Tyrosine kinase 2 is not limiting human antiviral type III interferon responses

European Journal of Immunology

Volumn 46, Issue 11, 2016, Pages 2639-2649

  Fuchs, Sebastian ^a   Kaiser Labusch, Petra ^b   Bank, Julia ^a,c   Ammann, Sandra ^a,c   Kolb Kokocinski, Anja ^d   Edelbusch, Christine ^e   Omran, Heymut ^e   Ehl, Stephan ^a,f  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Prof Hess Kinderklinik   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^f UNIVERSITY OF FREIBURG   (Germany)

Author keywords

HAP1 cells; IFN lambda; Immunodeficiencies; NK cells; TYK2 VSV GFP; VSV GFP

Indexed keywords

ALPHA INTERFERON; ALPHA INTERFERON RECEPTOR; COMPLEMENTARY DNA; FOCAL ADHESION KINASE 1; IMMUNOGLOBULIN E; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR BETA; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 6; CYTOKINE RECEPTOR; GAMMA INTERFERON; INTERFERON; INTERLEUKIN 10 RECEPTOR; PROTEIN KINASE TYK2;

ANTIVIRAL ACTIVITY; ARTICLE; CASE REPORT; CELL ASSAY; CHILD; CONTROLLED STUDY; CYTOKINE RESPONSE; CYTOTOXICITY ASSAY; DEGRANULATION; ECZEMA; HUMAN; INFECTION RESISTANCE; MONOCYTE; NATURAL KILLER CELL; NONSENSE MUTATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY TRACT INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHOOL CHILD; SIGNAL TRANSDUCTION; SKIN ABSCESS; VIRUS REPLICATION; ANIMAL; BLOOD; CELL LINE; DEFICIENCY; DISEASE PREDISPOSITION; GENETICS; HYPER IGE SYNDROME; IMMUNOLOGY; METABOLISM; MOUSE; MUTATION; PATHOLOGY; SKIN; VIROLOGY;

ANIMALS; CELL LINE; CHILD; DISEASE SUSCEPTIBILITY; ECZEMA; HUMANS; IMMUNOGLOBULIN E; INTERFERON-GAMMA; INTERFERONS; INTERLEUKIN-10; INTERLEUKIN-6; JOB SYNDROME; KILLER CELLS, NATURAL; MICE; MUTATION; RECEPTORS, CYTOKINE; RECEPTORS, INTERLEUKIN-10; SIGNAL TRANSDUCTION; SKIN; TYK2 KINASE;

EID: 84992317629     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201646519     Document Type: Article

References (49)

