Ubiquitin-specific proteases 25 negatively regulates virus-induced type I interferon signaling

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Zhong, Huijuan ^a   Wang, Dang ^a   Fang, Liurong ^a   Zhang, Huan ^a   Luo, Rui ^a   Shang, Min ^a   Ouyang, Chao ^a   Ouyang, Haiping ^a   Chen, Huanchun ^a   Xiao, Shaobo ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERFERON REGULATORY FACTOR 3; IRF3 PROTEIN, HUMAN; LUCIFERASE; LYSINE; RARRES3 PROTEIN, HUMAN; RETINOIC ACID RECEPTOR; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN THIOLESTERASE; USP25 PROTEIN, HUMAN;

ANTAGONISTS AND INHIBITORS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHOSPHORYLATION; REPORTER GENE; SENDAI VIRUS; SIGNAL TRANSDUCTION; UBIQUITINATION;

GENE EXPRESSION REGULATION; GENE SILENCING; GENES, REPORTER; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; LUCIFERASES; LYSINE; PHOSPHORYLATION; RECEPTORS, RETINOIC ACID; RNA, SMALL INTERFERING; SENDAI VIRUS; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 2; TNF RECEPTOR-ASSOCIATED FACTOR 6; TRANSCRIPTION FACTOR RELA; UBIQUITIN THIOLESTERASE; UBIQUITINATION;

EID: 84894087907     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080976     Document Type: Article

References (55)

