A conserved IFN-α receptor tyrosine motif directs the biological response to type I IFNs

Journal of Immunology

Volumn 180, Issue 8, 2008, Pages 5483-5489

  Zhao, Wenli ^a   Lee, Carolyn ^a   Piganis, Rebecca ^c   Plumlee, Courtney ^a   Weerd, Nicole De ^c   Hertzog, Paul J ^c   Schindler, Christian ^a,b  

^a Department of Microbiology ^*  (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; INTERFERON ALPHA RECEPTOR 1; INTERFERON ALPHA RECEPTOR 2; STAT PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; TYROSINE; UNCLASSIFIED DRUG; ALPHA BETA INTERFERON RECEPTOR; ALPHA INTERFERON; IFNAR1 PROTEIN, MOUSE; IFNAR2 PROTEIN, MOUSE; STAT1 PROTEIN, MOUSE; STAT2 PROTEIN, MOUSE;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; EMBRYO; FIBROBLAST; GENE INDUCTION; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION INITIATION; ANIMAL; CHEMISTRY; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN MOTIF;

AMINO ACID MOTIFS; ANIMALS; BASE SEQUENCE; FIBROBLASTS; INTERFERON-ALPHA; MACROPHAGES; MICE; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; MUTATION; RECEPTOR, INTERFERON ALPHA-BETA; STAT1 TRANSCRIPTION FACTOR; STAT2 TRANSCRIPTION FACTOR; TYROSINE;

EID: 45949090278     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.8.5483     Document Type: Article

References (44)

