Salmonids Have an Extraordinary Complex Type I IFN System

Characterization of the IFN Locus in Rainbow Trout Oncorhynchus mykiss Reveals Two Novel IFN Subgroups

Jun Zou* (Corresponding Author), Bartolomeo Gorgoglione, Nicholas G. H. Taylor, Thitiya Summathed, Po-Tsang Lee, Akshaya Panigrahi, Carine Genet, Young-Mao Chen, Tzong-Yueh Chen, Mahmood Ul Hassan, Sharif M. Mughal, Pierre Boudinot, Christopher J. Secombes

*Corresponding author for this work

Research output: Contribution to journalArticle

52 Citations (Scopus)

Abstract

Fish type I IFNs are classified into two groups with two (group I) or four (group II) cysteines in the mature peptide and can be further divided into four subgroups, termed IFN-a, -b, -c, and -d. Salmonids possess all four subgroups, whereas other teleost species have one or more but not all groups. In this study, we have discovered two further subgroups (IFN-e and -f) in rainbow trout Oncorhynchus mykiss and analyzed the expression of all six subgroups in rainbow trout and brown trout Salmo trutta. In rainbow trout RTG-2 and RTS-11 cells, polyinosinic-polycytidylic acid stimulation resulted in early activation of IFN-d, whereas the IFN-e subgroup containing the highest number of members showed weak induction. In contrast with the cell lines, remarkable induction of IFN-a, -b, and -c was detected in primary head kidney leukocytes after polyinosinic-polycytidylic acid treatment, whereas a moderate increase of IFNs was observed after stimulation with resiquimod. Infection of brown trout with hemorrhagic septicemia virus resulted in early induction of IFN-d, -e, and -f and a marked increase of IFN-b and IFN-c expression in kidney and spleen. IFN transcripts were found to be strongly correlated with the viral burden and with marker genes of the IFN antiviral cascade. The results demonstrate that the IFN system of salmonids is far more complex than previously realized, and in-depth research is required to fully understand its regulation and function.

Original languageEnglish
Pages (from-to)2273-2286
Number of pages14
JournalThe Journal of Immunology
Volume193
Issue number5
Early online date15 Aug 2014
DOIs
Publication statusPublished - 1 Sep 2014

Keywords

  • infectious pancreatic necrosis virus
  • innate immune-response
  • art. no. 29
  • Atlantic salmon
  • teleost fish
  • functional-characterization
  • molecular characterization
  • expression analysis
  • antiviral activity
  • interferon genes

Cite this

Salmonids Have an Extraordinary Complex Type I IFN System : Characterization of the IFN Locus in Rainbow Trout Oncorhynchus mykiss Reveals Two Novel IFN Subgroups. / Zou, Jun (Corresponding Author); Gorgoglione, Bartolomeo; Taylor, Nicholas G. H.; Summathed, Thitiya; Lee, Po-Tsang; Panigrahi, Akshaya; Genet, Carine; Chen, Young-Mao; Chen, Tzong-Yueh; Ul Hassan, Mahmood; Mughal, Sharif M.; Boudinot, Pierre; Secombes, Christopher J.

In: The Journal of Immunology, Vol. 193, No. 5, 01.09.2014, p. 2273-2286.

