Viral hijacking of the host ubiquitin system to evade interferon responses

Current Opinion in Microbiology

Volumn 13, Issue 4, 2010, Pages 517-523

  Viswanathan, Kasinath ^a   Früh, Klaus ^a   DeFilippis, Victor ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; BONE MARROW STROMAL ANTIGEN 2; IMMUNOGLOBULIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; ISG15; MEMBRANE PROTEIN; PROTEASOME; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN;

ADAPTIVE IMMUNITY; ANTIVIRAL ACTIVITY; BOVINE DIARRHEA VIRUS; CYTOKINE PRODUCTION; DENGUE VIRUS; EBOLA VIRUS; ENZYME INHIBITION; HOST RESISTANCE; IMMUNE RESPONSE; INNATE IMMUNITY; LASSA VIRUS; LENTIVIRINAE; MOLECULE; NONHUMAN; PATHOGENESIS; PESTIVIRUS; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; REGULATORY MECHANISM; RETROVIRUS; REVIEW; ROTAVIRUS; SIGNAL TRANSDUCTION; UBIQUITINATION; VIRUS ENTRY; VIRUS INFECTION; VIRUS REPLICATION;

HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; INTERFERONS; SIGNAL TRANSDUCTION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; UBIQUITINS; VIRUS DISEASES; VIRUSES;

EID: 77955427276     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2010.05.012     Document Type: Review

References (70)

