Viral evasion mechanisms of early antiviral responses involving regulation of ubiquitin pathways

Trends in Microbiology

Volumn 21, Issue 8, 2013, Pages 421-429

  Rajsbaum, Ricardo ^a   García Sastre, Adolfo ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Antiviral; Evasion of innate immunity; Restriction factors; Ubiquitin system

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE; CYTOKINE; HYDROLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; RETINOIC ACID INDUCIBLE PROTEIN I; STAT PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AUTOPHAGY; CORONAVIRUS; DEUBIQUITINATION; EPSTEIN BARR VIRUS; FOOT AND MOUTH DISEASE VIRUS; HOST CELL; HUMAN; HUMAN HERPESVIRUS 8; IMMUNE EVASION; INNATE IMMUNITY; MURINE HEPATITIS CORONAVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INDUCTION; PROTEIN MODIFICATION; REVIEW; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS INHIBITION; VIRUS REPLICATION;

ANTIVIRAL; EVASION OF INNATE IMMUNITY; RESTRICTION FACTORS; UBIQUITIN SYSTEM;

ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; UBIQUITIN; VIRAL PROTEINS; VIRUS PHYSIOLOGICAL PHENOMENA; VIRUSES;

EID: 84881030086     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2013.06.006     Document Type: Review

References (105)

