USP18 recruits USP20 to promote innate antiviral response through deubiquitinating STING/MITA

Cell Research

Volumn 26, Issue 12, 2016, Pages 1302-1319

  Zhang, Man ^a   Zhang, Meng Xin ^a   Zhang, Qiang ^a   Zhu, Gao Feng ^a   Yuan, Lei ^a   Zhang, Dong Er ^d   Zhu, Qiyun ^c   Yao, Jing ^a   Shu, Hong Bing ^b   Zhong, Bo ^a,b  

^a WUHAN UNIVERSITY   (China)

^b WUHAN UNIVERSITY   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Deubiquitination; Innate antiviral response; STING MITA; USP18; USP20

Indexed keywords

ALPHA BETA INTERFERON RECEPTOR; CYTOKINE; G1P2 PROTEIN, MOUSE; IFNAR1 PROTEIN, MOUSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; MEMBRANE PROTEIN; MPYS PROTEIN, MOUSE; PROTEINASE; UBIQUITIN; UBIQUITIN THIOLESTERASE; USP18 PROTEIN, MOUSE; USP20 PROTEIN, MOUSE;

ANIMAL; ANTAGONISTS AND INHIBITORS; BONE MARROW CELL; CELL CULTURE; CHEMISTRY; CYTOLOGY; DEFICIENCY; FIBROBLAST; GENETICS; HEK293 CELL LINE; HERPES SIMPLEX; HUMAN; HUMAN ALPHAHERPESVIRUS 1; KNOCKOUT MOUSE; METABOLISM; MORTALITY; MOUSE; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SURVIVAL RATE; VETERINARY; VIROLOGY;

ANIMALS; BONE MARROW CELLS; CELLS, CULTURED; CYTOKINES; ENDOPEPTIDASES; FIBROBLASTS; HEK293 CELLS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NF-KAPPA B; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION; SURVIVAL RATE; UBIQUITIN THIOLESTERASE; UBIQUITINS;

EID: 84994152020     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2016.125     Document Type: Article

References (61)

1. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140:805-820.
2. Wu J, Chen ZJ. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 2014; 32:461-488.
3. Hou F, Sun L, Zheng H, Skaug B, Jiang QX, Chen ZJ. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 2011; 146:448-461.
4. Seth RB, Sun L, Ea CK, Chen ZJ. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 2005; 122:669-682.
5. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 2005; 19:727-740.
6. Kawai T, Takahashi K, Sato S, et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 2005; 6:981-988.
7. Meylan E, Curran J, Hofmann K, et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005; 437:1167-1172.
8. Ablasser A, Bauernfeind F, Hartmann G, Latz E, Fitzgerald KA, Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat Immunol 2009; 10:1065-1072.
9. Chiu YH, Macmillan JB, Chen ZJ. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009; 138:576-591.
10. Takaoka A, Wang Z, Choi MK, et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007; 448:501-505.
11. Unterholzner L, Keating SE, Baran M, et al. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 2010; 11:997-1004.
12. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 2011; 12:959-965.
13. Li Y, Chen R, Zhou Q, et al. LSm14A is a processing body-associated sensor of viral nucleic acids that initiates cellular antiviral response in the early phase of viral infection. Proc Natl Acad Sci USA 2012; 109:11770-11775.
14. Sun L, Wu J, Du F, Chen X, Chen ZJ. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013; 339:786-791.
15. Li XD, Wu J, Gao D, Wang H, Sun L, Chen ZJ. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 2013; 341:1390-1394.
16. Schoggins JW, MacDuff DA, Imanaka N, et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 2014; 505:691-695.
17. Zhang X, Shi H, Wu J, et al. Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high - affinity ligand for STING. Mol Cell 2013; 51:226-235.
18. Ablasser A, Goldeck M, Cavlar T, et al. cGAS produces a 2'-5'-linked cyclic dinucleotide second messenger that activates STING. Nature 2013; 498:380-384.
19. Zhong B, Yang Y, Li S, et al. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 2008; 29:538-550.
20. Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008; 455:674-678.
21. Jin L, Hill KK, Filak H, et al. MPYS is required for IFN response factor 3 activation and type I IFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. J Immunol 2011; 187:2595-2601.
22. Sun W, Li Y, Chen L, et al. ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc Natl Acad Sci USA 2009; 106:8653-8658.
23. Ouyang S, Song X, Wang Y, et al. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 2012; 36:1073-1086.
24. Yin Q, Tian Y, Kabaleeswaran V, et al. Cyclic di-GMP sensing via the innate immune signaling protein STING. Mol Cell 2012; 46:735-745.
25. Shu C, Yi G, Watts T, Kao CC, Li P. Structure of STING bound to cyclic di-GMP reveals the mechanism of cyclic dinucleotide recognition by the immune system. Nat Struct Mol Biol 2012; 19:722-724.
26. You F, Sun H, Zhou X, et al. PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat Immunol 2009; 10:1300-1308.
27. Zhong B, Zhang Y, Tan B, Liu TT, Wang YY, Shu HB. The E3 ubiquitin ligase RNF5 targets virus-induced signaling adaptor for ubiquitination and degradation. J Immunol 2010; 184:6249-6255.
28. Zhong B, Zhang L, Lei C, et al. The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity 2009; 30:397-407.
29. Qin Y, Zhou MT, Hu MM, et al. RNF26 temporally regulates virus-triggered type I interferon induction by two distinct mechanisms. PLoS Pathog 2014; 10:e1004358.
30. Zhang J, Hu MM, Wang YY, Shu HB. 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.
31. Tsuchida T, Zou J, Saitoh T, et al. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 2010; 33:765-776.
32. Wang Q, Liu X, Cui Y, et al. The E3 ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 2014; 41:919-933.
33. Reyes-Turcu FE, Ventii KH, Wilkinson KD. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 2009; 78:363-397.
34. Li Z, Wang D, Messing EM, Wu G. VHL protein-interacting deubiquitinating enzyme 2 deubiquitinates and stabilizes HIF-1alpha. EMBO Rep 2005; 6:373-378.
35. Berthouze M, Venkataramanan V, Li Y, Shenoy SK. The deubiquitinases USP33 and USP20 coordinate beta2 adrenergic receptor recycling and resensitization. EMBO J 2009; 28:1684-1696.
36. Yasunaga J, Lin FC, Lu X, Jeang KT. Ubiquitin-specific peptidase 20 targets TRAF6 and human T cell leukemia virus type 1 tax to negatively regulate NF-kappaB signaling. J Virol 2011; 85:6212-6219.
37. Yuan J, Luo K, Deng M, et al. HERC2-USP20 axis regulates DNA damage checkpoint through Claspin. Nucleic Acids Res 2014; 42:13110-13121.
38. Zhu M, Zhao H, Liao J, Xu X. HERC2/USP20 coordinates CHK1 activation by modulating CLASPIN stability. Nucleic Acids Res 2014; 42:13074-13081.
39. Schwer H, Liu LQ, Zhou L, et al. Cloning and characterization of a novel human ubiquitin-specific protease, a homologue of murine UBP43 (Usp18). Genomics 2000; 65:44-52.
40. Malakhov MP, Malakhova OA, Kim KI, Ritchie KJ, Zhang DE. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J Biol Chem 2002; 277:9976-9981.
41. Ritchie KJ, Malakhov MP, Hetherington CJ, et al. Dysregulation of protein modification by ISG15 results in brain cell injury. Genes Dev 2002; 16:2207-2212.
42. Ketscher L, Hannss R, Morales DJ, et al. Selective inactivation of USP18 isopeptidase activity in vivo enhances ISG15 conjugation and viral resistance. Proc Natl Acad Sci USA 2015; 112:1577-1582.
43. Malakhova OA, Kim KI, Luo JK, et al. UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J 2006; 25:2358-2367.
44. Kim KI, Yan M, Malakhova O, et al. Ube1L and protein IS-Gylation are not essential for alpha/beta interferon signaling. Mol Cell Biol 2006; 26:472-479.
45. Knobeloch KP, Utermohlen O, Kisser A, Prinz M, Horak I. Reexamination of the role of ubiquitin-like modifier ISG15 in the phenotype of UBP43-deficient mice. Mol Cell Biol 2005; 25:11030-11034.
46. Liu X, Li H, Zhong B, et al. USP18 inhibits NF-kappaB and NFAT activation during Th17 differentiation by deubiquitinating the TAK1-TAB1 complex. J Exp Med 2013; 210:1575-1590.
47. Yang Z, Xian H, Hu J, et al. USP18 negatively regulates NF-kappaB signaling by targeting TAK1 and NEMO for deubiquitination through distinct mechanisms. Sci Rep 2015; 5:12738.
48. Ritchie KJ, Hahn CS, Kim KI, et al. Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat Med 2004; 10:1374-1378.
49. Honke N, Shaabani N, Cadeddu G, et al. Enforced viral replication activates adaptive immunity and is essential for the control of a cytopathic virus. Nat Immunol 2012; 13:51-57.
50. Donley DK. TORCH infections in the newborn. Semin Neurol 1993; 13:106-115.
51. Meuwissen ME, Schot R, Buta S, et al. Human USP18 deficiency underlies type 1 interferonopathy leading to severe pseudo-TORCH syndrome. J Exp Med 2016; 213:1163-1174.
52. Basters A, Geurink PP, El Oualid F, et al. Molecular characterization of ubiquitin-specific protease 18 reveals substrate specificity for interferon-stimulated gene 15. FEBS J 2014; 281:1918-1928.
53. Malakhova OA, Yan M, Malakhov MP, et al. Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev 2003; 17:455-460.
54. Cai X, Chiu YH, Chen ZJ. The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Mol Cell 2014; 54:289-296.
55. Wu J, Sun L, Chen X, et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 2013; 339:826-830.
56. You F, Wang P, Yang L, et al. ELF4 is critical for induction of type I interferon and the host antiviral response. Nat Immunol 2013; 14:1237-1246.
57. Holm CK, Rahbek SH, Gad HH, et al. Influenza A virus targets a cGAS-independent STING pathway that controls enveloped RNA viruses. Nat Commun 2016; 7:10680.
58. Kim KI, Malakhova OA, Hoebe K, Yan M, Beutler B, Zhang DE. Enhanced antibacterial potential in UBP43-deficient mice against Salmonella typhimurium infection by up-regulating type I IFN signaling. J Immunol. 2005; 175:847-854.
59. Zhou Q, Lin H, Wang S, et al. The ER-associated protein ZDHHC1 is a positive regulator of DNA virus-triggered, MITA/STING-dependent innate immune signaling. Cell Host Microbe 2014; 16:450-461.
60. Lin D, Zhang M, Zhang MX, et al. Induction of USP25 by viral infection promotes innate antiviral responses by mediating the stabilization of TRAF3 and TRAF6. Proc Natl Acad Sci USA 2015; 112: 11324-11329.
61. Zhong B, Liu X, Wang X, et al. Ubiquitin-specific protease 25 regulates TLR4-dependent innate immune responses through deubiquitination of the adaptor protein TRAF3. Sci Signal 2013; 6:ra35.