The Atlantic salmon protein tyrosine kinase Tyk2: Molecular cloning, modulation of expression and function

Developmental and Comparative Immunology

Volumn 41, Issue 4, 2013, Pages 553-563

  Sobhkhez, Mehrdad ^a   Hansen, Tom ^a   Iliev, Dimitar B ^a   Skjesol, Astrid ^a   Jørgensen, Jorunn B ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Innate immunity; Interferons; JAK; STAT; Tyrosine kinase 2 (Tyk2)

Indexed keywords

COMPLEMENTARY DNA; PROTEIN KINASE TYK2;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; ATLANTIC SALMON; CODON; CONTROLLED STUDY; DNA SEQUENCE; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; GENE; GENE OVEREXPRESSION; MAMMAL; MODULATION; MOLECULAR CLONING; MX GENE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; SPECIES; TYK2 GENE; UPREGULATION;

MAMMALIA; SALMO SALAR; VERTEBRATA;

AA; AMINO ACID; BASE PAIR; BP; HEAD KIDNEY; HK; IFN; INNATE IMMUNITY; INTERFERON; INTERFERON RESPONSIVE GENES; INTERFERON STIMULATED RESPONSE ELEMENT; INTERFERONS; ISG'S; ISRE; JAK; JANUS HOMOLOGY; JANUS KINASE; JH; SALMO SALAR; SIGNAL TRANSDUCERS AND ACTIVATORS OF THE TRANSCRIPTION; SS; STAT; TYK2; TYROSINE KINASE 2; TYROSINE KINASE 2 (TYK2);

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FISH PROTEINS; GENE EXPRESSION; INTERFERONS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHYLOGENY; PROTEIN-TYROSINE KINASES; SALMO SALAR; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; TYK2 KINASE;

EID: 84883399611     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.07.008     Document Type: Article

References (47)