1. de Weerd N.A., Nguyen T. The interferons and their receptors - distribution and regulation. Immunol. Cell Biol. 2012, 90:483-491.
2. Thompson M.R., et al. Pattern recognition receptors and the innate immune response to viral infection. Viruses 2011, 3:920-940.
3. Oudshoorn D., et al. Regulation of the innate immune system by ubiquitin and ubiquitin-like modifiers. Cytokine Growth Factor Rev. 2012, 23:273-282.
4. Kanarek N., Ben-Neriah Y. Regulation of NF-kappaB by ubiquitination and degradation of the IkappaBs. Immunol. Rev. 2012, 246:77-94.
5. Versteeg G.A., Garcia-Sastre A. Viral tricks to grid-lock the type I interferon system. Curr. Opin. Microbiol. 2010, 13:508-516.
6. Taylor K.E., Mossman K.L. Recent advances in understanding viral evasion of type I interferon. Immunology 2013, 138:190-197.
7. Randles L., Walters K.J. Ubiquitin and its binding domains. Front. Biosci. 2012, 17:2140-2157.
8. Trempe J.F. Reading the ubiquitin postal code. Curr. Opin. Struct. Biol. 2011, 21:792-801.
9. Zeng W., et al. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 2010, 141:315-330.
10. Wodrich H., et al. A capsid-encoded PPxY-motif facilitates adenovirus entry. PLoS Pathog. 2010, 6:e1000808.
11. van Kasteren P.B., et al. Deubiquitinase function of arterivirus papain-like protease 2 suppresses the innate immune response in infected host cells. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E838-E847.
12. van Kasteren P.B., et al. Arterivirus and nairovirus ovarian tumor domain-containing Deubiquitinases target activated RIG-I to control innate immune signaling. J. Virol. 2012, 86:773-785.
13. Frias-Staheli N., et al. Ovarian tumor domain-containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2007, 2:404-416.
14. Zheng D., et al. PLP2, a potent deubiquitinase from murine hepatitis virus, strongly inhibits cellular type I interferon production. Cell Res. 2008, 18:1105-1113.
15. Saito S., et al. Epstein-Barr virus deubiquitinase downregulates TRAF6-mediated NF-kappaB signaling during productive replication. J. Virol. 2013, 87:4060-4070.
16. Inn K.S., et al. Inhibition of RIG-I-mediated signaling by Kaposi's sarcoma-associated herpesvirus-encoded deubiquitinase ORF64. J. Virol. 2011, 85:10899-10904.
17. Wang D., et al. The leader proteinase of foot-and-mouth disease virus negatively regulates the type I interferon pathway by acting as a viral deubiquitinase. J. Virol. 2011, 85:3758-3766.
18. Gack M.U., et al. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 2009, 5:439-449.
19. Rajsbaum R., et al. Species-specific inhibition of RIG-I ubiquitination and IFN induction by the influenza A virus NS1 protein. PLoS Pathog. 2012, 8:e1003059.
20. Barber M.R., et al. Association of RIG-I with innate immunity of ducks to influenza. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:5913-5918.
21. Duggal N.K., Emerman M. Evolutionary conflicts between viruses and restriction factors shape immunity. Nat. Rev. Immunol. 2012, 12:687-695.
22. Bishop K.N., et al. APOBEC-mediated editing of viral RNA. Science 2004, 305:645.
23. Harris R.S., et al. The restriction factors of human immunodeficiency virus. J. Biol. Chem. 2012, 287:40875-40883.
24. Yu X., et al. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 2003, 302:1056-1060.
25. Ahn J., et al. HIV/simian immunodeficiency virus (SIV) accessory virulence factor Vpx loads the host cell restriction factor SAMHD1 onto the E3 ubiquitin ligase complex CRL4DCAF1. J. Biol. Chem. 2012, 287:12550-12558.
26. Lahouassa H., et al. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat. Immunol. 2012, 13:223-228.
27. Swiecki M., et al. BST-2/tetherin: structural biology, viral antagonism, and immunobiology of a potent host antiviral factor. Mol. Immunol. 2013, 54:132-139.
28. Cao W., et al. Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. J. Exp. Med. 2009, 206:1603-1614.
29. Mitchell R.S., et al. Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog. 2009, 5:e1000450.
30. Douglas J.L., et al. Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a βTrCP-dependent mechanism. J. Virol. 2009, 83:7931-7947.
31. Jia B., et al. Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog. 2009, 5:e1000429.
32. Hauser H., et al. HIV-1 Vpu and HIV-2 Env counteract BST-2/tetherin by sequestration in a perinuclear compartment. Retrovirology 2010, 7:51.
33. Kaletsky R.L., et al. Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2886-2891.
34. Yondola M.A., et al. Budding capability of the influenza virus neuraminidase can be modulated by tetherin. J. Virol. 2011, 85:2480-2491.
35. Mangeat B., et al. Influenza virus partially counteracts restriction imposed by tetherin/BST-2. J. Biol. Chem. 2012, 287:22015-22029.
36. Sarras H., et al. In search of a function for BCLAF1. ScientificWorldJournal 2010, 10:1450-1461.