1. Cadwell K., Coscoy L. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 2005, 309:127-130.
2. Wang X., Herr R.A., Chua W.J., Lybarger L., Wiertz E.J., Hansen T.H. Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J Cell Biol 2007, 177:613-624.
3. Isaacson M.K., Ploegh H.L. Ubiquitination, ubiquitin-like modifiers, and deubiquitination in viral infection. Cell Host Microbe 2009, 5:559-570.
4. Randow F., Lehner P.J. Viral avoidance and exploitation of the ubiquitin system. Nat Cell Biol 2009, 11:527-534.
5. Yu G.-Y., Lai M.M.C. The ubiquitin-proteasome system facilitates the transfer of murine coronavirus from endosome to cytoplasm during virus entry. J Virol 2005, 79:644-648.
6. Chen C., Zhuang X. Epsin 1 is a cargo-specific adaptor for the clathrin-mediated endocytosis of the influenza virus. Proc Natl Acad Sci USA 2008, 105:11790-11795.
7. Delboy M.G., Roller D.G., Nicola A.V. Cellular proteasome activity facilitates herpes simplex virus entry at a postpenetration step. J Virol 2008, 82:3381-3390.
8. Satheshkumar P.S., Anton L.C., Sanz P., Moss B. Inhibition of the ubiquitin-proteasome system prevents vaccinia virus DNA replication and expression of intermediate and late genes. J Virol 2009, 83:2469-2479.
9. Teale A., Campbell S., Van Buuren N., Magee W.C., Watmough K., Couturier B., Shipclark R., Barry M. Orthopoxviruses require a functional ubiquitin-proteasome system for productive replication. J Virol 2009, 83:2099-2108.
10. Si X., Gao G., Wong J., Wang Y., Zhang J., Luo H. Ubiquitination is required for effective replication of coxsackievirus B3. PLoS One 2008, 3:e2585.
11. Lupfer C., Pastey M.K. Decreased replication of human respiratory syncytial virus treated with the proteasome inhibitor MG-132. Virus Res 2010, 149:36-41.
12. Takeuchi O., Akira S. Innate immunity to virus infection. Immunol Rev 2009, 227:75-86.
13. Gale M., Sen G.C. Viral evasion of the interferon system. J Interferon Cytokine Res 2009, 29:475-476.
14. Bhoj V.G., Chen Z.J. Ubiquitylation in innate and adaptive immunity. Nature 2009, 458:430-437.
15. Bauhofer O., Summerfield A., Sakoda Y., Tratschin J.D., Hofmann M.A., Ruggli N. Classical swine fever virus Npro interacts with interferon regulatory factor 3 and induces its proteasomal degradation. J Virol 2007, 81:3087-3096.
16. Chen Z., Rijnbrand R., Jangra R.K., Devaraj S.G., Qu L., Ma Y., Lemon S.M., Li K. Ubiquitination and proteasomal degradation of interferon regulatory factor-3 induced by Npro from a cytopathic bovine viral diarrhea virus. Virology 2007, 366:277-292.
17. Szymanski M.R., Fiebach A.R., Tratschin J.D., Gut M., Ramanujam V.M., Gottipati K., Patel P., Ye M., Ruggli N., Choi K.H. Zinc binding in pestivirus N(pro) is required for interferon regulatory factor 3 interaction and degradation. J Mol Biol 2009, 391:438-449.
18. Barro M., Patton J.T. Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. Proc Natl Acad Sci USA 2005, 102:4114-4119.
19. Graff J.W., Mitzel D.N., Weisend C.M., Flenniken M.L., Hardy M.E. Interferon regulatory factor 3 is a cellular partner of rotavirus NSP1. J Virol 2002, 76:9545-9550.
20. Okumura A., Alce T., Lubyova B., Ezelle H., Strebel K., Pitha P.M. HIV-1 accessory proteins VPR and Vif modulate antiviral response by targeting IRF-3 for degradation. Virology 2008, 373:85-97.
21. Chang T.H., Kubota T., Matsuoka M., Jones S., Bradfute S.B., Bray M., Ozato K. Ebola Zaire virus blocks type I interferon production by exploiting the host SUMO modification machinery. PLoS Pathog 2009, 5:e1000493.
22. Gack M.U., Albrecht R.A., Urano T., Inn K.S., Huang I.C., Carnero E., Farzan M., Inoue S., Jung J.U., Garcia-Sastre A. 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.
23. Chang S.-J., Hsiao J.-C., Sonnberg S., Chiang C.-T., Yang M.-H., Tzou D.-L., Mercer A.A., Chang W. Poxvirus host range protein CP77 contains an F-box-like domain that is necessary to suppress NF-kB activation by tumor necrosis factor alpha but is independent of its host range function. J Virol 2009, 83:4140-4152.
24. Rahman M.M., Mohamed M.R., Kim M., Smallwood S., McFadden G. Co-regulation of NF-kappaB and inflammasome-mediated inflammatory responses by myxoma virus pyrin domain-containing protein M013. PLoS Pathog 2009, 5:e1000635.