1. Strobl, B., Stoiber, D., Sexl, V. and Mueller, M., Tyrosine kinase 2 (TYK2) in cytokine signalling and host immunity. Front. Biosci. (Landmark Ed) 2011. 16: 3214–3232.
2. Ragimbeau, J., Dondi, E., Alcover, A., Eid, P., Uze, G. and Pellegrini, S., The tyrosine kinase Tyk2 controls IFNAR1 cell surface expression. EMBO J. 2003. 22: 537–547.
3. Minegishi, Y., Saito, M., Morio, T., Watanabe, K., Agematsu, K., Tsuchiya, S., Takada, H. et al., Human tyrosine kinase 2 deficiency reveals its requisite roles in multiple cytokine signals involved in innate and acquired immunity. Immunity 2006. 25: 745–755.
4. Kreins, A. Y., Ciancanelli, M. J., Okada, S., Kong, X. F., Ramirez-Alejo, N., Kilic, S. S., El Baghdadi, J. et al., Human TYK2 deficiency: Mycobacterial and viral infections without hyper-IgE syndrome. J. Exp. Med. 2015. 212: 1641–1662.
5. Sohn, S. J., Barrett, K., Van Abbema, A., Chang, C., Kohli, P. B., Kanda, H., Smith, J. et al., A restricted role for TYK2 catalytic activity in human cytokine responses revealed by novel TYK2-selective inhibitors. J. Immunol. 2013. 191: 2205–2216.
6. Guschin, D., Rogers, N., Briscoe, J., Witthuhn, B., Watling, D., Horn, F., Pellegrini, S. et al., A major role for the protein tyrosine kinase JAK1 in the JAK/STAT signal transduction pathway in response to interleukin-6. EMBO J. 1995. 14: 1421–1429.
7. Prchal-Murphy, M., Semper, C., Lassnig, C., Wallner, B., Gausterer, C., Teppner-Klymiuk, I., Kobolak, J. et al., TYK2 kinase activity is required for functional type I interferon responses in vivo. PLoS One 2012. 7: e39141.
8. Velazquez, L., Mogensen, K. E., Barbieri, G., Fellous, M., Uze, G. and Pellegrini, S., Distinct domains of the protein tyrosine kinase tyk2 required for binding of interferon-alpha/beta and for signal transduction. J. Biol. Chem. 1995. 270: 3327–3334.
9. Karaghiosoff, M., Neubauer, H., Lassnig, C., Kovarik, P., Schindler, H., Pircher, H., McCoy, B. et al., Partial impairment of cytokine responses in Tyk2-deficient mice. Immunity 2000. 13: 549–560.
10. Shimoda, K., Kato, K., Aoki, K., Matsuda, T., Miyamoto, A., Shibamori, M., Yamashita, M. et al., Tyk2 plays a restricted role in IFN alpha signaling, although it is required for IL-12-mediated T cell function. Immunity 2000. 13: 561–571.
11. Shaw, M. H., Freeman, G. J., Scott, M. F., Fox, B. A., Bzik, D. J., Belkaid, Y. and Yap, G. S., Tyk2 negatively regulates adaptive Th1 immunity by mediating IL-10 signaling and promoting IFN-gamma-dependent IL-10 reactivation. J. Immunol. 2006. 176: 7263–7271.
12. Strobl, B., Bubic, I., Bruns, U., Steinborn, R., Lajko, R., Kolbe, T., Karaghiosoff, M. et al., Novel functions of tyrosine kinase 2 in the antiviral defense against murine cytomegalovirus. J. Immunol. 2005. 175: 4000–4008.
13. Schleicher, U., Mattner, J., Blos, M., Schindler, H., Rollinghoff, M., Karaghiosoff, M., Muller, M. et al., Control of Leishmania major in the absence of Tyk2 kinase. Eur. J. Immunol. 2004. 34: 519–529.
14. Stoiber, D., Kovacic, B., Schuster, C., Schellack, C., Karaghiosoff, M., Kreibich, R., Weisz, E. et al., TYK2 is a key regulator of the surveillance of B lymphoid tumors. J. Clin. Invest. 2004. 114: 1650–1658.
15. Simma, O., Zebedin, E., Neugebauer, N., Schellack, C., Pilz, A., Chang-Rodriguez, S., Lingnau, K. et al., Identification of an indispensable role for tyrosine kinase 2 in CTL-mediated tumor surveillance. Cancer Res. 2009. 69: 203–211.
16. Boisson-Dupuis, S., Kong, X. F., Okada, S., Cypowyj, S., Puel, A., Abel, L. and Casanova, J. L., Inborn errors of human STAT1: allelic heterogeneity governs the diversity of immunological and infectious phenotypes. Curr. Opin. Immunol. 2012. 24: 364–378.
