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Identification of a Second Group of Type I IFNs in Fish Sheds Light on IFN Evolution in Vertebrates¹

Jun Zou^2,*, Carolina Tafalla, Jonathan Truckle^* and Chris J. Secombes^*

^* Scottish Fish Immunology Research Centre, School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom; and Centro de Investigacion en Sanidad Animal (CISA-INIA), Valdeolmos, Madrid, Spain

In this report, three type I IFN genes were identified in rainbow trout (rt) Oncorhynchus mykiss and are classified into two groups based on their primary protein sequences: group I containing two cysteine residues; and group II containing four cysteines residues. The group I rtIFNs were induced in fibroblasts (RTG-2 cells), macrophages (RTS-11 cells), and head kidney leukocytes when stimulated with polyinosinic:polycytidylic acid, whereas group II IFN was up-regulated in head kidney leukocytes but not in RTG-2 and RTS-11 cells. Recombinant group I rtIFNs were potent at inducing Mx expression and eliciting antiviral responses, whereas recombinant group II rtIFN was poor in these activities. That two subgroups of type I IFN exist in trout prompted a survey of the genomes of several fish species, including zebrafish, medaka, threespine stickleback and fugu, the amphibian Xenopus tropicalis, the monotreme platypus and the marsupial opossum, to gain further insight into possible IFN evolution. Analysis of the sequences confirmed that the new IFN subgroup found in trout (group II IFN) exists in other fish species but was not universally present in fish. The IFN genes in amphibians were shown for the first time to contain introns and to conserve the four cysteine structure found in all type I IFNs except IFN- and fish group I IFN. The data overall support the concept that different vertebrate groups have independently expanded their IFN types, with deletion of different pairs of cysteines apparent in fish group I IFN and IFN- of mammals.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ This work was supported by an European Community-funded IMAQUANIM project (Contract 007103).

² Address correspondence and reprint requests to Dr. Jun Zou, Scottish Fish Immunology Research Centre, School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom. E-mail address: j.j.zou{at}abdn.ac.uk

³ Abbreviations used in this paper: poly(I:C), polyinosinic-polycytidylic acid; rtIFN, rainbow trout IFN; RTG, rainbow trout gonad; EST, expressed sequence tag; UTR, untranslated region; VHSV, viral hemorrhagic septicemia virus; IPNV, infectious pancreatic necrosis virus; P/S, 100 µg/ml penicillin and 100 U/ml streptomycin; oligo(dT), oligodeoxythymidylate; oligo(dG), oligodeoxyguanylate; rrtIFN, recombinant rtIFN.

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