, 29:1-4.
295. Zhang H., Evenhuis J.P., Thorgaard G.H., Ristow S.S. Cloning, characterization and genomic structure of the natural killer cell enhancement factor (NKEF)-like gene from homozygous clones of rainbow trout (Oncorhynchus mykiss). Dev. Comp. Immunol. 2001, 25:25-35.
296. Zhang Y.-A., Salinas I., Li J., Parra D., Bjork S., Xu Z., LaPatra S.E., Bartholomew J., Sunyer J.O. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 2010, 11:827-835.
297. Zhang Y.B., Gui J.F. Molecular regulation of interferon antiviral response in fish. Dev. Comp. Immunol. 2012, 38:193-202.
298. Zhao C., Denison C., Huibregtse J.M., Gygi S., Krug R.M. Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. PNAS 2005, 102:10200-10205.
299. Zou J., Tafalla C., Truckle J., Secombes C.J. Light on IFN evolution in vertebrates. J. Immunol. 2007, 179:3859-3871.
300. De Zoysa M., Kang H.S., Song Y.B., Jee Y., Lee Y.D., Lee J. First report of invertebrate Mx: cloning, characterization and expression analysis of Mx cDNA in disk abalone (Haliotis discus discus). Fish Shellfish Immunol. 2007, 23:86-96.