17. Chapgier, A., Wynn, R. F., Jouanguy, E., Filipe-Santos, O., Zhang, S., Feinberg, J., Hawkins, K. et al., Human complete Stat-1 deficiency is associated with defective type I and II IFN responses in vitro but immunity to some low virulence viruses in vivo. J. Immunol. 2006. 176: 5078–5083.
18. Dupuis, S., Jouanguy, E., Al-Hajjar, S., Fieschi, C., Al-Mohsen, I. Z., Al-Jumaah, S., Yang, K. et al., Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency. Nat. Genet. 2003. 33: 388–391.
19. Kilic, S. S., Hacimustafaoglu, M., Boisson-Dupuis, S., Kreins, A. Y., Grant, A. V., Abel, L. and Casanova, J. L., A patient with tyrosine kinase 2 deficiency without hyper-IgE syndrome. J. Pediatr. 2012. 160: 1055–1057.
20. Kotenko, S. V. and Langer, J. A., Full house: 12 receptors for 27 cytokines. Int. Immunopharmacol. 2004. 4: 593–608.
21. Witte, K., Gruetz, G., Volk, H. D., Looman, A. C., Asadullah, K., Sterry, W., Sabat, R. et al., Despite IFN-lambda receptor expression, blood immune cells, but not keratinocytes or melanocytes, have an impaired response to type III interferons: implications for therapeutic applications of these cytokines. Genes Immun. 2009. 10: 702–714.
22. Carette, J. E., Raaben, M., Wong, A. C., Herbert, A. S., Obernosterer, G., Mulherkar, N., Kuehne, A. I. et al., Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 2011. 477: 340–343.
23. Essletzbichler, P., Konopka, T., Santoro, F., Chen, D., Gapp, B. V., Kralovics, R., Brummelkamp, T. R. et al., Megabase-scale deletion using CRISPR/Cas9 to generate a fully haploid human cell line. Genome Res. 2014. 24: 2059–2065.
24. Boldt, A., Borte, S., Fricke, S., Kentouche, K., Emmrich, F., Borte, M., Kahlenberg, F. et al., Eight-color immunophenotyping of T-, B-, and NK-cell subpopulations for characterization of chronic immunodeficiencies. Cytometry B Clin. Cytom. 2014. 86: 191–206.
25. Beziat, V., Duffy, D., Quoc, S. N., Le Garff-Tavernier, M., Decocq, J., Combadiere, B. et al., CD56brightCD16+ NK cells: a functional intermediate stage of NK cell differentiation. J. Immunol. 2011. 186: 6753–6761.
26. Juelke, K., Killig, M., Luetke-Eversloh, M., Parente, E., Gruen, J., Morandi, B., Ferlazzo, G. et al., CD62L expression identifies a unique subset of polyfunctional CD56dim NK cells. Blood 2010. 116: 1299–1307.
27. Lopez-Verges, S., Milush, J. M., Pandey, S., York, V. A., Arakawa-Hoyt, J., Pircher, H., Norris, P. J. et al., CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood 2010. 116: 3865–3874.
28. Kotenko, S. V., Gallagher, G., Baurin, V. V., Lewis-Antes, A., Shen, M., Shah, N. K., Langer, J. A. et al., IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 2003. 4: 69–77.
29. Sheppard, P., Kindsvogel, W., Xu, W., Henderson, K., Schlutsmeyer, S., Whitmore, T. E., Kuestner, R. et al., IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 2003. 4: 63–68.
30. Haller, O., Kochs, G. and Weber, F., The interferon response circuit: induction and suppression by pathogenic viruses. Virology 2006. 344: 119–130.
31. Mahlakoiv, T., Hernandez, P., Gronke, K., Diefenbach, A. and Staeheli, P., Leukocyte-derived IFN-alpha/beta and epithelial IFN-lambda constitute a compartmentalized mucosal defense system that restricts enteric virus infections. PLoS Pathog. 2015. 11: e1004782.
32. Egli, A., Levin, A., Santer, D. M., Joyce, M., O'Shea, D., Thomas, B. S., Lisboa, L. F. et al., Immunomodulatory Function of Interleukin 28B during primary infection with cytomegalovirus. J. Infect. Dis. 2014. 210: 717–727.
