Putting the brakes on the anti-viral response: Negative regulators of type I interferon (IFN) production

Microbes and Infection

Volumn 13, Issue 4, 2011, Pages 291-302

  Richards, Kathryn H ^a   Macdonald, Andrew ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Interferon; Negative regulation; Virus

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN TAB1; ADAPTOR PROTEIN TAB2; ADAPTOR PROTEIN TAB3; ADAPTOR PROTEIN TAK1; ALPHA INTERFERON; BETA INTERFERON; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 8; I KAPPA B KINASE EPSILON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; MITOFUSIN 2; MYELOID DIFFERENTIATION FACTOR 88; POLO LIKE KINASE 1; PROTEIN IPS 1; PROTEIN MDA 5; PROTEIN SERINE THREONINE KINASE; PROTEIN TBK1; REGULATOR PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; SMALL CYTOPLASMIC RNA; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TRIPARTITE MOTIF PROTEIN 21; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VIRUS RNA;

ANTIOXIDANT ACTIVITY; ANTIVIRAL ACTIVITY; CALICIVIRUS; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; HEPATITIS C VIRUS; HUMAN; IMMUNOREGULATION; INFLUENZA VIRUS A; NONHUMAN; PICORNAVIRUS; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SENDAI VIRUS; SHORT SURVEY; SIGNAL TRANSDUCTION; VIRUS GENOME; VIRUS IMMUNITY; VIRUS INFECTION; VIRUS PARTICLE;

ANIMALS; CYTOPLASM; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; IMMUNOMODULATION; INTERFERON REGULATORY FACTORS; INTERFERON TYPE I; PROTEIN-SERINE-THREONINE KINASES; RNA, VIRAL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; VIRUS DISEASES; VIRUSES;

EID: 79952446319     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2010.12.007     Document Type: Short Survey

References (72)

