Interferon-mediated host response in experimentally induced salmonid alphavirus 1 infection in Atlantic salmon (Salmo salar L.)

Veterinary Immunology and Immunopathology

Volumn 155, Issue 1-2, 2013, Pages 9-20

  Herath, Tharangani K ^a   Thompson, Kim D ^a   Adams, Alexandra ^a   Richards, Randolph H ^a  

^a UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

Atlantic salmon; Immunohistochemistry; Interferon I; Mx protein; QRT PCR; Salmonid alphavirus

Indexed keywords

GAMMA INTERFERON; MYXOVIRUS RESISTANCE PROTEIN;

ALPHA VIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ATLANTIC SALMON; CONTROLLED STUDY; ENDOCARDIUM; EPICARDIUM; EXPERIMENTAL INFECTION; FIBROSIS; FISH DISEASE; HEART; HEART MUSCLE; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; KIDNEY PARENCHYMA; MUCOSA; NONHUMAN; PANCREAS; PROTECTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONID; SALMONID ALPHAVIRUS 1 INFECTION; TARGET ORGAN; TISSUE CULTURE; VIRUS INFECTION;

ALPHAVIRUS; SALMO SALAR; SALMONIDAE;

ATLANTIC SALMON; IMMUNOHISTOCHEMISTRY; INTERFERON I; MX PROTEIN; QRT-PCR; SALMONID ALPHAVIRUS;

ALPHAVIRUS; ALPHAVIRUS INFECTIONS; ANIMALS; FISH DISEASES; FISH PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNOHISTOCHEMISTRY; INTERFERON TYPE I; INTERFERON-GAMMA; INTERFERONS; MYXOVIRUS RESISTANCE PROTEINS; SALMO SALAR;

EID: 84881022908     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2013.05.011     Document Type: Article

References (50)

