Unanchored K48-Linked Polyubiquitin Synthesized by the E3-Ubiquitin Ligase TRIM6 Stimulates the Interferon-IKKε Kinase-Mediated Antiviral Response

Immunity

Volumn 40, Issue 6, 2014, Pages 880-895

  Rajsbaum, Ricardo ^a   Versteeg, Gijs A ^a,b   Schmid, Sonja ^a   Maestre, Ana M ^a   Belicha Villanueva, Alan ^a   Martínez Romero, Carles ^a   Patel, Jenish R ^a   Morrison, Juliet ^a   Pisanelli, Giuseppe ^a,c   Miorin, Lisa ^a   Laurent Rolle, Maudry ^a   Moulton, Hong M ^d   Stein, David A ^d   Fernandez Sesma, Ana ^a   tenOever, Benjamin R ^a   García Sastre, Adolfo ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANTIVIRAL AGENTS; CELLS, CULTURED; ENZYME ACTIVATION; HUMANS; I-KAPPA B KINASE; INTERFERON TYPE I; JANUS KINASE 1; MICE; PHOSPHORYLATION; POLYUBIQUITIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES;

EID: 84903647409     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2014.04.018     Document Type: Article

References (36)

1. Abes S., Moulton H.M., Clair P., Prevot P., Youngblood D.S., Wu R.P., Iversen P.L., Lebleu B. Vectorization of morpholino oligomers by the (R-Ahx-R)4 peptide allows efficient splicing correction in the absence of endosomolytic agents. J.Control. Release 2006, 116:304-313.
2. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
3. Chen Z., Pickart C.M. A 25-kilodalton ubiquitin carrier protein (E2) catalyzes multi-ubiquitin chain synthesis via lysine 48 of ubiquitin. J.Biol. Chem. 1990, 265:21835-21842.
4. Chen Z.J., Sun L.J. Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 2009, 33:275-286.
5. Fernandez-Sesma A., Marukian S., Ebersole B.J., Kaminski D., Park M.S., Yuen T., Sealfon S.C., García-Sastre A., Moran T.M. Influenza virus evades innate and adaptive immunity via the NS1 protein. J.Virol. 2006, 80:6295-6304.
6. Frias-Staheli N., Giannakopoulos N.V., Kikkert M., Taylor S.L., Bridgen A., Paragas J., Richt J.A., Rowland R.R., Schmaljohn C.S., Lenschow D.J., et al. Ovarian tumor domain-containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2007, 2:404-416.
7. Friedman C.S., O'Donnell M.A., Legarda-Addison D., Ng A., Cárdenas W.B., Yount J.S., Moran T.M., Basler C.F., Komuro A., Horvath C.M., et al. The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep. 2008, 9:930-936.
8. Gack M.U., Shin Y.C., Joo C.H., Urano T., Liang C., Sun L., Takeuchi O., Akira S., Chen Z., Inoue S., Jung J.U. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007, 446:916-920.
9. Hemmi H., Takeuchi O., Sato S., Yamamoto M., Kaisho T., Sanjo H., Kawai T., Hoshino K., Takeda K., Akira S. The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J.Exp. Med. 2004, 199:1641-1650.
10. Ikeda F., Hecker C.M., Rozenknop A., Nordmeier R.D., Rogov V., Hofmann K., Akira S., Dötsch V., Dikic I. Involvement of the ubiquitin-like domain of TBK1/IKK-i kinases in regulation of IFN-inducible genes. EMBO J. 2007, 26:3451-3462.
11. Jiang X., Chen Z.J. The role of ubiquitylation in immune defence and pathogen evasion. Nat. Rev. Immunol. 2012, 12:35-48.
12. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H., Ishii K.J., Takeuchi O., Akira S. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 2005, 6:981-988.
13. Medzhitov R., Preston-Hurlburt P., Janeway C.A. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 1997, 388:394-397.
14. Meroni G., Diez-Roux G. TRIM/RBCC, a novel class of 'single protein RING finger' E3 ubiquitin ligases. Bioessays 2005, 27:1147-1157.
15. Meylan E., Tschopp J., Karin M. Intracellular pattern recognition receptors in the host response. Nature 2006, 442:39-44.
16. Ng S.L., Friedman B.A., Schmid S., Gertz J., Myers R.M., Tenoever B.R., Maniatis T. IκB kinase epsilon (IKK(epsilon)) regulates the balance between type I and type II interferon responses. Proc. Natl. Acad. Sci. USA 2011, 108:21170-21175.