1. Theofilopoulos A.N., Baccala R., Beutler B., Kono D.H. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu. Rev. Immunol. 2005, 23:307-336.
2. Kawai T., Akira S. Antiviral signaling through pattern recognition receptors. J. Biochem. 2007, 141:137-145.
3. Kawai T., Akira S. Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 2008, 1143:1-20.
4. Liew F.Y., Xu D., Brint E.K., O'Neill L.A. Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 2005, 5:446-458.
5. McGettrick A.F., O'Neill L.A. Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr. Opin. Immunol. 2010, 22:20-27.
6. Barton G.M., Kagan J.C. A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 2009, 9:535-542.
7. Sasai M., Linehan M.M., Iwasaki A. Bifurcation of Toll-like receptor 9 signaling by adaptor protein 3. Science 2010, 329:1530-1534.
8. Chuang T.H., Ulevitch R.J. Triad3A, an E3 ubiquitin-protein ligase regulating Toll-like receptors. Nat. Immunol. 2004, 5:495-502.
9. Yao M., Liu X., Li D., Chen T., Cai Z., Cao X. Late endosome/lysosome-localized Rab7b suppresses TLR9-initiated proinflammatory cytokine and type I IFN production in macrophages. J. Immunol. 2009, 183:1751-1758.
10. Kenny E.F., O'Neill L.A. Signalling adaptors used by Toll-like receptors: an update. Cytokine 2008, 43:342-349.
11. Wertz I.E., Dixit V.M. Signaling to NF-kappaB: regulation by ubiquitination. Cold Spring Harb Perspect. Biol. 2010, 2:a003350.
12. Wald D., Qin J., Zhao Z., Qian Y., Naramura M., Tian L., Towne J., Sims J.E., Stark G.R., Li X. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat. Immunol. 2003, 4:920-927.
13. Brint E.K., Xu D., Liu H., Dunne A., McKenzie A.N., O'Neill L.A., Liew F.Y. ST2 is an inhibitor of interleukin 1 receptor and Toll-like receptor 4 signaling and maintains endotoxin tolerance. Nat. Immunol. 2004, 5:373-379.
14. Burns K., Janssens S., Brissoni B., Olivos N., Beyaert R., Tschopp J. Inhibition of interleukin 1 receptor/Toll-like receptor signaling through the alternatively spliced, short form of MyD88 is due to its failure to recruit IRAK-4. J. Exp. Med. 2003, 197:263-268.
15. Carty M., Goodbody R., Schroder M., Stack J., Moynagh P.N., Bowie A.G. The human adaptor SARM negatively regulates adaptor protein TRIF-dependent Toll-like receptor signaling. Nat. Immunol. 2006, 7:1074-1081.
16. Into T., Inomata M., Niida S., Murakami Y., Shibata K.I. Regulation of MyD88 aggregation and the MyD88-dependent signaling pathway by sequestosome 1 and histone deacetylase 6. J. Biol. Chem. 2010, 285:35759-35769.
17. Su X., Li S., Meng M., Qian W., Xie W., Chen D., Zhai Z., Shu H.B. TNF receptor-associated factor-1 (TRAF1) negatively regulates Toll/IL-1 receptor domain-containing adaptor inducing IFN-beta (TRIF)-mediated signaling. Eur. J. Immunol. 2006, 36:199-206.
18. Wilkins C., Gale M. Recognition of viruses by cytoplasmic sensors. Curr. Opin. Immunol. 2010, 22:41-47.
19. Saito T., Gale M. Differential recognition of double-stranded RNA by RIG-I-like receptors in antiviral immunity. J. Exp. Med. 2008, 205:1523-1527.
20. Loo Y.M., Fornek J., Crochet N., Bajwa G., Perwitasari O., Martinez-Sobrido L., Akira S., Gill M.A., Garcia-Sastre A., Katze M.G., Gale M. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 2008, 82:335-345.
21. Rehwinkel J., Reis e Sousa C. RIGorous detection: exposing virus through RNA sensing. Science 2010, 327:284-286.
22. Pichlmair A., Schulz O., Tan C.P., Rehwinkel J., Kato H., Takeuchi O., Akira S., Way M., Schiavo G., Reis e Sousa C. Activation of MDA5 requires higher-order RNA structures generated during virus infection. J. Virol. 2009, 83:10761-10769.
23. Venkataraman T., Valdes M., Elsby R., Kakuta S., Caceres G., Saijo S., Iwakura Y., Barber G.N. Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J. Immunol. 2007, 178:6444-6455.
24. Nistal-Villan E., Gack M.U., Martinez-Delgado G., Maharaj N.P., Inn K.S., Yang H., Wang R., Aggarwal A.K., Jung J.U., Garcia-Sastre A. Negative role of RIG-I serine 8 phosphorylation in the regulation of interferon-beta production. J. Biol. Chem. 2010, 285:20252-20261.
25. Gack M.U., Nistal-Villan E., Inn K.S., Garcia-Sastre A., Jung J.U. Phosphorylation-mediated negative regulation of RIG-I antiviral activity. J. Virol. 2010, 84:3220-3229.
26. Friedman C.S., O'Donnell M.A., Legarda-Addison D., Ng A., Cardenas W.B., Yount J.S., Moran T.M., Basler C.F., Komuro A., Horvath C.M., Xavier R., Ting A.T. The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep. 2008, 9:930-936.
27. Arimoto K., Takahashi H., Hishiki T., Konishi H., Fujita T., Shimotohno K. Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:7500-7505.