1. Abbas A.K., Lichtman A.H., Pober J.S. Cellular and Molecular Immunology 2000, W.B Saunders Company, United States of America. 4th edition.
2. Andersen L., Bratland A., Hodneland K., Nylund A. Tissue tropism of salmonid alphaviruses (subtypes SAV1 and SAV3) in experimentally challenged Atlantic salmon (Salmo salar L.). Arch. Virol 2007, 152:1871-1883.
3. Boucher P., Raynard R.S., Houghton G., Laurencin F.B. Comparative experimental transmission of pancreas disease in Atlantic salmon, rainbow trout and brown trout. Dis. Aquat. Organ. 1995, 22(19-24).
4. Boucher P., Laurencin F.B. Sleeping disease and pancreas disease: comparative histopathology and acquired cross-protection. J. Fish Dis. 1996, 19:303-310.
5. Buckley C.D., Pilling D., Lord J.M., Akbar A.N., Scheel-Toellner D., Salmon M. Fibroblasts regulate the switch from acute resolving to chronic persistent inflammation. Trends Immunol. 2001, 22:199-204.
6. Christie K.E., Graham D.A., McLoughlin M.F., Villoing S., Todd D., Knappskog D. Experimental infection of Atlantic salmon Salmo salar pre-smolts by i.p. injection with new Irish and Norwegian salmonid alphavirus (SAV) isolates: a comparative study. Dis. Aquat. Organ. 2007, 75:13-22.
7. 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.
8. Desvignes L., Quentel C., Lamour F., Le Ven 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.
9. Ferguson H.W., Roberts R.J., Richards R.H., Collins R.O., Rice D.A. Severe degenerative cardiomyopathy associated with pancreas disease in Atlantic salmon, Salmo salar L. J. Fish Dis. 1986, 9:95-98.
10. Fischer U., Utke K., Somamoto T., Kollner B., Ototake M., Nakanishi T. Cytotoxic activities of fish leucocytes. Fish Shellfish Immunol. 2006, 20:209-226.
11. Gahlawat S.K., Ellis A.E., Collet B. Expression of interferon and interferon-induced genes in Atlantic salmon Salmo salar cell lines SHK-1 and TO following infection with salmon alphavirus SAV. Fish Shellfish Immunol. 2009, 26:672-675.
12. Graham D.A., McLaughlin K., Rowley H.M., Gabestad I., Gordon A., McLoughlin M.F. A comparative study of marine salmonid alphavirus subtypes 1-6 using an experimental cohabitation challenge model. J. Fish Dis. 2011, 34:273-286.
13. Haller O., Stertz S., Kochs G. The Mx GTPase family of interferon-induced antiviral proteins. Microbes Infect. 2007, 9:1636-1643.
14. Haller O., Staeheli P., Kochs G. Interferon-induced Mx proteins in antiviral host defense. Biochimie 2007, 89:812-818.
15. Helenius A. Alphavirus and flavivirus glycoproteins - structures and functions. Cell 1995, 81:651-653.
16. Herath T., Bron J.E., Thompson K.D., Taggart J.B., Adams A., 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.
17. Jensen I., Albuqueque A., Sommer A.I., Robertsen B. Effect of poly I:C on the expression of Mx proteins and resistance against infection by infectious salmon anaemia virus in Atlantic salmon. Fish Shellfish Immunol. 2002, 13:311-326.
18. Jensen I., Robertsen B. The effect of interferon and Mx protein on infection of Atlantic salmon cells by infectious salmon anaemia virus (ISAV). Dev. Comp. Immunol. 2000, 24:S3-S4.
19. Karlsen M., Hodneland K., Endresen C., Nylund A. Genetic stability within the Norwegian subtype of salmonid alphavirus (family Togaviridae). Arch. Virol 2006, 151:861-874.
20. Kongtorp R.T., Taksdal T., Lyngoy A. Pathology of heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon Salmo salar. Dis. Aquat. Organ. 2004, 59:217-224.
21. Kongtorp R.T., Kjerstad A., Taksdal T., Guttvik A., Falk K. Heart and skeletal muscle inflammation in Atlantic salmon, Salmo salar L.: a new infectious disease. J. Fish Dis. 2004, 27:351-358.
22. Landis H., Simon-Jodicke A., Kloti A., Di Paolo C., Schnorr J., Schneider-Schaulies S., Hefti P., Pavlovic J. Human MxA protein confers resistance to Simliki forest virus and inhibits the amplification of a Simliki forest virus-based replication in the absence of viral structural protein. J. Virol. 1998, 72:1516-1522.
23. Lee S., Vidal S.M. Functional diversity of Mx proteins: variations on a theme of host resistance to infection. Genome Res. 2002, 12:527-530.
24. Leong J.C., Torbridge G.D., Kim C.H., Johnson M., Simon B. Interferon-inducible Mx proteins in fish. Immunol. Rev. 1998, 166:346-363.
25. MacKenzie S., Stertz S., Reichelt M., Krijnse-Locker J., MacKenzie J.C., Simpson O., Haller O., Kochs G. Interferon-induced, antiviral human MxA protein localizes to a distinct subcompartment of the smooth endoplasmic reticulum. J. Interferon Cytokine Res. 2006, 25:650-660.
26. McBeath A.J.A 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, 22:241-247.
27. McLoughlin M., Nelson R., McCormick J.I., Rowley H. Pathology of experimental pancreas disease in freshwater Atlantic salmon parr. J. Aquat. Anim. Health 1995, 7:104-110.
28. McLoughlin M.F., Nelson R.T., Rowley H.M., Cox D.I., Grant A.N. Experimental pancreas disease in Atlantic salmon Salmo salar post-smolts induced by salmon pancreas disease virus (SPDV). Dis. Aquat. Organ. 1996, 26:117-124.
29. McLoughlin M.F., Graham D.A. Alphavirus infections in salmonids - a review. J. Fish Dis. 2007, 30:511-531.
30. McVicar A.H. Pancreas disease of farmed Atlantic salmon, Salmo salar, in Scotland - epidemiology and early pathology. Aquaculture 1987, 67:71-78.
31. Nelson R.T., McLoughlin M.F., Rowley H.M., Platten M.A., Mccormick J.I. Isolation of a Toga-like virus from farmed Atlantic salmon Salmo salar with pancreas disease. Dis. Aquat. Organ. 1995, 22:25-32.
32. Plaff M.W. Quantification strategies in real-time PCR. A-Z Quantitative PCR. IUI Biotechnology Series 5 2004, 106-107. International University Line, La Jolla, CA. S.A. Bustin (Ed.).
33. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST (c)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002, 30:e36.
34. Pfaffl M.W., Tichopad A., Prgomet C., Neuvians TP Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol. Lett. 2004, 6(6):509-515.
35. Powers A.M., Brault A.C., Shirako Y., Strauss E.G., Kang W.L., Strauss J.H., Weaver S.C. Evolutionary relationships and systematics of the alphaviruses. J. Virol. 2001, 75:10118-10131.
36. Robertsen B., Bergan V., Rokenes T., Larsen R., Albuquerque A. Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J. Interferon Cytokine Res. 2003, 23:601-612.
37. Robertsen B. The interferon system of teleost fish. Fish Shellfish Immunol. 2006, 20:172-191.
38. 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.
39. Rodger H., Mitchell S. Epidemiological observations of pancreas disease of farmed Atlantic salmon, Salmo salar L., in Ireland. J. Fish Dis. 2007, 30:157-167.
40. Ryman K.D., Klimstra W.B. Host responses to alphavirus infection. Immunol. Rev. 2008, 225:27-45.
41. Schroder K., Hertzog P.J., Ravasi T., Hume D. Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 2004, 75:163-189.
42. Sen G.C. Viruses and interferons. Annu. Rev. Microbiol. 2001, 283:255-281.
43. Strandskog G., Villoing S., Iliev D.B., Thim H.L., Christie K.E., Jørgensen J.B. Formulations combining CpG containing oligonucleotides and poly I:C enhance the magnitude of immune responses and protection against pancreas disease in Atlantic salmon. Dev. Comp. Immunol. 2011, 35:1116-1127.
44. Taksdal T., Olsen A.B., Bjerkas 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.
45. Villoing S., Castric J., Jeffroy J., Le Ven A., Thiery R., Bremont M. An RT-PCR-based method for the diagnosis of the sleeping disease virus in experimentally and naturally infected salmonids. Dis. Aquat. Organ. 2000, 40:19-27.
46. Weaver S.C., Brault A.C., Kang W., Holland J.J. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J. Virol. 1999, 73:4316-4326.
47. Weston J., Villoing S., Bremont M., Castric J., Pfeffer M., Jewhurst V., McLoughlin M., Rodseth O., Christie K.E., Koumans J., Todd D. Comparison of two aquatic alphaviruses, salmon pancreas disease virus and sleeping disease virus, by using genome sequence analysis, monoclonal reactivity, and cross-infection. J. Virol. 2002, 76:6155-6163.
48. Xu C., Guo T.C., Mutoloki S., Haugland Ø., Majara I.S.E., Evensen Ø. Alpha interferon and not gamma interferon inhibits salmonid alphavirus subtype 3 replication in vitro. J. Virol. 2010, 84:8903-8927.
49. Zhang Y.G., Burke C.W., Rayman K.D., Klimstra W.B. Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. J. Virol. 2007, 81:11246-11255.
50. 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. J. Immunol. 2005, 175:2484-3249.