37. Hwang J., Kalejta R.F. Proteasome-dependent, ubiquitin-independent degradation of Daxx by the viral pp71 protein in human cytomegalovirus-infected cells. Virology 2007, 367:334-338.
38. Salsman J., et al. Proteomic profiling of the human cytomegalovirus UL35 gene products reveals a role for UL35 in the DNA repair response. J. Virol. 2012, 86:806-820.
39. Saffert R.T., Kalejta R.F. Human cytomegalovirus gene expression is silenced by Daxx-mediated intrinsic immune defense in model latent infections established in vitro. J. Virol. 2007, 81:9109-9120.
40. Lukashchuk V., et al. Human cytomegalovirus protein pp71 displaces the chromatin-associated factor ATRX from nuclear domain 10 at early stages of infection. J. Virol. 2008, 82:12543-12554.
41. Winkler L.L., et al. Ubiquitin-independent proteasomal degradation of tumor suppressors by human cytomegalovirus pp71 requires the 19S regulatory particle. J. Virol. 2013, 87:4665-4671.
42. Lee S.H., et al. BclAF1 restriction factor is neutralized by proteasomal degradation and microRNA repression during human cytomegalovirus infection. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:9575-9580.
43. Rodriguez-Madoz J.R., et al. Inhibition of the type I interferon response in human dendritic cells by dengue virus infection requires a catalytically active NS2B3 complex. J. Virol. 2010, 84:9760-9774.
44. Morrison J., et al. Dengue virus co-opts UBR4 to degrade STAT2 and antagonize type I interferon signaling. PLoS Pathog. 2013, 9:e1003265.
45. Stevenson N.J., et al. Hepatitis C virus targets the interferon-alpha JAK/STAT pathway by promoting proteasomal degradation in immune cells and hepatocytes. FEBS Lett. 2013, 587:1571-1578.
46. Le V.T., et al. Human cytomegalovirus interferes with signal transducer and activator of transcription (STAT) 2 protein stability and tyrosine phosphorylation. J. Gen. Virol. 2008, 89:2416-2426.
47. Kadeppagari R.K., et al. HSV-2 inhibits type-I interferon signaling via multiple complementary and compensatory STAT2-associated mechanisms. Virus Res. 2012, 167:273-284.
48. Ramachandran A., Horvath C.M. Paramyxovirus disruption of interferon signal transduction: STATus report. J. Interferon Cytokine Res. 2009, 29:531-537.
49. Elliott J., et al. Respiratory syncytial virus NS1 protein degrades STAT2 by using the Elongin-Cullin E3 ligase. J. Virol. 2007, 81:3428-3436.
50. Stremlau M., et al. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004, 427:848-853.
51. Sastri J., Campbell E.M. Recent insights into the mechanism and consequences of TRIM5alpha retroviral restriction. AIDS Res. Hum. Retroviruses 2011, 27:231-238.
52. Pertel T., et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011, 472:361-365.
53. Hatziioannou T., et al. Generation of simian-tropic HIV-1 by restriction factor evasion. Science 2006, 314:95.
54. Uchil P.D., et al. TRIM E3 ligases interfere with early and late stages of the retroviral life cycle. PLoS Pathog. 2008, 4:e16.
55. Han K., et al. Identification of a genomic reservoir for new TRIM genes in primate genomes. PLoS Genet. 2011, 7:e1002388.
56. Versteeg G.A., et al. The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune pattern-recognition receptors. Immunity 2013, 38:384-398.
57. Uchil P.D., et al. TRIM protein-mediated regulation of inflammatory and innate immune signaling and its association with antiretroviral activity. J. Virol. 2013, 87:257-272.
58. Rajsbaum R., et al. Type I interferon-dependent and -independent expression of tripartite motif proteins in immune cells. Eur. J. Immunol. 2008, 38:619-630.
59. Geoffroy M.C., Chelbi-Alix M.K. Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res. 2011, 31:145-158.
60. Boutell C., et al. A viral ubiquitin ligase has substrate preferential SUMO targeted ubiquitin ligase activity that counteracts intrinsic antiviral defence. PLoS Pathog. 2011, 7:e1002245.
61. Cuchet-Lourenco D., et al. Herpes simplex virus 1 ubiquitin ligase ICP0 interacts with PML isoform I and induces its SUMO-independent degradation. J. Virol. 2012, 86:11209-11222.
62. El McHichi B., et al. SUMOylation promotes PML degradation during encephalomyocarditis virus infection. J. Virol. 2010, 84:11634-11645.
63. Zhang Z., et al. The E3 ubiquitin ligase TRIM21 negatively regulates the innate immune response to intracellular double-stranded DNA. Nat. Immunol. 2013, 14:172-178.
64. Tsuchida T., et al. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 2010, 33:765-776.
65. Zhang J., et al. TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked ubiquitination. J. Biol. Chem. 2012, 287:28646-28655.
66. Poole E., et al. Identification of TRIM23 as a cofactor involved in the regulation of NF-kappaB by human cytomegalovirus. J. Virol. 2009, 83:3581-3590.
67. Arimoto K., et al. Polyubiquitin conjugation to NEMO by triparite motif protein 23 (TRIM23) is critical in antiviral defense. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15856-15861.