1. Kawai T, Akira S (2006) Innate immune recognition of viral infection. Nat Immunol 7: 131-137. doi:10.1038/ni1303. PubMed: 16424890. (Pubitemid 43135878)
2. Darnell JE Jr., Kerr IM, Stark GR (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264: 1415-1421. doi:10.1126/science.8197455. PubMed: 8197455. (Pubitemid 24217131)
3. Hubackova S, Novakova Z, Krejcikova K, Kosar M, Dobrovolna J et al. (2010) Regulation of the PML tumor suppressor in drug-induced senescence of human normal and cancer cells by JAK/STAT-mediated signaling. Cell Cycle 9: 3085-3099. doi:10.4161/cc.9.15.12521. PubMed: 20699642.
4. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105. doi:10.1038/nature04734. PubMed: 16625202.
5. Pichlmair A, Schulz O, Tan CP, Näslund TI, Liljeström P et al. (2006) RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314: 997-1001. doi:10.1126/science.1132998. PubMed: 17038589. (Pubitemid 44749946)
6. Ye J, Maniatis T (2011) Negative regulation of interferon-beta gene expression during acute and persistent virus infections. PLOS ONE 6: e20681. doi:10.1371/journal.pone.0020681. PubMed: 21677781.
7. Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O et al. (2008) Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82: 335-345. doi:10.1128/JVI.01080-07. PubMed: 17942531. (Pubitemid 350309149)
8. Maelfait J, Beyaert R (2012) Emerging role of ubiquitination in antiviral RIG-I signaling. Microbiol Mol Biol Rev 76: 33-45. doi:10.1128/MMBR.05012-11. PubMed: 22390971.
9. Seth RB, Sun L, Ea CK, Chen ZJ (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682. doi:10.1016/j.cell.2005.08.012. PubMed: 16125763. (Pubitemid 41242633)
10. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z et al. (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19: 727-740. doi:10.1016/j.molcel.2005.08.014. PubMed: 16153868. (Pubitemid 41316668)
11. Kawai T, Takahashi K, Sato S, Coban C, Kumar H et al. (2005) IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6: 981-988. doi:10.1038/ni1243. PubMed: 16127453. (Pubitemid 41486182)
12. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M et al. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167-1172. doi:10.1038/nature04193. PubMed: 16177806. (Pubitemid 41509355)
13. Kato H, Takahasi K, Fujita T (2011) RIG-I-like receptors: cytoplasmic sensors for non-self RNA. Immunol Rev 243: 91-98. doi:10.1111/j.1600-065X.2011. 01052.x. PubMed: 21884169.
14. Yoneyama M, Fujita T (2007) RIG-I family RNA helicases: cytoplasmic sensor for antiviral innate immunity. Cytokine Growth Factor Rev 18: 545-551. doi:10.1016/j.cytogfr.2007.06.023. PubMed: 17683970. (Pubitemid 47302820)
15. Weissman AM (2001) Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol 2: 169-178. doi:10.1038/35056563. PubMed: 11265246.
16. Reyes-Turcu FE, Ventii KH, Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78: 363-397. doi:10.1146/annurev.biochem.78.082307.091526. PubMed: 19489724.
17. Wilkinson KD (2009) DUBs at a glance. J Cell Sci 122: 2325-2329. doi:10.1242/jcs.041046. PubMed: 19571111.
18. Song L, Rape M (2008) Reverse the curse - the role of deubiquitination in cell cycle control. Curr Opin Cell Biol 20: 156-163. doi:10.1016/j.ceb.2008.01. 012. PubMed: 18346885.
19. Schmidt M, Hanna J, Elsasser S, Finley D (2005) Proteasome-associated proteins: regulation of a proteolytic machine. Biol Chem 386: 725-737. PubMed: 16201867. (Pubitemid 41448153)
20. Kayagaki N, Phung Q, Chan S, Chaudhari R, Quan C et al. (2007) DUBA: a deubiquitinase that regulates type I interferon production. Science 318: 1628-1632. doi:10.1126/science.1145918. PubMed: 17991829. (Pubitemid 350233662)
21. Adhikari A, Xu M, Chen ZJ (2007) Ubiquitin-mediated activation of TAK1 and IKK. Oncogene 26: 3214-3226. doi:10.1038/sj.onc.1210413. PubMed: 17496917. (Pubitemid 46763016)
22. Pickart CM (2001) Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533. doi:10.1146/annurev.biochem.70.1.503. PubMed: 11395416.
23. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM et al. (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123: 773-786. doi:10.1016/j.cell.2005.11.007. PubMed: 16325574. (Pubitemid 41721026)
24. McCloskey RJ, Kemphues KJ (2012) Deubiquitylation machinery is required for embryonic polarity in Caenorhabditis elegans. PLOS Genet 8: e1003092. PubMed: 23209443.
25. Bhoj VG, Chen ZJ (2009) Ubiquitylation in innate and adaptive immunity. Nature 458: 430-437. doi:10.1038/nature07959. PubMed: 19325622.
26. Friedman CS, O'Donnell MA, Legarda-Addison D, Ng A, Cárdenas WB et al. (2008) The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep 9: 930-936. doi:10.1038/embor.2008.136. PubMed: 18636086.
27. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L et al. (2004) Deubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430: 694-699. doi:10.1038/nature02794. PubMed: 15258597. (Pubitemid 39061687)
28. Ehrhardt C, Kardinal C, Wurzer WJ, Wolff T, von Eichel-Streiber C et al. (2004) Rac1 and PAK1 are upstream of IKK-epsilon and TBK-1 in the viral activation of interferon regulatory factor-3. FEBS Lett 567: 230-238. doi:10.1016/j.febslet.2004.04.069. PubMed: 15178328. (Pubitemid 38748397)
29. Nishikawa H, Ooka S, Sato K, Arima K, Okamoto J et al. (2004) Mass spectrometric and mutational analyses reveal Lys-6-linked polyubiquitin chains catalyzed by BRCA1-BARD1 ubiquitin ligase. J Biol Chem 279: 3916-3924. PubMed: 14638690. (Pubitemid 38198974)
30. Clementz MA, Chen Z, Banach BS, Wang Y, Sun L et al. (2010) Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J Virol 84: 4619-4629. doi:10.1128/JVI.02406-09. PubMed: 20181693.