1. Aaronson D.S., Horvath C.M. A road map for those who don't know JAK-STAT. Science (New York, N.Y.) 2002, 296:1653-1655.
2. Aggad D., Mazel M., Boudinot P., Mogensen K.E., Hamming O.J., Hartmann R., Kotenko S., Herbomel P., Lutfalla G., Levraud J.P. The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains. J. Immunol. (Baltimore, Md.: 1950) 2009, 183:3924-3931.
3. Araki T., Nawa H., Neel B.G. Tyrosyl phosphorylation of Shp2 is required for normal ERK activation in response to some, but not all, growth factors. J. Biol. Chem. 2003, 278:41677-41684.
4. Aringer M., Cheng A., Nelson J.W., Chen M., Sudarshan C., Zhou Y.J., O'Shea J.J. Janus kinases and their role in growth and disease. Life Sci. 1999, 64:2173-2186.
5. Brierley M.M., Fish E.N. Stats: multifaceted regulators of transcription. J. Interferon Cytokine Res. 2005, 25:733-744.
6. Colamonici O., Yan H., Domanski P., Handa R., Smalley D., Mullersman J., Witte M., Krishnan K., Krolewski J. Direct binding to and tyrosine phosphorylation of the alpha subunit of the type I interferon receptor by p135tyk2 tyrosine kinase. Mol. Cell. Biol. 1994, 14:8133-8142.
7. Colamonici O.R., Uyttendaele H., Domanski P., Yan H., Krolewski J.J. P135tyk2, an interferon-alpha-activated tyrosine kinase, is physically associated with an interferon-alpha receptor. J. Biol. Chem. 1994, 269:3518-3522.
8. Collet B., Secombes C.J. The rainbow trout (Oncorhynchus mykiss) Mx1 promoter. Structural and functional characterization. FEBS J. 2001, 268:1577-1584.
9. Collet B., Secombes C.J. The rainbow trout (Oncorhynchus mykiss) Mx1 promoter. Structural and functional characterization. Eur. J. Biochem. 2001, 268:1577-1584.
10. Collet B., Bain N., Prevost S., Besinque G., McBeath A., Snow M., Collins C. Isolation of an atlantic salmon (Salmo salar) signal transducer and activator of transcription STAT1 gene: Kinetics of expression upon ISAV or IPNV infection. Fish Shellfish Immunol. 2008, 25:861-867.
11. Constantinescu S.N., Croze E., Wang C., Murti A., Basu L., Mullersman J.E., Pfeffer L.M. Role of interferon alpha/beta receptor chain 1 in the structure and transmembrane signaling of the interferon alpha/beta receptor complex. Proc. Natl. Acad. Sci. 1994, 91:9602-9606.
12. Conway G., Margoliath A., Wong-Madden S., Roberts R.J., Gilbert W. Jak1 kinase is required for cell migrations and anterior specification in zebrafish embryos. Proc. Natl. Acad. Sci. 1997, 94:3082-3087.
13. Gadina M., Hilton D., Johnston J.A., Morinobu A., Lighvani A., Zhou Y.J., Visconti R., O'Shea J.J. Signaling by type I and II cytokine receptors: ten years after. Curr. Opin. Immunol. 2001, 13:363-373.
14. Gauzzi M.C., Velazquez L., McKendry R., Mogensen K.E., Fellous M., Pellegrini S. Interferon-α-dependent activation of tyk2 requires phosphorylation of positive regulatory tyrosines by another kinase. J. Biol. Chem. 1996, 271:20494-20500.
15. Gauzzi M.C., Barbieri G., Richter M.F., Uzé G., Ling L., Fellous M., Pellegrini S. The amino-terminal region of Tyk2 sustains the level of interferon α receptor 1, a component of the interferon α/β receptor. Proc. Natl. Acad. Sci. 1997, 94:11839-11844.
16. Guo C.-J., Zhang Y.-F., Yang L.-S., Yang X.-B., Wu Y.-Y., Liu D., Chen W.-J., Weng S.-P., Yu X.-Q., He J.-G. The JAK and STAT family members of the mandarin fish Siniperca chuatsi: molecular cloning, tissues distribution and immunobiological activity. Fish Shellfish Immunol. 2009, 27:349-359.
17. Hansen T.E., Jørgensen J.B. Cloning and characterisation of p38 MAP kinase from atlantic salmon: a kinase important for regulating salmon TNF-2 and IL-1β expression. Mol. Immunol. 2007, 44:3137-3146.
18. Ihle J.N., Kerr I.M. Jaks and Stats in signaling by the cytokine receptor superfamily. Trends Genet. 1995, 11:69-74.
19. Jensen I., Robertsen B. Effect of double-stranded RNA and interferon on the antiviral activity of atlantic salmon cells against infectious salmon anemia virus and infectious pancreatic necrosis virus. Fish Shellfish Immunol. 2002, 13:221-241.
20. Lemmon M.A., Schlessinger J. Regulation of signal transduction and signal diversity by receptor oligomerization. Trends Biochem. Sci. 1994, 19:459-463.
21. Leu J.H., Yan S.J., Lee T.F., Chou C.M., Chen S.T., Hwang P.P., Chou C.K., Huang C.J. Complete genomic organization and promoter analysis of the round-spotted pufferfish JAK1, JAK2, JAK3, and TYK2 genes. DNA Cell Biol. 2000, 19:431-446.
22. Ma A.C., Ward A.C., Liang R., Leung A.Y. The role of jak2a in zebrafish hematopoiesis. Blood 2007, 110:1824-1830.
23. Martin C.S., Wight P.A., Dobretsova A., Bronstein I. Dual luminescence-based reporter gene assay for luciferase and beta-galactosidase. Biotechniques 1996, 21:520-524.