25. Tait S.W., Reid E.B., Greaves D.R., Wileman T.E., Powell P.P. Mechanism of inactivation of NF-kappa B by a viral homologue of I kappa b alpha. Signal-induced release of i kappa b alpha results in binding of the viral homologue to NF-kappa B. J Biol Chem 2000, 275:34656-34664.
26. Rodrigues L., Filipe J., Seldon M.P., Fonseca L., Anrather J., Soares M.P., Simas J.P. Termination of NF-kappaB activity through a gammaherpesvirus protein that assembles an EC5S ubiquitin-ligase. EMBO J 2009, 28:1283-1295.
27. Yokota S., Okabayashi T., Yokosawa N., Fujii N. Measles virus P protein suppresses Toll-like receptor signal through up-regulation of ubiquitin-modifying enzyme A20. FASEB J 2008, 22:74-83.
28. Graff J.W., Ettayebi K., Hardy M.E. Rotavirus NSP1 inhibits NFkappaB activation by inducing proteasome-dependent degradation of beta-TrCP: a novel mechanism of IFN antagonism. PLoS Pathog 2009, 5:e1000280.
29. Didcock L., Young D.F., Goodbourn S., Randall R.E. The V protein of simian virus 5 inhibits interferon signalling by targeting STAT1 for proteasome-mediated degradation. J Virol 1999, 73:9928-9933.
30. Ulane C.M., Horvath C.M. Paramyxoviruses SV5 and HPIV2 assemble STAT protein ubiquitin ligase complexes from cellular components. Virology 2002, 304:160-166.
31. Elliott J., Lynch O.T., Suessmuth Y., Qian P., Boyd C.R., Burrows J.F., Buick R., Stevenson N.J., Touzelet O., Gadina M., et al. Respiratory syncytial virus NS1 protein degrades STAT2 by using the Elongin-Cullin E3 ligase. J Virol 2007, 81:3428-3436.
32. Ashour J., Laurent-Rolle M., Shi P.Y., Garcia-Sastre A. NS5 of dengue virus mediates STAT2 binding and degradation. J Virol 2009, 83:5408-5418.
33. Puri M., Lemon K., Duprex W.P., Rima B.K., Horvath C.M. A point mutation, E95D, in the mumps virus V protein disengages STAT3 targeting from STAT1 targeting. J Virol 2009, 83:6347-6356.
34. Sadler A.J., Williams B.R. Interferon-inducible antiviral effectors. Nat Rev Immunol 2008, 8:559-568.
35. Jeon Y.J., Yoo H.M., Chung C.H. ISG15 and immune diseases. Biochim Biophys Acta 2010, 1802:485-496.
36. Harty R.N., Pitha P.M., Okumura A. Antiviral activity of innate immune protein ISG15. J Innate Immun 2009, 1:397-404.
37. Zhao C., Denison C., Huibregtse J.M., Gygi S., Krug R.M. Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc Natl Acad Sci USA 2005, 102:10200-10205.
38. Shi H.X., Yang K., Liu X., Liu X.Y., Wei B., Shan Y.F., Zhu L.H., Wang C. Positive Regulation of IRF3 Activation by Herc5 via ISG15 Modification. Mol Cell Biol 2010, 30:2424-2436.
39. Lu G., Reinert J.T., Pitha-Rowe I., Okumura A., Kellum M., Knobeloch K.P., Hassel B., Pitha P.M. ISG15 enhances the innate antiviral response by inhibition of IRF-3 degradation. Cell Mol Biol (Noisy-le-grand) 2006, 52:29-41.
40. 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.
41. Giannakopoulos N.V., Arutyunova E., Lai C., Lenschow D.J., Haas A.L., Virgin H.W. ISG15 Arg151 and the ISG15-conjugating enzyme UbE1L are important for innate immune control of Sindbis virus. J Virol 2009, 83:1602-1610.
42. Lenschow D.J., Lai C., Frias-Staheli N., Giannakopoulos N.V., Lutz A., Wolff T., Osiak A., Levine B., Schmidt R.E., Garcia-Sastre A., et al. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc Natl Acad Sci USA 2007, 104:1371-1376.
43. Malakhova O.A., Zhang D.E. ISG15 inhibits Nedd4 ubiquitin E3 activity and enhances the innate antiviral response. J Biol Chem 2008, 283:8783-8787.
44. Okumura A., Lu G., Pitha-Rowe I., Pitha P.M. Innate antiviral response targets HIV-1 release by the induction of ubiquitin-like protein ISG15. Proc Natl Acad Sci USA 2006, 103:1440-1445.
45. Osiak A., Utermöhlen O., Niendorf S., Horak I., Knobeloch K.-P. ISG15, an interferon-stimulated ubiquitin-like protein, is not essential for STAT1 signaling and responses against vesicular stomatitis and lymphocytic choriomeningitis virus. Mol Cell Biol 2005, 25:6338-6345.
46. Sridharan H., Zhao C., Krug R.M. 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.
47. Versteeg G.A., Hale B.G., van Boheemen S., Wolff T., Lenschow D.J., Garcia-Sastre A. Species-specific antagonism of host ISGylation by the influenza B virus NS1 protein. J Virol 2010, 84:5423-5430.