68. Cocka L.J., Bates P. Identification of alternatively translated Tetherin isoforms with differing antiviral and signaling activities. PLoS Pathog. 2012, 8:e1002931.
69. Galao R.P., et al. Innate sensing of HIV-1 assembly by Tetherin induces NFkappaB-dependent proinflammatory responses. Cell Host Microbe 2012, 12:633-644.
70. Tokarev A., et al. Stimulation of NF-kappaB activity by the HIV restriction factor BST2. J. Virol. 2013, 87:2046-2057.
71. Pichlmair A., et al. IFIT1 is an antiviral protein that recognizes 5'-triphosphate RNA. Nat. Immunol. 2011, 12:624-630.
72. Diamond M.S., Farzan M. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat. Rev. Immunol. 2013, 13:46-57.
73. Liu X.Y., et al. IFN-induced TPR protein IFIT3 potentiates antiviral signaling by bridging MAVS and TBK1. J. Immunol. 2011, 187:2559-2568.
74. Skaug B., Chen Z.J. Emerging role of ISG15 in antiviral immunity. Cell 2010, 143:187-190.
75. Wimmer P., et al. Human pathogens and the host cell SUMOylation system. J. Virol. 2012, 86:642-654.
76. van der Veen A.G., Ploegh H.L. Ubiquitin-like proteins. Annu. Rev. Biochem. 2012, 81:323-357.
77. Zhao C., et al. Interferon-induced ISG15 pathway: an ongoing virus-host battle. Trends Microbiol. 2013, 21:181-186.
78. Guerra S., et al. Vaccinia virus E3 protein prevents the antiviral action of ISG15. PLoS Pathog. 2008, 4:e1000096.
79. Yuan W., Krug R.M. Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 2001, 20:362-371.
80. Versteeg G.A., et al. Species-specific antagonism of host ISGylation by the influenza B virus NS1 protein. J. Virol. 2010, 84:5423-5430.
81. Sridharan H., et al. Species specificity of the NS1 protein of influenza B virus: NS1 binds only human and non-human primate ubiquitin-like ISG15 proteins. J. Biol. Chem. 2010, 285:7852-7856.
82. Kawaguchi Y., et al. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 2003, 115:727-738.
83. Kirkin V., et al. A role for ubiquitin in selective autophagy. Mol. Cell 2009, 34:259-269.
84. Lamark T., et al. NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets. Cell Cycle 2009, 8:1986-1990.
85. Komatsu M., et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007, 131:1149-1163.
86. Jo E.K., et al. Roles of autophagy in elimination of intracellular bacterial pathogens. Front. Immunol. 2013, 4:97.
87. Jordan T.X., Randall G. Manipulation or capitulation: virus interactions with autophagy. Microbes Infect. 2012, 14:126-139.
88. Yordy B., Iwasaki A. Autophagy in the control and pathogenesis of viral infection. Curr. Opin. Virol. 2011, 1:196-203.
89. Orvedahl A., et al. Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 2010, 7:115-127.
90. Xu Y., et al. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 2007, 27:135-144.
91. Shi C.S., Kehrl J.H. MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J. Biol. Chem. 2008, 283:33175-33182.
92. Geng J., Klionsky D.J. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep. 2008, 9:859-864.
93. Fliss P.M., et al. Viral mediated redirection of NEMO/IKKgamma to autophagosomes curtails the inflammatory cascade. PLoS Pathog. 2012, 8:e1002517.
94. Ku B., et al. Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine gamma-herpesvirus 68. PLoS Pathog. 2008, 4:e25.
95. Kihara A., et al. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2001, 2:330-335.
96. Kyei G.B., et al. Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J. Cell Biol. 2009, 186:255-268.
97. Zeng X., Carlin C.R. Host cell autophagy modulates early stages of adenovirus infections in airway epithelial cells. J. Virol. 2013, 87:2307-2319.
98. Shoji-Kawata S., et al. Identification of a candidate therapeutic autophagy-inducing peptide. Nature 2013, 494:201-206.
99. Jin R., et al. Japanese encephalitis virus activates autophagy as a viral immune evasion strategy. PLoS ONE 2013, 8:e52909.
100. Zhu H., et al. Varicella-zoster virus immediate-early protein ORF61 abrogates the IRF3-mediated innate immune response through degradation of activated IRF3. J. Virol. 2011, 85:11079-11089.
101. Wang L., et al. Disruption of PML nuclear bodies is mediated by ORF61 SUMO-interacting motifs and required for varicella-zoster virus pathogenesis in skin. PLoS Pathog. 2011, 7:e1002157.
102. Boname J.M., et al. Efficient internalization of MHC I requires lysine-11 and lysine-63 mixed linkage polyubiquitin chains. Traffic 2011, 11:210-220.
103. Boutell C., Everett R.D. Regulation of alphaherpesvirus infections by the ICP0 family of proteins. J. Gen. Virol. 2013, 94:465-481.
104. Zhang L., et al. Interplay between poxviruses and the cellular ubiquitin/ubiquitin-like pathways. FEBS Lett. 2009, 583:607-614.
105. Gupta R., et al. Ubiquitination screen using protein microarrays for comprehensive identification of Rsp5 substrates in yeast. Mol. Syst. Biol. 2007, 3:116.