TY - JOUR
T1 - Salmonids Have an Extraordinary Complex Type I IFN System
T2 - Characterization of the IFN Locus in Rainbow Trout Oncorhynchus mykiss Reveals Two Novel IFN Subgroups
AU - Zou, Jun
AU - Gorgoglione, Bartolomeo
AU - Taylor, Nicholas G. H.
AU - Summathed, Thitiya
AU - Lee, Po-Tsang
AU - Panigrahi, Akshaya
AU - Genet, Carine
AU - Chen, Young-Mao
AU - Chen, Tzong-Yueh
AU - Ul Hassan, Mahmood
AU - Mughal, Sharif M.
AU - Boudinot, Pierre
AU - Secombes, Christopher J.
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).
PY - 2014/9/1
Y1 - 2014/9/1
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.
AB - 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.
KW - infectious pancreatic necrosis virus
KW - innate immune-response
KW - art. no. 29
KW - Atlantic salmon
KW - teleost fish
KW - functional-characterization
KW - molecular characterization
KW - expression analysis
KW - antiviral activity
KW - interferon genes
U2 - 10.4049/jimmunol.1301796
DO - 10.4049/jimmunol.1301796
M3 - Article
C2 - 25080482
VL - 193
SP - 2273
EP - 2286
JO - The Journal of Immunology
JF - The Journal of Immunology
SN - 0022-1767
IS - 5
ER -