48. 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.
49. Zhao C., Hsiang T.Y., Kuo R.L., Krug R.M. ISG15 conjugation system targets the viral NS1 protein in influenza A virus-infected cells. Proc Natl Acad Sci USA 2010, 107:2253-2258.
50. Pal S., Rosas J.M., Rosas-Acosta G. Identification of the non-structural influenza A viral protein NS1A as a bona fide target of the Small Ubiquitin-like MOdifier by the use of dicistronic expression constructs. J Virol Methods 2010, 163:498-504.
51. Guerra S., Caceres A., Knobeloch K.P., Horak I., Esteban M. Vaccinia virus E3 protein prevents the antiviral action of ISG15. PLoS Pathog 2008, 4:e1000096.
52. 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.
53. Clementz M.A., Chen Z., Banach B.S., Wang Y., Sun L., Ratia K., Baez-Santos Y.M., Wang J., Takayama J., Ghosh A.K., et al. Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J Virol 2010, 84:4619-4629.
54. Blasius A.L., Giurisato E., Cella M., Schreiber R.D., Shaw A.S., Colonna M. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J Immunol 2006, 177:3260-3265.
55. Kupzig S., Korolchuk V., Rollason R., Sugden A., Wilde A., Banting G. Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 2003, 4:694-709.
56. Bartee E., McCormack A., Fruh K. Quantitative membrane proteomics reveals new cellular targets of viral immune modulators. PLoS Pathog 2006, 2:e107.
57. Douglas J.L., Viswanathan K., McCarroll M.N., Gustin J.K., Fruh K., Moses A.V. Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a {beta}TrCP-dependent mechanism. J Virol 2009, 83:7931-7947.
58. Bartee E., Mansouri M., Hovey Nerenberg B.T., Gouveia K., Fruh K. Downregulation of major histocompatibility complex class I by human ubiquitin ligases related to viral immune evasion proteins. J Virol 2004, 78:1109-1120.
59. Nathan J.A., Lehner P.J. The trafficking and regulation of membrane receptors by the RING-CH ubiquitin E3 ligases. Exp Cell Res 2009, 315:1593-1600.
60. Neil S.J., Zang T., Bieniasz P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451:425-430.
61. Van Damme N., Goff D., Katsura C., Jorgenson R.L., Mitchell R., Johnson M.C., Stephens E.B., Guatelli J. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 2008, 3:245-252.
62. Douglas J.L., Gustin J.K., Viswanathan K., Mansouri M., Moses A.V., Früh K. The Great Escape: viral strategies to counter BST-2/Tetherin. PLoS Pathog 2010, 6:e1000913.
63. Mansouri M., Viswanathan K., Douglas J.L., Hines J., Gustin J., Moses A.V., Fruh K. Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of Kaposi's sarcoma-associated herpesvirus. J Virol 2009, 83:9672-9681.
64. Mitchell R.S., Katsura C., Skasko M.A., Fitzpatrick K., Lau D., Ruiz A., Stephens E.B., Margottin-Goguet F., Benarous R., Guatelli J.C. Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog 2009, 5:e1000450.
65. Goffinet C., Allespach I., Homann S., Tervo H.-M., Habermann A., Rupp D., Oberbremer L., Kern C., Tibroni N., Welsch S., et al. HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor. Cell Host Microbe 2009, 5:285-297.
66. Mangeat B., Gers-Huber G., Lehmann M., Zufferey M., Luban J., Piguet V. HIV-1 Vpu neutralizes the antiviral factor Tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation. PLoS Pathog 2009, 5:e1000574.
67. Dallaire F., Blanchette P., Branton P.E. A proteomic approach to identify candidate substrates of human adenovirus E4orf6-E1B55K and other viral cullin-based E3 ubiquitin ligases. J Virol 2009, 83:12172-12184.
68. Dallaire F., Blanchette P., Groitl P., Dobner T., Branton P.E. Identification of integrin alpha3 as a new substrate of the adenovirus E4orf6/E1B 55-kilodalton E3 ubiquitin ligase complex. J Virol 2009, 83:5329-5338.
69. Hor S., Ziv T., Admon A., Lehner P.J. Stable isotope labeling by amino acids in cell culture and differential plasma membrane proteome quantitation identify new substrates for the MARCH9 transmembrane E3 ligase. Mol Cell Proteomics 2009, 8:1959-1971.
70. Garaigorta U., Chisari F.V. Hepatitis C virus blocks interferon effector function by inducing protein kinase R phosphorylation. Cell Host Microbe 2009, 6:513-522.