28. Kim M.J., Hwang S.Y., Imaizumi T., Yoo J.Y. Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. J. Virol. 2008, 82:1474-1483.
29. Diao F., Li S., Tian Y., Zhang M., Xu L.G., Zhang Y., Wang R.P., Chen D., Zhai Z., Zhong B., Tien P., Shu H.B. Negative regulation of MDA5- but not RIG-I-mediated innate antiviral signaling by the dihydroxyacetone kinase. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11706-11711.
30. Scott I. The role of mitochondria in the mammalian antiviral defense system. Mitochondrion 2010, 10:316-320.
31. Seth R.B., Sun L., Ea C.K., Chen Z.J. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 2005, 122:669-682.
32. Tal M.C., Sasai M., Lee H.K., Yordy B., Shadel G.S., Iwasaki A. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2770-2775.
33. Tal M.C., Iwasaki A. Autophagic control of RLR signaling. Autophagy 2009, 5:749-750.
34. Jounai N., Takeshita F., Kobiyama K., Sawano A., Miyawaki A., Xin K.Q., Ishii K.J., Kawai T., Akira S., Suzuki K., Okuda K. The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14050-14055.
35. Vitour D., Dabo S., Ahmadi Pour M., Vilasco M., Vidalain P.O., Jacob Y., Mezel-Lemoine M., Paz S., Arguello M., Lin R., Tangy F., Hiscott J., Meurs E.F. Polo-like kinase 1 (PLK1) regulates interferon (IFN) induction by MAVS. J. Biol. Chem. 2009, 284:21797-21809.
36. Yasukawa K., Oshiumi H., Takeda M., Ishihara N., Yanagi Y., Seya T., Kawabata S., Koshiba T. Mitofusin 2 inhibits mitochondrial antiviral signaling. Sci. Signal. 2009, 2:ra47.
37. Moore C.B., Bergstralh D.T., Duncan J.A., Lei Y., Morrison T.E., Zimmermann A.G., Accavitti-Loper M.A., Madden V.J., Sun L., Ye Z., Lich J.D., Heise M.T., Chen Z., Ting J.P. NLRX1 is a regulator of mitochondrial antiviral immunity. Nature 2008, 451:573-577.
38. Xu L., Xiao N., Liu F., Ren H., Gu J. Inhibition of RIG-I and MDA5-dependent antiviral response by gC1qR at mitochondria. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1530-1535.
39. Meylan E., Tschopp J. NLRX1: friend or foe?. EMBO Rep. 2008, 9:243-245.
40. You F., Sun H., Zhou X., Sun W., Liang S., Zhai Z., Jiang Z. PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat. Immunol. 2009, 10:1300-1308.
41. Jia Y., Song T., Wei C., Ni C., Zheng Z., Xu Q., Ma H., Li L., Zhang Y., He X., Xu Y., Shi W., Zhong H. Negative regulation of MAVS-mediated innate immune response by PSMA7. J. Immunol. 2009, 183:4241-4248.
42. Singhal S., Taylor M.C., Baker R.T. Deubiquitylating enzymes and disease. BMC Biochem. 2008, 9(Suppl. 1):S3.
43. Kovalenko A., Chable-Bessia C., Cantarella G., Israel A., Wallach D., Courtois G. The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 2003, 424:801-805.
44. Hymowitz S.G., Wertz I.E. A20: from ubiquitin editing to tumour suppression. Nat. Rev. Cancer 2010, 10:332-341.
45. Li S., Zheng H., Mao A.P., Zhong B., Li Y., Liu Y., Gao Y., Ran Y., Tien P., Shu H.B. Regulation of virus-triggered signaling by OTUB1- and OTUB2-mediated deubiquitination of TRAF3 and TRAF6. J. Biol. Chem. 2010, 285:4291-4297.
46. Sanada T., Takaesu G., Mashima R., Yoshida R., Kobayashi T., Yoshimura A. FLN29 deficiency reveals its negative regulatory role in the Toll-like receptor (TLR) and retinoic acid-inducible gene I (RIG-I)-like helicase signaling pathway. J. Biol. Chem. 2008, 283:33858-33864.
47. Kawagoe T., Takeuchi O., Takabatake Y., Kato H., Isaka Y., Tsujimura T., Akira S. TANK is a negative regulator of Toll-like receptor signaling and is critical for the prevention of autoimmune nephritis. Nat. Immunol. 2009, 10:965-972.
48. Zhu G., Wu C.J., Zhao Y., Ashwell J.D. Optineurin negatively regulates TNFalpha- induced NF-kappaB activation by competing with NEMO for ubiquitinated RIP. Curr. Biol. 2007, 17:1438-1443.
49. Mankouri J., Fragkoudis R., Richards K.H., Wetherill L.F., Harris M., Kohl A., Elliott R.M., Macdonald A. Optineurin negatively regulates the induction of IFNbeta in response to RNA virus infection. PLoS Pathog. 2010, 6:e1000778.
50. Shi M., Deng W., Bi E., Mao K., Ji Y., Lin G., Wu X., Tao Z., Li Z., Cai X., Sun S., Xiang C., Sun B. TRIM30 alpha negatively regulates TLR-mediated NF-kappa B activation by targeting TAB2 and TAB3 for degradation. Nat. Immunol. 2008, 9:369-377.
51. Cui J., Zhu L., Xia X., Wang H.Y., Legras X., Hong J., Ji J., Shen P., Zheng S., Chen Z.J., Wang R.F. NLRC5 negatively regulates the NF-kappaB and type I interferon signaling pathways. Cell 2010, 141:483-496.