1. Pestka, S., C. D. Krause, D. Sarkar, M. R. Walter, Y. Shi, and P. B. Fisher. 2004. Interleukin-10 and related cytokines and receptors. Anna. Rev. Immunol. 22: 929-979.
2. Isaacs, A., and J. Lindenmann. 1957. Virus interference: I. The interferon. Proc. R. Soc. Lond. B Biol. Sci. 147: 258-267.
3. Uze, G., G. Schreiber, J. Piehler, and S. Pellegrini. 2007. The receptor of the type I interferon family. Curr. Top. Microbiol. Immunol. 316: 71-95.
4. Velazquez, L., M. Fellous, G. R. Stark, and S. Pellegrini. 1992. A protein tyrosine kinase in the interferon αβ signaling pathway. Cell 70: 313-322.
5. Schindler, C, D. E. Levy, and T. Decker. 2007. JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282: 20059-20063.
6. Müller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264: 1918-1921.
7. Hardy, M. P., C. M. Owczarek, S. Trajanovska, X. Liu, I. Kola, and P. J. Hertzog. 2001. The soluble murine type I interferon receptor Ifnar-2 is present in serum, is independently regulated, and has both agonistic and antagonistic properties. Blood 97: 473-482.
8. Fenner, J. E., R. Starr, A. L. Cornish, J. G. Zhang, D. Metcalf, R. D. Schreiber, K. Sheehan, D. J. Hilton, W. S. Alexander, and P. J. Hertzog. 2006. Suppressor of cytokine signaling 1 regulates the immune response to infection by a unique inhibition of type I interferon activity. Nat. Immunol. 7: 33-39.
9. Karaghiosoff, M., H. Neubauer, C. Lassnig, P. Kovarik, H. Schindler, H. Pircher, B. McCoy, C. Bogdan, T. Decker, G. Brem, et al. 2000. Partial impairment of cytokine responses in Tyk2-deficient mice. Immunity 13: 549-560.
10. Minegishi, Y., M. Saito, T. Morio, K. Watanabe, K. Agematsu, S. Tsuchiya, H. Takada, T. Hara, N. Kawamura, T. Ariga, et al. 2006. Human tyrosine kinase 2 deficiency reveals its requisite roles in multiple cytokine signals involved in innate and acquired immunity. Immunity 25: 745-755.
11. Stahl, N., T. J. Farruggella, T. G. Boulton, Z. Zhong, J. E. Darnell, Jr., and G. D. Yancopoulos. 1995. Choice of STATs and other substrates specified by modular tyro sine-based motifs in cytokine receptors. Science 267: 1349-1353.
12. Klingmueller, U., U. Lorenz, L. C. Cantley, B. G. Neel, and H. F. Lodish. 1995. Specefic recruitment of SH-PTP1 to the erythropoietin receptor causes inactivation of Jak2 and termination of proliferative signals. Cell 80: 729-738.
13. Schmitz, J., M. Weissenbach, S. Haan, P. C. Heinrich, and F. Schaper. 2000. SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gpl30. J. Biol. Chem. 275: 12848-12856.
14. Ohtani, T., K. Ishihara, T. Atsumi, K. Nishida, Y. Kaneko, T. Miyata, S. Itoh, M. Narimatsu, H. Maeda, T Fukada, et al. 2000. Dissection of signaling cascades through gpl30 in vivo: reciprocal roles for STAT3- and SHP2-mediated signals in immune responses. Immunity 12: 95-105.
15. Greenlund, A., M. O. Morales, B. L. Viviano, H. Yan, J. Krolewski, and R. D. Schreiber. 1995. STAT recruitment by tyrosine phosphorylated receptors: An ordered, reversible affinity driven process. Immunity 2: 677-687.
16. Zhao, W., E. N. Cha, C. Lee, C. Y. Park, and C. Schindler. 2007. Stat2-dependent regulation of MHC class II expression. J. Immunol. 179: 463-471.
17. Park, C, S. Li, E. Cha, and C. Schindler. 2000. Immune response in Stat2 knockout mice. Immunity 13: 795-804.
18. Decker, T., M. Muller, and S. Stockinger. 2005. The yin and yang of type I interferon activity in bacterial infection. Nat. Rev. Immunol. 5: 675-687.
19. Takaoka, A., Y. Mitani, H. Suemori, M. Sato, T. Yokochi, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Cross talk between interferon-γ and -αβ signaling components in caveolar membrane domains. Science 288: 2357-2360.
20. Yan, H., K. Krishnan, A. C. Greenlund, S. Gupta, J. T. Lim, R. D. Schreiber, C. W. Schindler, and J. J. Krolewski. 1996. Phosphorylated interferon-a receptor 1 subunit (IFNaRl) acts as a docking site for the latent form of the 113 kDa STAT2 protein. EMBO J. 15: 1064-1074.
21. Leung, S., S. A. Qureshi, I. M. Kerr, J. E. Darnell, Jr., and G. R. Stark. 1995. Role of STAT2 in the a interferon signaling pathway. Mol. Cell. Biol. 15: 1312-1317.
22. Nguyen, V. P., A. Z. Saleh, A. E. Arch, H. Yan, F. Piazza, J. Kim, and J. J. Krolewski. 2002. Stat2 binding to the interferon-α receptor 2 subunit is not required for interferon-α signaling. J. Biol. Chem. 277: 9713-9721.
23. Wagner, T. C, S. Velichko, D. Vogel, M. R. Rani, S. Leung, R. M. Ransohoff, G. R. Stark, H. D. Perez, and E. Croze. 2002. Interferon signaling is dependent on specific tyrosines located within the intracellular domain of IFNAR2c: expression of IFNAR2c tyrosine mutants in USA cells. J. Biol. Chem. 277: 1493-1499.