33. Griffiths, S. J., Koegl, M., Boutell, C., Zenner, H. L., Crump, C. M., Pica, F., Gonzalez, O. et al., A systematic analysis of host factors reveals a Med23-interferon-lambda regulatory axis against herpes simplex virus type 1 replication. PLoS Pathog. 2013. 9: e1003514.
34. Lampertico, P., Vigano, M., Cheroni, C., Facchetti, F., Invernizzi, F., Valveri, V., Soffredini, R. et al., IL28B polymorphisms predict interferon-related hepatitis B surface antigen seroclearance in genotype D hepatitis B e antigen-negative patients with chronic hepatitis B. Hepatology 2013. 57: 890–896.
35. Ge, D., Fellay, J., Thompson, A. J., Simon, J. S., Shianna, K. V., Urban, T. J., Heinzen, E. L. et al., Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 2009. 461: 399–401.
36. Lazear, H. M., Nice, T. J. and Diamond, M. S., Interferon-lambda: Immune functions at barrier surfaces and beyond. Immunity 2015. 43: 15–28.
37. Kotenko, S. V., Krause, C. D., Izotova, L. S., Pollack, B. P., Wu, W. and Pestka, S., Identification and functional characterization of a second chain of the interleukin-10 receptor complex. EMBO J. 1997. 16: 5894–5903.
38. Vairo, D., Tassone, L., Tabellini, G., Tamassia, N., Gasperini, S., Bazzoni, F., Plebani, A. et al., Severe impairment of IFN-gamma and IFN-alpha responses in cells of a patient with a novel STAT1 splicing mutation. Blood 2011. 118: 1806–1817.
39. Duncan, C. J., Mohamad, S. M., Young, D. F., Skelton, A. J., Leahy, T. R., Munday, D. C., Butler, K. M. et al., Human IFNAR2 deficiency: Lessons for antiviral immunity. Sci. Transl. Med. 2015. 7: 307ra154.
40. Hambleton, S., Goodbourn, S., Young, D. F., Dickinson, P., Mohamad, S. M., Valappil, M., McGovern, N. et al., STAT2 deficiency and susceptibility to viral illness in humans. Proc. Natl. Acad. Sci. U S A 2013. 110: 3053–3058.
41. Prchal-Murphy, M., Witalisz-Siepracka, A., Bednarik, K. T., Putz, E. M., Gotthardt, D., Meissl, K., Sexl, V. et al., tumor surveillance by NK cells requires TYK2 but not TYK2 kinase activity. Oncoimmunology 2015. 4: e1047579.
42. Paolini, R., Bernardini, G., Molfetta, R. and Santoni, A., NK cells and interferons. Cytokine Growth Factor Rev. 2015. 26: 113–120.
43. Ortaldo, J. R. and Young, H. A., IL-18 as critical co-stimulatory molecules in modulating the immune response of ITAM bearing lymphocytes. Semin. Immunol. 2006. 18: 193–196.
44. Souza-Fonseca-Guimaraes, F., Young, A., Mittal, D., Martinet, L., Bruedigam, C., Takeda, K., Andoniou, C. E. et al., NK cells require IL-28R for optimal in vivo activity. Proc. Natl. Acad. Sci. U S A 2015. 112: E2376–2384.
45. Sato, A., Ohtsuki, M., Hata, M., Kobayashi, E. and Murakami, T., Antitumor activity of IFN-lambda in murine tumor models. J. Immunol. 2006. 176: 7686–7694.
46. Ravn, P., Boesen, H., Pedersen, B. K. and Andersen, P., Human T cell responses induced by vaccination with Mycobacterium bovis bacillus Calmette-Guerin. J. Immunol. 1997. 158: 1949–1955.
47. Frommer, A., Hjeij, R., Loges, N. T., Edelbusch, C., Jahnke, C., Raidt, J., Werner, C. et al., Immunofluorescence analysis and diagnosis of primary ciliary dyskinesia with radial spoke defects. Am. J. Respir. Cell Mol. Biol. 2015. 53: 563–573.
48. Tarkar, A., Loges, N. T., Slagle, C. E., Francis, R., Dougherty, G. W., Tamayo, J. V., Shook, B. et al., DYX1C1 is required for axonemal dynein assembly and ciliary motility. Nat. Genet. 2013. 45: 995–1003.
49. Maul-Pavicic, A., Chiang, S. C., Rensing-Ehl, A., Jessen, B., Fauriat, C., Wood, S. M., Sjoqvist, S. et al., ORAI1-mediated calcium influx is required for human cytotoxic lymphocyte degranulation and target cell lysis. Proc. Natl. Acad. Sci. U S A 2011. 108: 3324–3329.