دورية أكاديمية
RIPLET, and not TRIM25, is required for endogenous RIG-I-dependent antiviral responses.
العنوان: | RIPLET, and not TRIM25, is required for endogenous RIG-I-dependent antiviral responses. |
---|---|
المؤلفون: | Hayman TJ; The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.; Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia., Hsu AC; Priority Research Centre for Asthma and Respiratory Diseases, Hunter Medical Research Institute, The University of Newcastle, Newcastle, NSW, Australia., Kolesnik TB; The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia., Dagley LF; The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.; Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia., Willemsen J; Research Group Dynamics of Early Viral Infection and the Innate Antiviral Response, Division Virus-Associated Carcinogenesis (F170), German Cancer Research Center (DKFZ), Heidelberg, Germany., Tate MD; Centre for Innate Immunity and Infectious Diseases, Hudson Institute of Medical Research, Clayton, VIC, Australia.; Department of Molecular Translational Science, School of Clinical Sciences, Monash University, Clayton, VIC, Australia., Baker PJ; The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.; Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia., Kershaw NJ; The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.; Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia., Kedzierski L; Department of Microbiology and Immunology, University of Melbourne, Peter Doherty Institute for Infection and Immunity, Parkville, VIC, Australia., Webb AI; The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.; Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia., Wark PA; Priority Research Centre for Asthma and Respiratory Diseases, Hunter Medical Research Institute, The University of Newcastle, Newcastle, NSW, Australia.; Centre for Inflammation, Centenary Institute, The University of Technology Sydney, Sydney, NSW, Australia., Kedzierska K; Department of Microbiology and Immunology, University of Melbourne, Peter Doherty Institute for Infection and Immunity, Parkville, VIC, Australia., Masters SL; The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.; Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia., Belz GT; The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.; Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia., Binder M; Research Group Dynamics of Early Viral Infection and the Innate Antiviral Response, Division Virus-Associated Carcinogenesis (F170), German Cancer Research Center (DKFZ), Heidelberg, Germany., Hansbro PM; Priority Research Centre for Asthma and Respiratory Diseases, Hunter Medical Research Institute, The University of Newcastle, Newcastle, NSW, Australia.; Centre for Inflammation, Centenary Institute, The University of Technology Sydney, Sydney, NSW, Australia., Nicola NA; The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.; Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia., Nicholson SE; The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.; Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia. |
المصدر: | Immunology and cell biology [Immunol Cell Biol] 2019 Oct; Vol. 97 (9), pp. 840-852. Date of Electronic Publication: 2019 Aug 19. |
نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't |
اللغة: | English |
بيانات الدورية: | Publisher: Wiley Country of Publication: United States NLM ID: 8706300 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1440-1711 (Electronic) Linking ISSN: 08189641 NLM ISO Abbreviation: Immunol Cell Biol Subsets: MEDLINE |
أسماء مطبوعة: | Publication: 2018- : [Hoboken, NJ] : Wiley Original Publication: [Adelaide, South Australia] : University of Adelaide, [c1987- |
مواضيع طبية MeSH: | Signal Transduction*, Antiviral Agents/*metabolism , DEAD Box Protein 58/*metabolism , DNA-Binding Proteins/*metabolism , Transcription Factors/*metabolism , Tripartite Motif Proteins/*metabolism , Ubiquitin-Protein Ligases/*metabolism, A549 Cells ; Animals ; Cell Line ; Epithelial Cells/microbiology ; Epithelial Cells/virology ; Gene Deletion ; Humans ; Ligands ; Mice, Inbred C57BL ; RNA/metabolism ; Receptors, Immunologic |