24. Kotenko, S. V., L. S. Izotova, O. V. Mirochintchenko, C. Lee, and S. Pestka. 1999. The intracellular domain of interferon-a receptor 2c (IFN-aR2c) chain is responsible for Stat activation. Proc. Natl. Acad. Sci. USA 96: 5007-5012.
25. Tang, X., J. S. Gao, Y. J. Guan, K. E. McLane, Z. L. Yuan, B. Ramratnam, and Y. E. Chin. 2007. Acetylation-dependent signal transduction for type I interferon receptor. Cell 131: 93-105.
26. Nguyen, K. B., W. T. Watford, R. Salomon, S. R. Hofmann, G. C. Pien, A. Morinobu, M. Gadina, J. J. O'Shea, and C. A. Biron. 2002. Critical role for STAT4 activation by type 1 interferons in the interferon-γ response to viral infection. Science 297: 2063-2066.
27. Bhattacharya, S., and C. Schindler. 2003. Regulation of Stat3 nuclear export. J. Clin. Invest. 111: 553-559.
28. Gimeno, R., C. K. Lee, C. Schindler, and D. E. Levy. 2005. Statl and Stat2 but not Stat3 arbitrate contradictory growth signals elicited by αβ interferon in T lymphocytes. Mol. Cell. Biol. 25: 5456-5465.
29. Hemmann, U., C. Gerhartz, B. Heesel, J. Sasse, G. Kurapkat, J. Grotzinger, A. Wollmer, Z. Zhong, J. E. Darnell, Jr., L. Graeve, et al. 1996. Differential activation of acute phase response factor/Stat3 and Statl via the cytoplasmic domain of the interleukin 6 signal transducer gpl30: II. Src homology SH2 domains define the specificity of stat factor activation. J. Biol. Chem. 271: 12999-13007.
30. Hwang, S. Y., P. J. Hertzog, K. A. Holland, S. H. Sumarsono, M. J. Tymms, J. A. Hamilton, G. Whitty, I. Bertoncello, and I. Kola. 1995. A null mutation in the gene encoding a type I interferon receptor component eliminates antiproliferative and antiviral responses to interferons α and β and alters macrophage responses. Proc. Natl. Acad. Sci. USA 92: 11284-11288.
31. Trajanovska, S., C. M. Owczarek, P. G. Stanton, and P. J. Hertzog. 2003. Generation and characterization of recombinant unmodified and phosphorylatable murine IFN-α1 in the methylotropic yeast Pichiapastoris. J. Interferon Cytokine Res. 23: 351-358.
32. Song, L., S. Bhattacharya, A. A. Yunus, C. D. Lima, and C. Schindler. 2006. Statl and SUMO modification. Blood 108: 3237-3244.
33. Schindler, C, K. Shuai, V. Prezioso, and J. E. Darnell. 1992. Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257: 809-813.
34. Takaoka, A., and H. Yanai. 2006. Interferon signalling network in innate defence. Cell. Micro Biol. 8: 907-922.
35. Kisseleva, T., S. Bhattacharya, J. Braunstein, and C. W. Schindler. 2002. Signaling through the JAK/STAT pathway, recent advances, and future challenges. Gene 285: 1-24.
36. Yan, H., K. Krishnan, J. T. Lim, L. G. Contillo, and J. J. Krolewski. 1996. Molecular characterization of an α interferon receptor 1 subunit (IFNaRl) domain required for TYK2 binding and signal transduction. Mol. Cell. Biol. 16: 2074-2082.
37. Colamonici, O., H. Yan, P. Domanski, R. Handa, D. Smalley, J. Mullersman, M. Witte, K. Krishnan, and J. Krolewski. 1994. Direct binding to and tyrosine phosphorylation of the a subunit of the type I interferon receptor by pl35tyk2 tyrosine kinase. Mol. Cell. Biol. 14: 8133-8142.
38. Pfeffer, L. M., J. E. Mullersman, S. R. Pfeffer, A. Murti, W. Shi, and C. H. Yang. 1997. Stat3 as an adapter to couple phosphatidylinostol 3-kinase to the INFAR1 chain of the type I interferon receptor. Science 276: 1418-1420.
39. Schindler, U., P. Wu, M. Rothe, M. Brasseur, and S. L. McKnight. 1995. Components of a Stat recognition code: evidence for two layers of molecular selectivity. Immunity 2: 689-697.
40. Hou, J., U. Schindler, W. J. Henzel, T. C. Ho, M. Brasseur, and S. L. McKnight. 1994. An interleukin-4-induced transcription factor: IL-4 Stat. Science 265: 1701-1706.
41. Shuai, K., C. M. Horvath, L. H. Huang, S. A. Qureshi, D. Cowburn, and J. E. Darnell, Jr. 1994. Interferon activation of the transcription factor Stat91 involves dimerization through SH2-phosphotyrosyl peptide interactions. Cell 76: 821-828.
42. Gupta, S., H. Yan, L. H. Wong, S. Ralph, J. Krolewski, and C. Schindler. 1996. The SH2 domains of Statl and Stat2 mediate multiple interactions in the transduction of IFN-α signals. EMBO J. 15: 1075-1084.
43. Chen, X., U. Vinkemeier, Y. Zhao, D. Jeruzalmi, J. E. Darnell, Jr., and J. Kuriyan. 1998. Crystal structure of a tyrosine phosphorylated STAT-1 dimer bound to DNA. Cell 93: 827-839.
44. Velichko, S., T. C. Wagner, J. Turkson, R. Jove, and E. Croze. 2002. STAT3 activation by type I interferons is dependent on specific tyrosines located in the cytoplasmic domain of interferon receptor chain 2c: activation of multiple STATS proceeds through the redundant usage of two tyrosine residues. J. Biol. Chem. 277: 35635-35641.