Antiviral activity of salmonid gamma interferon against infectious pancreatic necrosis virus and salmonid alphavirus and its dependency on type I interferon

Baojian Sun, Ingrid Skjaeveland, Tina Svingerud, Jun Zou, Jorunn Jorgensen, Borre Robertsen

Research output: Contribution to journalArticle

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Abstract

We investigated the antiviral activity and gene induction properties of interferon gamma (IFN-gamma) compared to type I IFN (IFNa1) in Atlantic salmon. IFN-gamma protected salmon cells against infectious pancreatic necrosis virus (IPNV)-induced cytopathic effect (CPE), reduced virus titers, and inhibited the synthesis of the viral structural protein VP3. Moreover, IFN-gamma showed potent antiviral activity against salmonid alphavirus 3 (SAV3) measured as a reduction in virus nsP1 transcripts. IFN-gamma (a type II IFN) had less specific antiviral activity against IPNV than IFNa1, showing a half-maximal effective concentration of 1.6 ng/ml versus 31 pg/ml determined in the CPE reduction assay. Compared to IFNa1, IFN-gamma was a more effective inducer of the antiviral protein GBP, several interferon regulatory transcription factors (IRFs), and the chemokine IP-10. The antiviral activity of IFN-gamma may also in part be ascribed to upregulation of Mx, ISG15, and viperin. These are typical type I IFN-induced genes in mammals and were also more strongly induced by IFNa1 than by IFN-gamma in salmon cells. Fish and mammalian IFN-gamma thus show strikingly similar gene induction properties. Interestingly, the antiviral activity of IFN-gamma against IPNV and SAV3 and its ability to induce Mx and ISG15 markedly decreased in the presence of neutralizing antiserum against IFNa1. In contrast, antiIFNa1 had no effect on the induction of IRF-1 and IP-10 by IFN-gamma. This suggests that the antiviral activity of IFN-gamma is partially dependent on IFNa induction. However, because antiIFNa1 could not abolish the IFN-gamma-mediated induction of Mx and ISG15 completely, IFN-gamma may possibly also induce such genes directly.

Original languageEnglish
Pages (from-to)9188-9198
Number of pages11
JournalJournal of Virology
Volume85
Issue number17
DOIs
Publication statusPublished - Sep 2011

Keywords

  • double-stranded-RNA
  • trout oncorhynchus-mykiss
  • Atlantic salmon
  • anemia-virus
  • IFN-gamma
  • expression analysis
  • binding protein
  • teleost fish
  • MX proteins
  • kinase PKR

Cite this

Antiviral activity of salmonid gamma interferon against infectious pancreatic necrosis virus and salmonid alphavirus and its dependency on type I interferon. / Sun, Baojian; Skjaeveland, Ingrid; Svingerud, Tina; Zou, Jun; Jorgensen, Jorunn; Robertsen, Borre.

In: Journal of Virology, Vol. 85, No. 17, 09.2011, p. 9188-9198.

Research output: Contribution to journalArticle

Sun, Baojian ; Skjaeveland, Ingrid ; Svingerud, Tina ; Zou, Jun ; Jorgensen, Jorunn ; Robertsen, Borre. / Antiviral activity of salmonid gamma interferon against infectious pancreatic necrosis virus and salmonid alphavirus and its dependency on type I interferon. In: Journal of Virology. 2011 ; Vol. 85, No. 17. pp. 9188-9198.
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T1 - Antiviral activity of salmonid gamma interferon against infectious pancreatic necrosis virus and salmonid alphavirus and its dependency on type I interferon

AU - Sun, Baojian

AU - Skjaeveland, Ingrid

AU - Svingerud, Tina

AU - Zou, Jun

AU - Jorgensen, Jorunn

AU - Robertsen, Borre

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AB - We investigated the antiviral activity and gene induction properties of interferon gamma (IFN-gamma) compared to type I IFN (IFNa1) in Atlantic salmon. IFN-gamma protected salmon cells against infectious pancreatic necrosis virus (IPNV)-induced cytopathic effect (CPE), reduced virus titers, and inhibited the synthesis of the viral structural protein VP3. Moreover, IFN-gamma showed potent antiviral activity against salmonid alphavirus 3 (SAV3) measured as a reduction in virus nsP1 transcripts. IFN-gamma (a type II IFN) had less specific antiviral activity against IPNV than IFNa1, showing a half-maximal effective concentration of 1.6 ng/ml versus 31 pg/ml determined in the CPE reduction assay. Compared to IFNa1, IFN-gamma was a more effective inducer of the antiviral protein GBP, several interferon regulatory transcription factors (IRFs), and the chemokine IP-10. The antiviral activity of IFN-gamma may also in part be ascribed to upregulation of Mx, ISG15, and viperin. These are typical type I IFN-induced genes in mammals and were also more strongly induced by IFNa1 than by IFN-gamma in salmon cells. Fish and mammalian IFN-gamma thus show strikingly similar gene induction properties. Interestingly, the antiviral activity of IFN-gamma against IPNV and SAV3 and its ability to induce Mx and ISG15 markedly decreased in the presence of neutralizing antiserum against IFNa1. In contrast, antiIFNa1 had no effect on the induction of IRF-1 and IP-10 by IFN-gamma. This suggests that the antiviral activity of IFN-gamma is partially dependent on IFNa induction. However, because antiIFNa1 could not abolish the IFN-gamma-mediated induction of Mx and ISG15 completely, IFN-gamma may possibly also induce such genes directly.

KW - double-stranded-RNA

KW - trout oncorhynchus-mykiss

KW - Atlantic salmon

KW - anemia-virus

KW - IFN-gamma

KW - expression analysis

KW - binding protein

KW - teleost fish

KW - MX proteins

KW - kinase PKR

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DO - 10.1128/JVI.00319-11

M3 - Article

VL - 85

SP - 9188

EP - 9198

JO - Journal of Virology

JF - Journal of Virology

SN - 0022-538X

IS - 17

ER -