مستخلص: | The innate immune system is our first line of defense against viral pathogens. Host cell pattern recognition receptors sense viral components and initiate immune signaling cascades that result in the production of an array of cytokines to combat infection. Retinoic acid-inducible gene-I (RIG-I) is a pattern recognition receptor that recognizes viral RNA and, when activated, results in the production of type I and III interferons (IFNs) and the upregulation of IFN-stimulated genes. Ubiquitination of RIG-I by the E3 ligases tripartite motif-containing 25 (TRIM25) and Riplet is thought to be requisite for RIG-I activation; however, recent studies have questioned the relative importance of these two enzymes for RIG-I signaling. In this study, we show that deletion of Trim25 does not affect the IFN response to either influenza A virus (IAV), influenza B virus, Sendai virus or several RIG-I agonists. This is in contrast to deletion of either Rig-i or Riplet, which completely abrogated RIG-I-dependent IFN responses. This was consistent in both mouse and human cell lines, as well as in normal human bronchial cells. With most of the current TRIM25 literature based on exogenous expression, these findings provide critical evidence that Riplet, and not TRIM25, is required endogenously for the ubiquitination of RIG-I. Despite this, loss of TRIM25 results in greater susceptibility to IAV infection in vivo, suggesting that it may have an alternative role in host antiviral defense. This study refines our understanding of RIG-I signaling in viral infections and will inform future studies in the field. (© 2019 Australian and New Zealand Society for Immunology Inc.) |
References: | Yoneyama M, Kikuchi M, Natsukawa T, et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5: 730-737. Kato H, Takeuchi O, Sato S, et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441: 101-105. Cui S, Eisenächer K, Kirchhofer A, et al. The C-terminal regulatory domain is the RNA 5′-triphosphate sensor of RIG-I. Mol Cell 2008; 29: 169-179. Kowalinski E, Lunardi T, McCarthy A, et al. Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 2011; 147: 423-435. Seth RB, Sun L, Ea C-K, et al. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 2005; 122: 669-682. Schlee M. Master sensors of pathogenic RNA - RIG-I like receptors. Immunobiology 2013; 218: 1322-1335. Ablasser A, Bauernfeind F, Hartmann G, et al. 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. Sato S, Li K, Kameyama T, et al. The RNA sensor RIG-I dually functions as an innate sensor and direct antiviral factor for hepatitis B virus. Immunity 2015; 42: 123-132. Weber F. The catcher in the RIG-I. Cytokine 2015; 76: 38-41. Gao D, Yang Y-K, Wang R-P, et al. REUL is a novel E3 ubiquitin ligase and stimulator of retinoic-acid-inducible gene-I. PLoS One 2009; 4: e5760. Oshiumi H, Matsumoto M, Hatakeyama S, et al. Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-β induction during the early phase of viral infection. J Biol Chem 2009; 284: 807-817. Oshiumi H, Miyashita M, Inoue N, et al. The ubiquitin ligase Riplet is essential for RIG-I-dependent innate immune responses to RNA virus infection. Cell Host Microbe 2010; 8: 496-509. Oshiumi H, Miyashita M, Matsumoto M, et al. A distinct role of Riplet-mediated K63-Linked polyubiquitination of the RIG-I repressor domain in human antiviral innate immune responses. PLoS Pathog 2013; 9: e1003533. Gack MU, Shin YC, Joo C-H, et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007; 446: 916-920. Zeng W, Sun L, Jiang X, et al. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 2010; 141: 315-330. Peisley A, Wu B, Xu H, et al. Structural basis for ubiquitin-mediated antiviral signal activation by RIG-I. Nature 2014; 509: 110. Zhu J, Zhang Y, Ghosh A, et al. Antiviral activity of human OASL protein is mediated by enhancing signaling of the RIG-I RNA sensor. Immunity 2014; 40: 936-948. Hsu AC-Y, Barr I, Hansbro PM, et al. Human influenza is more effective than avian influenza at antiviral suppression in airway cells. Am J Respir Cell Mol Biol 2011; 44: 906-913. Shi Y, Yuan B, Zhu W, et al. Ube2D3 and Ube2N are essential for RIG-I-mediated MAVS aggregation in antiviral innate immunity. Nat Commun 2017; 8: 15138. Meyerson NR, Zhou L, Guo YR, et al. Nuclear TRIM25 specifically targets influenza virus ribonucleoproteins to block the onset of rna chain elongation. Cell Host Microbe 2017; 22: 627-638. Diamond MS, Farzan M. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat Rev Immunol 2013; 13: 46-57. Verhelst J, Hulpiau P, Saelens X. Mx proteins: antiviral gatekeepers that restrain the uninvited. Microbiol Mol Biol Rev 2013; 77: 551-566. Klinkhammer J, Schnepf D, Ye L, et al. IFN-λ prevents influenza virus spread from the upper airways to the lungs and limits virus transmission. eLife 2018; 7: 266. Hsu AC-Y, Parsons K, Barr I, et al. Critical role of constitutive type I interferon response in bronchial epithelial cell to influenza infection. PLoS One 2012; 7: e32947. Orimo A, Inoue S, Minowa O, et al. Underdeveloped uterus and reduced estrogen responsiveness in mice with disruption of the estrogen-responsive finger protein gene, which is a direct target of estrogen receptor α. Proc Natl Acad Sci USA 1999; 96: 12027-12032. Walters MS, Gomi K, Ashbridge B, et al. Generation of a human airway epithelium derived basal cell line with multipotent differentiation capacity. Respir Res 2013; 14: 135. Cadena C, Ahmad S, Xavier