17. Parvatiyar K., Barber G.N., Harhaj E.W. TAX1BP1 and A20 inhibit antiviral signaling by targeting TBK1-IKKi kinases. J.Biol. Chem. 2010, 285:14999-15009.
18. Pertel T., Hausmann S., Morger D., Züger S., Guerra J., Lascano J., Reinhard C., Santoni F.A., Uchil P.D., Chatel L., et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011, 472:361-365.
19. Perwitasari O., Cho H., Diamond M.S., Gale M. Inhibitor of κB kinase epsilon (IKK(epsilon)), STAT1, and IFIT2 proteins define novel innate immune effector pathway against West Nile virus infection. J.Biol. Chem. 2011, 286:44412-44423.
20. Petroski M.D., Deshaies R.J. Mechanism of lysine 48-linked ubiquitin-chain synthesis by the cullin-RING ubiquitin-ligase complex SCF-Cdc34. Cell 2005, 123:1107-1120.
21. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 2005, 5:375-386.
22. Rajsbaum R., García-Sastre A., Versteeg G.A. TRIMmunity: the roles of the TRIM E3-ubiquitin ligase family in innate antiviral immunity. J.Mol. Biol. 2014, 426:1265-1284.
23. Reyes-Turcu F.E., Horton J.R., Mullally J.E., Heroux A., Cheng X., Wilkinson K.D. The ubiquitin binding domain ZnF UBP recognizes the C-terminal diglycine motif of unanchored ubiquitin. Cell 2006, 124:1197-1208.
24. Reymond A., Meroni G., Fantozzi A., Merla G., Cairo S., Luzi L., Riganelli D., Zanaria E., Messali S., Cainarca S., et al. The tripartite motif family identifies cell compartments. EMBO J. 2001, 20:2140-2151.
25. Sharma S., tenOever B.R., Grandvaux N., Zhou G.P., Lin R., Hiscott J. Triggering the interferon antiviral response through an IKK-related pathway. Science 2003, 300:1148-1151.
26. Shin D.Y., Lee H., Park E.S., Yoo Y.J. Assembly of different length of polyubiquitins on the catalytic cysteine of E2 enzymes without E3 ligase; a novel application of non-reduced/reduced 2-dimensional electrophoresis. FEBS Lett. 2011, 585:3959-3963.
27. Shuai K., Ziemiecki A., Wilks A.F., Harpur A.G., Sadowski H.B., Gilman M.Z., Darnell J.E. Polypeptide signalling to the nucleus through tyrosine phosphorylation of Jak and Stat proteins. Nature 1993, 366:580-583.
28. Talon J., Horvath C.M., Polley R., Basler C.F., Muster T., Palese P., García-Sastre A. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. J.Virol. 2000, 74:7989-7996.
29. Tenoever B.R., Ng S.L., Chua M.A., McWhirter S.M., García-Sastre A., Maniatis T. Multiple functions of the IKK-related kinase IKKepsilon in interferon-mediated antiviral immunity. Science 2007, 315:1274-1278.
30. Trempe J.F. Reading the ubiquitin postal code. Curr. Opin. Struct. Biol. 2011, 21:792-801.
31. Uchil P.D., Hinz A., Siegel S., Coenen-Stass A., Pertel T., Luban J., Mothes W. TRIM protein-mediated regulation of inflammatory and innate immune signaling and its association with antiretroviral activity. J.Virol. 2013, 87:257-272.
32. Versteeg G.A., Rajsbaum R., Sánchez-Aparicio M.T., Maestre A.M., Valdiviezo J., Shi M., Inn K.S., Fernandez-Sesma A., Jung J., García-Sastre A. The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune pattern-recognition receptors. Immunity 2013, 38:384-398.
33. Wilson R.C., Edmondson S.P., Flatt J.W., Helms K., Twigg P.D. The E2-25K ubiquitin-associated (UBA) domain aids in polyubiquitin chain synthesis and linkage specificity. Biochem. Biophys. Res. Commun. 2011, 405:662-666.
34. Xia Z.P., Sun L., Chen X., Pineda G., Jiang X., Adhikari A., Zeng W., Chen Z.J. Direct activation of protein kinases by unanchored polyubiquitin chains. Nature 2009, 461:114-119.
35. Yamamoto M., Sato S., Hemmi H., Hoshino K., Kaisho T., Sanjo H., Takeuchi O., Sugiyama M., Okabe M., Takeda K., Akira S. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003, 301:640-643.
36. Zeng W., Sun L., Jiang X., Chen X., Hou F., Adhikari A., Xu M., Chen Z.J. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 2010, 141:315-330.