Identification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties

Developmental and Comparative Immunology

Volumn 33, Issue 4, 2009, Pages 547-558

  Sun, Baojian ^a   Robertsen, Børre ^a   Wang, Zhiqiang ^b   Liu, Bin ^b  

^a UNIVERSITY OF TROMSØ   (Norway)

^b INSTITUTE OF OCEANOLOGY   (China)

Author keywords

Anolis; Antiviral; dsRNA; Evolution; Fish; Interferon; Promoter; Reptile; Virus

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON A1; INTERFERON A3; INTERFERON B1; INTERFERON B2; INTERFERON B3; INTERFERON C1; INTERFERON C2; INTERFERON C3; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ATLANTIC SALMON; CONTROLLED STUDY; GENE CLUSTER; GENE EXPRESSION; GENE IDENTIFICATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL;

ANOLIS; MAMMALIA; REPTILIA; SALMO SALAR;

EID: 58649114710     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2008.10.001     Document Type: Article

References (51)

1. Takeuchi O., and Akira S. Recognition of viruses by innate immunity. Immunol Rev 220 (2007) 214-224
2. Muller U., Steinhoff U., Reis L.F., Hemmi S., Pavlovic J., Zinkernagel R.M., et al. Functional role of type I and type II interferons in antiviral defense. Science 264 (1994) 1918-1921
3. Uze G., and Monneron D. IL-28 and IL-29: newcomers to the interferon family. Biochimie 89 (2007) 729-734
4. Pestka S., Krause C.D., and Walter M.R. Interferons, interferon-like cytokines, and their receptors. Immunol Rev 202 (2004) 8-32
5. Kotenko S.V., Gallagher G., Baurin V.V., Lewis-Antes A., Shen M., Shah N.K., et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 4 (2003) 69-77
6. Robertsen B. The interferon system of teleost fish. Fish Shellfish Immunol 20 (2006) 172-191
7. Robertsen B. Expression of interferon and interferon-induced genes in salmonids in response to virus infection, interferon-inducing compounds and vaccination. Fish Shellfish Immunol 25 (2008) 351-357
8. Altmann S.M., Mellon M.T., Distel D.L., and Kim C.H. Molecular and functional analysis of an interferon gene from the Zebrafish, Danio rerio. J Virol 77 (2003) 1992-2002
9. Lutfalla G., Crollius H.R., Stange-Thomann N., Jaillon O., Mogensen K., and Monneron D. Comparative genomic analysis reveals independent expansion of a lineage-specific gene family in vertebrates: the class II cytokine receptors and their ligands in mammals and fish. BMC Genomics 4 (2003) 29
10. Robertsen B., Bergan V., Rokenes T., Larsen R., and Albuquerque A. Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J Interferon Cytokine Res 23 (2003) 601-612
11. Long S., Milev-Milovanovic I., Wilson M., Bengten E., Clem L.W., Miller N.W., et al. Identification and expression analysis of cDNAs encoding channel catfish type I interferons. Fish Shellfish Immunol 21 (2006) 42-59
12. Long S., Wilson M., Bengten E., Bryan L., Clem L.W., Miller N.W., et al. Identification of a cDNA encoding channel catfish interferon. Dev Comp Immunol 28 (2004) 97-111
13. Zou J., Carrington A., Collet B., Dijkstra J.M., Yoshiura Y., Bols N., et al. Identification and bioactivities of IFN-gamma in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish. J Immunol 175 (2005) 2484-2494
14. Milev-Milovanovic I., Long S., Wilson M., Bengten E., Miller N.W., and Chinchar V.G. Identification and expression analysis of interferon gamma genes in channel catfish. Immunogenetics 58 (2006) 70-80
15. Kileng O., Brundtland M.I., and Robertsen B. Infectious salmon anemia virus is a powerful inducer of key genes of the type I interferon system of Atlantic salmon, but is not inhibited by interferon. Fish Shellfish Immunol 23 (2007) 378-389
16. Bergan V., Steinsvik S., Xu H., Kileng O., and Robertsen B. Promoters of type I interferon genes from Atlantic salmon contain two main regulatory regions. FEBS J 273 (2006) 3893-3906
17. Rokenes T.P., Larsen R., and Robertsen B. Atlantic salmon ISG15: Expression and conjugation to cellular proteins in response to interferon, double-stranded RNA and virus infections. Mol Immunol 44 (2007) 950-959
18. Zou J., Tafalla C., Truckle J., and Secombes C.J. Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J Immunol 179 (2007) 3859-3871
19. Liu Y.J. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 23 (2005) 275-306
20. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441 (2006) 101-105
21. Hemmi H., Kaisho T., Takeuchi O., Sato S., Sanjo H., Hoshino K., et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 3 (2002) 196-200
22. Doxsee C.L., Riter T.R., Reiter M.J., Gibson S.J., Vasilakos J.P., and Kedl R.M. The immune response modifier and Toll-like receptor 7 agonist S-27609 selectively induces IL-12 and TNF-alpha production in CD11c+CD11b+CD8- dendritic cells. J Immunol 171 (2003) 1156-1163
23. Alexopoulou L., Holt A.C., Medzhitov R., and Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413 (2001) 732-738