Research output: Contribution to journalArticle

Zou, J, Gorgoglione, B, Taylor, NGH, Summathed, T, Lee, P-T, Panigrahi, A, Genet, C, Chen, Y-M, Chen, T-Y, Ul Hassan, M, Mughal, SM, Boudinot, P & Secombes, CJ 2014, 'Salmonids Have an Extraordinary Complex Type I IFN System: Characterization of the IFN Locus in Rainbow Trout Oncorhynchus mykiss Reveals Two Novel IFN Subgroups', The Journal of Immunology, vol. 193, no. 5, pp. 2273-2286. https://doi.org/10.4049/jimmunol.1301796
Zou, Jun ; Gorgoglione, Bartolomeo ; Taylor, Nicholas G. H. ; Summathed, Thitiya ; Lee, Po-Tsang ; Panigrahi, Akshaya ; Genet, Carine ; Chen, Young-Mao ; Chen, Tzong-Yueh ; Ul Hassan, Mahmood ; Mughal, Sharif M. ; Boudinot, Pierre ; Secombes, Christopher J. / Salmonids Have an Extraordinary Complex Type I IFN System : Characterization of the IFN Locus in Rainbow Trout Oncorhynchus mykiss Reveals Two Novel IFN Subgroups. In: The Journal of Immunology. 2014 ; Vol. 193, No. 5. pp. 2273-2286.
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abstract = "Fish type I IFNs are classified into two groups with two (group I) or four (group II) cysteines in the mature peptide and can be further divided into four subgroups, termed IFN-a, -b, -c, and -d. Salmonids possess all four subgroups, whereas other teleost species have one or more but not all groups. In this study, we have discovered two further subgroups (IFN-e and -f) in rainbow trout Oncorhynchus mykiss and analyzed the expression of all six subgroups in rainbow trout and brown trout Salmo trutta. In rainbow trout RTG-2 and RTS-11 cells, polyinosinic-polycytidylic acid stimulation resulted in early activation of IFN-d, whereas the IFN-e subgroup containing the highest number of members showed weak induction. In contrast with the cell lines, remarkable induction of IFN-a, -b, and -c was detected in primary head kidney leukocytes after polyinosinic-polycytidylic acid treatment, whereas a moderate increase of IFNs was observed after stimulation with resiquimod. Infection of brown trout with hemorrhagic septicemia virus resulted in early induction of IFN-d, -e, and -f and a marked increase of IFN-b and IFN-c expression in kidney and spleen. IFN transcripts were found to be strongly correlated with the viral burden and with marker genes of the IFN antiviral cascade. The results demonstrate that the IFN system of salmonids is far more complex than previously realized, and in-depth research is required to fully understand its regulation and function.",
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AU - Gorgoglione, Bartolomeo

AU - Taylor, Nicholas G. H.

AU - Summathed, Thitiya

AU - Lee, Po-Tsang

AU - Panigrahi, Akshaya

AU - Genet, Carine

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N1 - We thank Dr. Richard Paley and Tom Hill for the contribution to the brown trout infection challenge experiments and viral assessment in the Centre for Environment, Fisheries and Aquaculture Science, Weymouth, U.K. This work was supported by the Department for Environment, Food and Rural Affairs (U.K.), the Marine Alliance for Science and Technology for Scotland, the British Council Inspire Programme, the Royal Society of Edinburgh, and the European Commission–funded Imaquanim project. The brown trout viral hemorrhagic septicemia trials were supported financially by the Department for Environment, Food and Rural Affairs (Contract C3490).

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N2 - Fish type I IFNs are classified into two groups with two (group I) or four (group II) cysteines in the mature peptide and can be further divided into four subgroups, termed IFN-a, -b, -c, and -d. Salmonids possess all four subgroups, whereas other teleost species have one or more but not all groups. In this study, we have discovered two further subgroups (IFN-e and -f) in rainbow trout Oncorhynchus mykiss and analyzed the expression of all six subgroups in rainbow trout and brown trout Salmo trutta. In rainbow trout RTG-2 and RTS-11 cells, polyinosinic-polycytidylic acid stimulation resulted in early activation of IFN-d, whereas the IFN-e subgroup containing the highest number of members showed weak induction. In contrast with the cell lines, remarkable induction of IFN-a, -b, and -c was detected in primary head kidney leukocytes after polyinosinic-polycytidylic acid treatment, whereas a moderate increase of IFNs was observed after stimulation with resiquimod. Infection of brown trout with hemorrhagic septicemia virus resulted in early induction of IFN-d, -e, and -f and a marked increase of IFN-b and IFN-c expression in kidney and spleen. IFN transcripts were found to be strongly correlated with the viral burden and with marker genes of the IFN antiviral cascade. The results demonstrate that the IFN system of salmonids is far more complex than previously realized, and in-depth research is required to fully understand its regulation and function.

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KW - functional-characterization

KW - molecular characterization

KW - expression analysis

KW - antiviral activity

KW - interferon genes

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