31. Luo R, Xiao S, Jiang Y, Jin H, Wang D et al. (2008) Porcine reproductive and respiratory syndrome virus (PRRSV) suppresses interferon-beta production by interfering with the RIG-I signaling pathway. Mol Immunol 45: 2839-2846. doi:10.1016/j.molimm.2008.01.028. PubMed: 18336912.
32. Yoneyama M, Suhara W, Fukuhara Y, Fukuda M, Nishida E et al. (1998) Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/p300. EMBO J 17: 1087-1095. doi:10.1093/emboj/17.4.1087. PubMed: 9463386. (Pubitemid 28077662)
33. Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199. doi:10.1016/0378-1119(91)90434-D. PubMed: 1660837.
34. Sun W, Tan X, Shi Y, Xu G, Mao R et al. (2010) USP11 negatively regulates TNFalpha-induced NF-kappaB activation by targeting on IkappaBalpha. Cell Signal 22: 386-394. doi:10.1016/j.cellsig.2009.10.008. PubMed: 19874889.
35. Beura LK, Sarkar SN, Kwon B, Subramaniam S, Jones C et al. (2010) Porcine reproductive and respiratory syndrome virus nonstructural protein 1beta modulates host innate immune response by antagonizing IRF3 activation. J Virol 84: 1574-1584. doi:10.1128/JVI.01326-09. PubMed: 19923190.
36. Wilkinson KD, Tashayev VL, O'Connor LB, Larsen CN, Kasperek E et al. (1995) Metabolism of the polyubiquitin degradation signal: structure, mechanism, and role of isopeptidase T. Biochemistry 34: 14535-14546. doi:10.1021/ bi00044a032. PubMed: 7578059.
37. Metzig M, Nickles D, Falschlehner C, Lehmann-Koch J, Straub BK et al. (2011) An RNAi screen identifies USP2 as a factor required for TNF-alpha-induced NF-kappaB signaling. Int J Cancer 29: 607-618.
38. Fan YH, Yu Y, Mao RF, Tan XJ, Xu GF et al. (2011) USP4 targets TAK1 to downregulate TNFalpha-induced NF-kappaB activation. Cell Death Differ 18: 1547-1560. doi:10.1038/cdd.2011.11. PubMed: 21331078.
39. Chen R, Zhang L, Zhong B, Tan B, Liu Y et al. (2010) The ubiquitin-specific protease 17 is involved in virus-triggered type I IFN signaling. Cell Res 20: 802-811. doi:10.1038/cr.2010.41. PubMed: 20368735.
40. Yasunaga J, Lin FC, Lu X, Jeang KT (2011) Ubiquitin-specific peptidase 20 targets TRAF6 and human T cell leukemia virus type 1 tax to negatively regulate NF-kappaB signaling. J Virol 85: 6212-6219. doi:10.1128/JVI.00079-11. PubMed: 21525354.
41. Xu G, Tan X, Wang H, Sun W, Shi Y et al. (2010) Ubiquitin-specific peptidase 21 inhibits tumor necrosis factor alpha-induced nuclear factor kappaB activation via binding to and deubiquitinating receptor-interacting protein 1. J Biol Chem 285: 969-978. doi:10.1074/jbc.M109.042689. PubMed: 19910467.
42. Enesa K, Zakkar M, Chaudhury H, Luong le A, Rawlinson L et al. (2008) NF-kappaB suppression by the deubiquitinating enzyme Cezanne: a novel negative feedback loop in pro-inflammatory signaling. J Biol Chem 283: 7036-7045. doi:10.1074/jbc.M708690200. PubMed: 18178551.
43. Brummelkamp TR, Nijman SM, Dirac AM, Bernards R (2003) Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 424: 797-801. doi:10.1038/nature01811. PubMed: 12917690. (Pubitemid 37021711)
44. Schweitzer K, Bozko PM, Dubiel W, Naumann M (2007) CSN controls NF-kappaB by deubiquitinylation of IkappaBalpha. EMBO J 26: 1532-1541. doi:10.1038/sj.emboj.7601600. PubMed: 17318178. (Pubitemid 46480929)
45. Tzimas C, Michailidou G, Arsenakis M, Kieff E, Mosialos G et al. (2006) Human ubiquitin specific protease 31 is a deubiquitinating enzyme implicated in activation of nuclear factor-kappaB. Cell Signal 18: 83-92. doi:10.1016/j. cellsig.2005.03.017. PubMed: 16214042. (Pubitemid 41415717)
46. Quesada V, Díaz-Perales A, Gutiérrez-Fernández A, Garabaya C, Cal S et al. (2004) Cloning and enzymatic analysis of 22 novel human ubiquitin-specific proteases. Biochem Biophys Res Commun 314: 54-62. doi:10.1016/j.bbrc.2003.12.050. PubMed: 14715245. (Pubitemid 38058368)
47. Isaacson MK, Ploegh HL (2009) Ubiquitination, ubiquitin-like modifiers, and deubiquitination in viral infection. Cell Host Microbe 5: 559-570. doi:10.1016/j.chom.2009.05.012. PubMed: 19527883.
48. Sun SC (2008) Deubiquitylation and regulation of the immune response. Nat Rev Immunol 8: 501-511. doi:10.1038/nri2337. PubMed: 18535581.
49. Gack MU, Shin YC, Joo CH, Urano T, Liang C et al. (2007) TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446: 916-920. doi:10.1038/nature05732. PubMed: 17392790. (Pubitemid 46633167)
50. Mao AP, Li S, Zhong B, Li Y, Yan J et al. (2010) Virus-triggered ubiquitination of TRAF3/6 by cIAP1/2 is essential for induction of interferon-beta (IFN-beta) and cellular antiviral response. J Biol Chem 285: 9470-9476. doi:10.1074/jbc.M109.071043. PubMed: 20097753.
51. Mace PD, Smits C, Vaux DL, Silke J, Day CL (2010) Asymmetric recruitment of cIAPs by TRAF2. J Mol Biol 400: 8-15. doi:10.1016/j.jmb.2010.04.055. PubMed: 20447407.
52. Denuc A, Bosch-Comas A, Gonzàlez-Duarte R, Marfany G (2009) The UBA-UIM domains of the USP25 regulate the enzyme ubiquitination state and modulate substrate recognition. PLOS ONE 4: e5571. doi:10.1371/journal.pone. 0005571. PubMed: 19440361.
53. Blount JR, Burr AA, Denuc A, Marfany G, Todi SV (2012) Ubiquitin-specific protease 25 functions in Endoplasmic Reticulum-associated degradation. PLOS ONE 7: e36542. doi:10.1371/journal.pone.0036542. PubMed: 22590560.
54. Zhong B, Liu X, Wang X, Chang SH, Wang A et al. (2012) Negative regulation of IL-17-mediated signaling and inflammation by the ubiquitin-specific protease USP25. Nat Immunol 13: 1110-1117. doi:10.1038/ni.2427. PubMed: 23042150.
55. Zhong B, Liu X, Wang X, Li H, Darnay BG et al. (2013) Ubiquitin-specific protease 25 regulates TLR4-dependent innate immune responses through deubiquitination of the adaptor protein TRAF3. Sci Signal 6: ra35-: ra35 PubMed: 23674823.