24. Nicholson B.L., Byrne C. An Established Cell Line from the atlantic salmon (Salmo salar). J. Fish. Res. Board Can. 1973, 30:913-916.
25. Oates A.C., Brownlie A., Pratt S.J., Irvine D.V., Liao E.C., Paw B.H., Dorian K.J., Johnson S.L., Postlethwait J.H., Zon L.I., Wilks A.F. Gene duplication of zebrafish JAK2 homologs is accompanied by divergent embryonic expression patterns: only jak2a is expressed during erythropoiesis. Blood 1999, 94:2622-2636.
26. Oates A.C., Wollberg P., Pratt S.J., Paw B.H., Johnson S.L., Ho R.K., Postlethwait J.H., Zon L.I., Wilks A.F. Zebrafish stat3 is expressed in restricted tissues during embryogenesis and stat1 rescues cytokine signaling in a STAT1-deficient human cell line. Dev. Dyn. 1999, 215:352-370.
27. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
28. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 2005, 5:375-386.
29. Prchal-Murphy M., Semper C., Lassnig C., Wallner B., Gausterer C., Teppner-Klymiuk I., Kobolak J., Müller S., Kolbe T., Karaghiosoff M., Dinnyés A., Rülicke T., Leitner N.R., Strobl B., Müller M. TYK2 kinase activity is required for functional type i interferon responses in vivo. PLoS One 2012, 7:e39141.
30. Rawlings J.S., Rosler K.M., Harrison D.A. The JAK/STAT signaling pathway. J. Cell Sci. 2004, 117:1281-1283.
31. Richter M.F., Dumenil G., Uze G., Fellous M., Pellegrini S. Specific contribution of Tyk2 JH regions to the binding and the expression of the interferon alpha/beta receptor component IFNAR1. J. Biol. Chem. 1998, 273:24723-24729.
32. Robertsen B., Bergan V., Røkenes T., Larsen R., Albuquerque A. Atlantic salmon interferon genes; cloning, sequence analysis, expression, and biological activity. J. Inteferon Cytokine Res 2003, 23(10):601-612.
33. Shi J., Zhang Y.-B., Liu T.-K., Sun F., Gui J.-F. Subcellular localization and functional characterization of a fish IRF9 from crucian carp Carassius auratus. Fish Shellfish Immunol. 2012, 33:258-266.
34. Skjesol A., Hansen T., Shi C.Y., Thim H.L., Jorgensen J.B. Structural and functional studies of STAT1 from atlantic salmon (Salmo salar). BMC Immunol. 2010, 11:17.
35. Stark G.R., Kerr I.M., Williams B.R.G., Silverman R.H., Schreiber R.D. How cells respond to interferons. Annu. Rev. Biochem. 1998, 67:227-264.
36. Strandskog G., Ellingsen T., Jorgensen J.B. Characterization of three distinct CpG oligonucleotide classes which differ in ability to induce IFN alpha/beta activity and cell proliferation in atlantic salmon (Salmo salar L.) leukocytes. Dev. Comp. Immunol. 2007, 31:39-51.
37. Sugiura R., Kita A., Kuno T. Upregulation of mRNA in MAPK signaling: transcriptional activation or mRNA stabilization?. Cell cycle (Georgetown, Tex.) 2004, 3:286-288.
38. Sun B., Skjaeveland I., Svingerud T., Zou J., Jorgensen J., Robertsen B. Antiviral activity of salmonid gamma interferon against infectious pancreatic necrosis virus and salmonid alphavirus and its dependency on type I interferon. J. Virol. 2011, 85:9188-9198.
39. Svingerud T., Solstad T., Sun B., Nyrud M.L., Kileng O., Greiner-Tollersrud L., Robertsen B. Atlantic salmon type I IFN subtypes show differences in antiviral activity and cell-dependent expression: evidence for high IFNb/IFNc-producing cells in fish lymphoid tissues. J. Immunol. (Baltimore, Md.: 1950) 2012, 189:5912-5923.
40. Velazquez L., Fellous M., Stark G.R., Pellegrini S. A protein tyrosine kinase in the interferon alpha/beta signaling pathway. Cell 1992, 70:313-322.
41. Wergeland H.I., Jakobsen R.A. A salmonid cell line (TO) for production of infectious salmon anaemia virus (ISAV). Dis. Aquat. Organ. 2001, 44:183-190.
42. Yamaoka K., Saharinen P., Pesu M., Holt V.E., Silvennoinen O., O'Shea J.J. The Janus kinases (Jaks). Genome Biol. 2004, 5:253.
43. Yamashita S., Miyagi C., Carmany-Rampey A., Shimizu T., Fujii R., Schier A.F., Hirano T. Stat3 controls cell movements during zebrafish gastrulation. Dev. Cell 2002, 2:363-375.
44. Yao Y., Kubota T., Sato K., Takeuchi H., Kitai R., Matsukawa S. Interferons upregulate thymidine phosphorylase expression via JAK-STAT-dependent transcriptional activation and mRNA stabilization in human glioblastoma cells. J. Neurooncol. 2005, 72:217-223.
45. Yeh T.C., Dondi E., Uzé G., Pellegrini S. A dual role for the kinase-like domain of the tyrosine kinase Tyk2 in interferon-α signaling. Proc. Natl. Acad. Sci. 2000, 97:8991-8996.
46. Yin T., Shen R., Feng G.S., Yang Y.C. Molecular characterization of specific interactions between SHP-2 phosphatase and JAK tyrosine kinases. J. Biol. Chem. 1997, 272:1032-1037.
47. Yu F.-F., Zhang Y.-B., Liu T.-K., Liu Y., Sun F., Jiang J., Gui J.-F. Fish virus-induced interferon exerts antiviral function through Stat1 pathway. Mol. Immunol. 2010, 47:2330-2341.