52. McWhirter S.M., Fitzgerald K.A., Rosains J., Rowe D.C., Golenbock D.T., Maniatis T. IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:233-238.
53. Fitzgerald K.A., McWhirter S.M., Faia K.L., Rowe D.C., Latz E., Golenbock D.T., Coyle A.J., Liao S.M., Maniatis T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003, 4:491-496.
54. Chau T.L., Gioia R., Gatot J.S., Patrascu F., Carpentier I., Chapelle J.P., O'Neill L., Beyaert R., Piette J., Chariot A. Are the IKKs and IKK-related kinases TBK1 and IKK-epsilon similarly activated?. Trends Biochem. Sci. 2008, 33:171-180.
55. Wang C., Chen T., Zhang J., Yang M., Li N., Xu X., Cao X. The E3 ubiquitin ligase Nrdp1 'preferentially' promotes TLR-mediated production of type I interferon. Nat. Immunol. 2009, 10:744-752.
56. 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.
57. Clark K., Plater L., Peggie M., Cohen P. Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IkappaB kinase epsilon: a distinct upstream kinase mediates Ser-172 phosphorylation and activation. J. Biol. Chem. 2009, 284:14136-14146.
58. Gabhann J.N., Higgs R., Brennan K., Thomas W., Damen J.E., Ben Larbi N., Krystal G., Jefferies C.A. Absence of SHIP-1 results in constitutive phosphorylation of tank-binding kinase 1 and enhanced TLR3-dependent IFN-beta production. J. Immunol. 2010, 184:2314-2320.
59. Nakhaei P., Mesplede T., Solis M., Sun Q., Zhao T., Yang L., Chuang T.H., Ware C.F., Lin R., Hiscott J. The E3 ubiquitin ligase Triad3A negatively regulates the RIG-I/MAVS signaling pathway by targeting TRAF3 for degradation. PLoS Pathog. 2009, 5:e1000650.
60. Kayagaki N., Phung Q., Chan S., Chaudhari R., Quan C., O'Rourke K.M., Eby M., Pietras E., Cheng G., Bazan J.F., Zhang Z., Arnott D., Dixit V.M. DUBA: a deubiquitinase that regulates type I interferon production. Science 2007, 318:1628-1632.
61. Huang J., Liu T., Xu L.G., Chen D., Zhai Z., Shu H.B. SIKE is an IKK epsilon/TBK1-associated suppressor of TLR3- and virus-triggered IRF-3 activation pathways. EMBO J. 2005, 24:4018-4028.
62. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S.P., Elledge S.J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
63. Saitoh T., Tun-Kyi A., Ryo A., Yamamoto M., Finn G., Fujita T., Akira S., Yamamoto N., Lu K.P., Yamaoka S. Negative regulation of interferon-regulatory factor 3-dependent innate antiviral response by the prolyl isomerase Pin1. Nat. Immunol. 2006, 7:598-605.
64. Zhang M., Tian Y., Wang R.P., Gao D., Zhang Y., Diao F.C., Chen D.Y., Zhai Z.H., Shu H.B. Negative feedback regulation of cellular antiviral signaling by RBCK1-mediated degradation of IRF3. Cell Res. 2008, 18:1096-1104.
65. Bibeau-Poirier A., Gravel S.P., Clement J.F., Rolland S., Rodier G., Coulombe P., Hiscott J., Grandvaux N., Meloche S., Servant M.J. Involvement of the IkappaB kinase (IKK)-related kinases tank-binding kinase 1/IKKi and cullin-based ubiquitin ligases in IFN regulatory factor-3 degradation. J. Immunol. 2006, 177:5059-5067.
66. Higgs R., Ni Gabhann J., Ben Larbi N., Breen E.P., Fitzgerald K.A., Jefferies C.A. The E3 ubiquitin ligase Ro52 negatively regulates IFN-beta production post-pathogen recognition by polyubiquitin-mediated degradation of IRF3. J. Immunol. 2008, 181:1780-1786.
67. Espinosa A., Dardalhon V., Brauner S., Ambrosi A., Higgs R., Quintana F.J., Sjostrand M., Eloranta M.L., Ni Gabhann J., Winqvist O., Sundelin B., Jefferies C.A., Rozell B., Kuchroo V.K., Wahren-Herlenius M. Loss of the lupus autoantigen Ro52/Trim21 induces tissue inflammation and systemic autoimmunity by disregulating the IL-23-Th17 pathway. J. Exp. Med. 2009, 206:1661-1671.
68. Yoshimi R., Chang T.H., Wang H., Atsumi T., Morse H.C., Ozato K. Gene disruption study reveals a nonredundant role for TRIM21/Ro52 in NF-kappaB-dependent cytokine expression in fibroblasts. J. Immunol. 2009, 182:7527-7538.
69. Kubota T., Matsuoka M., Chang T.H., Tailor P., Sasaki T., Tashiro M., Kato A., Ozato K. Virus infection triggers SUMOylation of IRF3 and IRF7, leading to the negative regulation of type I interferon gene expression. J. Biol. Chem. 2008, 283:25660-25670.
70. Nusinzon I., Horvath C.M. Positive and negative regulation of the innate antiviral response and beta interferon gene expression by deacetylation. Mol. Cell Biol. 2006, 26:3106-3113.
71. Kim H., Seed B. The transcription factor MafB antagonizes antiviral responses by blocking recruitment of coactivators to the transcription factor IRF3. Nat. Immunol. 2010, 11:743-750.
72. Heyninck K., Beyaert R. A20 inhibits NF-kappaB activation by dual ubiquitin-editing functions. Trends Biochem. Sci. 2005, 30:1-4.