24. Meijer A.H., Gabby Krens S.F., Medina Rodriguez I.A., He S., Bitter W., Ewa Snaar-Jagalska B., et al. Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish. Mol Immunol 40 (2004) 773-783
25. Jault C., Pichon L., and Chluba J. Toll-like receptor gene family and TIR-domain adapters in Danio rerio. Mol Immunol 40 (2004) 759-771
26. Rodriguez M.F., Wiens G.D., Purcell M.K., and Palti Y. Characterization of Toll-like receptor 3 gene in rainbow trout (Oncorhynchus mykiss). Immunogenetics 57 (2005) 510-519
27. Fan S., Chen S., Liu Y., Lin Y., Liu H., Guo L., et al. Zebrafish TRIF, a golgi-localized protein, participates in IFN induction and NF-{kappa}B activation. J Immunol 180 (2008) 5373-5383
28. Kileng Ø., Albuquerque A., and Robertsen B. Induction of interferon system genes in Atlantic salmon by the imidazoquinoline S-27609, a ligand for Toll-like receptor 7. Fish Shellfish Immunol 24 (2008) 514-522
29. Lenardo M.J., Fan C.M., Maniatis T., and Baltimore D. The involvement of NF-kappa B in beta-interferon gene regulation reveals its role as widely inducible mediator of signal transduction. Cell 57 (1989) 287-294
30. Wathelet M.G., Lin C.H., Parekh B.S., Ronco L.V., Howley P.M., and Maniatis T. Virus infection induces the assembly of coordinately activated transcription factors on the IFN-beta enhancer in vivo. Mol Cell 1 (1998) 507-518
31. MacDonald N.J., Kuhl D., Maguire D., Naf D., Gallant P., Goswamy A., et al. Different pathways mediate virus inducibility of the human IFN-alpha 1 and IFN-beta genes. Cell 60 (1990) 767-779
32. Civas A., Genin P., Morin P., Lin R., and Hiscott J. Promoter organization of the interferon-A genes differentially affects virus-induced expression and responsiveness to TBK1 and IKKepsilon. J Biol Chem 281 (2006) 4856-4866
33. Ewing B., and Green P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8 (1998) 186-194
34. Ewing B., Hillier L., Wendl M.C., and Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8 (1998) 175-185
35. Gordon D., Abajian C., and Green P. Consed: a graphical tool for sequence finishing. Genome Res 8 (1998) 195-202
36. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 (1994) 4673-4680
37. Tamura K., Dudley J., Nei M., and Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 (2007) 1596-1599
38. Rasmussen R. Quantification on the LightCycler. In: Meuer S., Wittwer C., and Nakagawara K. (Eds). Rapid cycle real-time PCR (2001), Springer Press, Heidelberg, Germany 21-34
39. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29 (2001) e45
40. Jorgensen J.B., Johansen A., Stenersen B., and Sommer A.I. CpG oligodeoxynucleotides and plasmid DNA stimulate Atlantic salmon (Salmo salar L.) leucocytes to produce supernatants with antiviral activity. Dev Comp Immunol 25 (2001) 313-321
41. Wergeland H.I., and Aakre Johansen R. A salmonid cell line (TO) for production of infectious salmon anaemia virus (ISAV). Dis Aquat Org 44 (2001) 183-190
42. Radhakrishnan R., Walter L.J., Hruza A., Reichert P., Trotta P.P., Nagabhushan T.L., et al. Zinc mediated dimer of human interferon-alpha 2b revealed by X-ray crystallography. Structure 4 (1996) 1453-1463
43. Cartharius K., Frech K., Grote K., Klocke B., Haltmeier M., Klingenhoff A., et al. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21 (2005) 2933-2942
44. Lin R., Genin P., Mamane Y., and Hiscott J. Selective DNA binding and association with the CREB binding protein coactivator contribute to differential activation of alpha/beta interferon genes by interferon regulatory factors 3 and 7. Mol Cell Biol 20 (2000) 6342-6353
45. Visvanathan K.V., and Goodbourn S. Double-stranded RNA activates binding of NF-kappa B to an inducible element in the human beta-interferon promoter. EMBO J 8 (1989) 1129-1138
46. Allendorf F.W., and Thorgaard G.H. Tetraploidy and the evolution of salmonid fishes. In: Turner B.J. (Ed). Evolutionary genetics of fishes (1984), Plenum, New York 1-53
47. Chen J., Baig E., and Fish E.N. Diversity and relatedness among the type I interferons. J Interferon Cytokine Res 24 (2004) 687-698
48. Purcell M.K., Smith K.D., Hood L., Winton J.R., and Roach J.C. Conservation of Toll-like receptor signaling pathways in teleost fish. Comp Biochem Physiol Part D Genomics Proteomics 1 (2006) 77-88
49. Stein C., Caccamo M., Laird G., and Leptin M. Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish. Genome Biol 8 (2007) R251
50. Matsuo A., Oshiumi H., Tsujita T., Mitani H., Kasai H., Yoshimizu M., et al. Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from birnaviruses. J Immunol 181 (2008) 3474-3485
51. Hughes A.L., and Roberts R.M. Independent origin of IFN-alpha and IFN-beta in birds and mammals. J Interferon Cytokine Res 20 (2000) 737-739