A, et al. Ubiquitin-dependent and-independent roles of E3 ligase RIPLET in innate immunity. Cell Press 2019; 177: 1187-1200. Chiang C, Beljanski V, Yin K, et al. Sequence-specific modifications enhance the broad spectrum antiviral response activated by RIG-I agonists. J Virol 2015; 89: 8011-8025. Choudhury NR, Heikel G, Trubitsyna M, et al. RNA-binding activity of TRIM25 is mediated by its PRY/SPRY domain and is required for ubiquitination. BMC Biol 2017; 15: 105. Willemsen J, Wicht O, Wolanski JC, et al. Phosphorylation-dependent feedback inhibition of RIG-I by DAPK1 identified by kinome-wide siRNA screening. Mol Cell 2017; 65: 403-415. Gack MU, Albrecht RA, Urano T, 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. D'Cruz AA, Kershaw NJ, Chiang JJ, et al. Crystal structure of the TRIM25 B30.2 (PRYSPRY) domain: a key component of antiviral signalling. Biochem J 2013; 456: 231-240. Sanchez JG, Chiang JJ, Sparrer KMJ, et al. Mechanism of TRIM25 catalytic activation in the antiviral RIG-I pathway. Cell Rep 2016; 16: 1315-1325. Sanchez-Aparicio MT, Feinman LJ, García-Sastre A, et al. Paramyxovirus V proteins interact with the RIG-I/TRIM25 regulatory complex and inhibit RIG-I signaling. J Virol 2018; 92: e01960-17. D'Cruz AA, Kershaw NJ, Hayman TJ, et al. Identification of a second binding site on the TRIM25 B30.2 domain. Biochem J 2018; 475: 429-440. Koliopoulos MG, Lethier M, Van der Veen AG, et al. Molecular mechanism of influenza A NS1-mediated TRIM25 recognition and inhibition. Nat Commun 2018; 9: 1820. Pichlmair A, Schulz O, Tan C-P, et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 2006; 314: 997-1001. Loo Y-M, Fornek J, Crochet N, et al. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 2008; 82: 335-345. Rehwinkel J, Tan C-P, Goubau D, et al. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 2010; 140: 397-408. Weber M, Gawanbacht A, Habjan M, et al. Incoming RNA virus nucleocapsids containing a 5′-triphosphorylated genome activate RIG-I and antiviral signaling. Cell Host Microbe 2013; 13: 336-346. Baker PJ, Boucher D, Bierschenk D, et al. NLRP3 inflammasome activation downstream of cytoplasmic LPS recognition by both caspase-4 and caspase-5. Eur J Immunol 2015; 45: 2918-2926. Huprikar J, Rabinowitz S. A simplified plaque assay for influenza viruses in Madin-Darby kidney (MDCK) cells. J Virol Methods 1980; 1: 117-120. Kim RY, Pinkerton JW, Essilfie AT, et al. Role for NLRP3 inflammasome-mediated, IL-1β-dependent responses in severe, steroid-resistant asthma. Am J Respir Crit Care Med 2017; 196: 283-297. Linossi EM, Chandrashekaran IR, Kolesnik TB, et al. Suppressor of Cytokine Signaling (SOCS) 5 utilises distinct domains for regulation of JAK1 and interaction with the adaptor protein Shc-1. PLoS One 2013; 8: e70536. Wiśniewski JR, Zougman A, Nagaraj N, et al. Universal sample preparation method for proteome analysis. Nat Methods 2009; 6: 359-362. Kedzierski L, Tate MD, Hsu AC, et al. Suppressor of cytokine signaling (SOCS)5 ameliorates influenza infection via inhibition of EGFR signaling. eLife 2017; 6: e20444. Cox J, Neuhauser N, Michalski A, et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 2011; 10: 1794-1805. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008; 26: 1367-1372. Delconte RB, Kolesnik TB, Dagley LF, et al. CIS is a potent checkpoint in NK cell-mediated tumor immunity. Nat Immunol 2016; 17: 816-824. Keilhauer EC, Hein MY, Mann M. Accurate protein complex retrieval by affinity enrichment mass spectrometry (AE-MS) rather than affinity purification mass spectrometry (AP-MS). Mol Cell Proteom 2015; 14: 120-135. Hsu AC-Y, Starkey MR, Hanish I, et al. Targeting PI3K-p110α suppresses influenza virus infection in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2015; 191: 1012-1023. Sanchez JG, Okreglicka K, Chandrasekaran V, et al. The tripartite motif coiled-coil is an elongated antiparallel hairpin dimer. Proc Natl Acad Sci USA 2014; 111: 2494-2499. Roberts AW, Robb L, Rakar S, et al. Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc Natl Acad Sci USA 2001; 98: 9324-9329. |
فهرسة مساهمة: | Keywords: RIG-I; Riplet; TRIM25; influenza |
المشرفين على المادة: | 0 (Antiviral Agents) 0 (DNA-Binding Proteins) 0 (Ligands) 0 (Receptors, Immunologic) 0 (Transcription Factors) 0 (Trim25 protein, mouse) 0 (Tripartite Motif Proteins) 63231-63-0 (RNA) EC 2.3.2.27 (RNF135 protein, human) EC 2.3.2.27 (Rnf135 protein, mouse) EC 2.3.2.27 (TRIM25 protein, human) EC 2.3.2.27 (Ubiquitin-Protein Ligases) EC 3.6.1.- (RIGI protein, human) EC 3.6.1.- (Ddx58 protein, mouse) EC 3.6.4.13 (DEAD Box Protein 58) |
تواريخ الأحداث: | Date Created: 20190724 Date Completed: 20200417 Latest Revision: 20231213 |
رمز التحديث: | 20240628 |
DOI: | 10.1111/imcb.12284 |
PMID: | 31335993 |
قاعدة البيانات: | MEDLINE |
كن أول من يترك تعليقا!