Pellino3 ligase negatively regulates influenza B dependent RIG-I signalling through downregulation of TRAF3-mediated induction of the transcription factor IRF3 and IFNβ production.


Journal

Immunology
ISSN: 1365-2567
Titre abrégé: Immunology
Pays: England
ID NLM: 0374672

Informations de publication

Date de publication:
07 2023
Historique:
received: 06 10 2022
accepted: 19 02 2023
medline: 16 6 2023
pubmed: 3 3 2023
entrez: 2 3 2023
Statut: ppublish

Résumé

Viral infection activates the innate immune system, which recognizes viral components by a variety of pattern recognition receptors and initiates signalling cascades leading to the production of pro-inflammatory cytokines. To date, signalling cascades triggered after virus recognition are not fully characterized and are investigated by many research groups. The critical role of the E3 ubiquitin ligase Pellino3 in antibacterial and antiviral response is now widely accepted, but the precise mechanism remains elusive. In this study, we sought to explore Pellino3 role in the retinoic acid-inducible gene I (RIG-I)-dependent signalling pathway. In this work, the molecular mechanisms of the innate immune response, regulated by Pellino3, were investigated in lung epithelial cells during influenza B virus infection. We used wild-type and Pellino3-deficient A549 cells as model cell lines to examine the role of Pellino3 ligase in the type I interferon (IFN) signalling pathway. Our results indicate that Pellino3 is involved in direct ubiquitination and degradation of the TRAF3, suppressing interferon regulatory factor 3 (IRF3) activation and interferon beta (IFNβ) production.

Identifiants

pubmed: 36861386
doi: 10.1111/imm.13637
doi:

Substances chimiques

TNF Receptor-Associated Factor 3 0
Interferon Regulatory Factor-3 0
Ubiquitin-Protein Ligases EC 2.3.2.27
IRF3 protein, human 0
TRAF3 protein, human 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

369-383

Informations de copyright

© 2023 John Wiley & Sons Ltd.

Références

Chang HL, Hsu JF, Tsai YM, Lin SY, Kuo HF, Yang CJ. Acute respiratory distress syndrome and acute myocarditis developed in a previously healthy adult with influenza B. BMC Pulm Med. 2016;16(1):3-7.
Sellers SA, Hagan RS, Hayden FG, Fischer WA. The hidden burden of influenza: a review of the extra-pulmonary complications of influenza infection. Influenza Other Respi Viruses. 2017;11(5):372-93.
Caini S, Kusznierz G, Garate VV, Wangchuk S, Thapa B, De Paula FJ, et al. The epidemiological signature of influenza B virus and its B/Victoria and B/Yamagata lineages in the 21st century. PLoS One. 2019;14(9):1-17.
Zaraket H, Hurt AC, Clinch B, Barr I, Lee N. Burden of influenza B virus infection and considerations for clinical management. Antiviral Res. 2021;185:104970.
Hatta M, Goto H, Kawaoka Y. Influenza B virus requires BM2 protein for replication. J Virol. 2004;78(11):5576-83.
Westenius V, Latvala S, Diamond MS, Gale M, Julkunen I. RIG-I signaling is essential for influenza B virus-induced rapid interferon gene expression. J Virol. 2015;89(23):12014-25.
Rehwinkel J, Gack MU. RIG-I-like receptors: their regulation and roles in RNA sensing. Nat Rev Immunol. 2020;20(9):537-51. https://doi.org/10.1038/s41577-020-0288-3
Onomoto K, Onoguchi K, Yoneyama M. Regulation of RIG-I-like receptor-mediated signaling: interaction between host and viral factors. Cell Mol Immunol. 2021;18(3):539-55.
Ren Z, Ding T, Zuo Z, Xu Z, Deng J, Wei Z. Regulation of MAVS expression and signaling function in the antiviral innate immune response. Front Immunol. 2020;11:1030.
Fang R, Jiang Q, Zhou X, Wang C, Guan Y, Tao J, et al. MAVS activates TBK1 and IKKε through TRAFs in NEMO dependent and independent manner. PLoS Pathog. 2017;13(11):1-22.
Reniewicz P, Kula A, Makuch E, Ochnik M, Lipiński T, Siednienko J. Ligase Pellino3 regulates macrophage action and survival in response to VSV infection in RIG-I-dependent path. Oxid Med Cell Longev. 2021;2021:6668463.
Butler MP, Hanly JA, Moynagh PN. Pellino3 is a novel upstream regulator of p38 MAPK and activates CREB in a p38-dependent manner. J Biol Chem. 2005;280(30):27759-68. https://doi.org/10.1074/jbc.M500756200
Jensen LE, Whitehead AS. Pellino3, a novel member of the Pellino protein family, promotes activation of c-Jun and Elk-1 and may act as a scaffolding protein. J Immunol. 2003;171(3):1500-6.
Siednienko J, Jackson R, Mellett M, Delagic N, Yang S, Wang B, et al. Pellino3 targets the IRF7 pathway and facilitates autoregulation of TLR3-and viral-induced expression of type I interferons. Nat Immunol. 2012;13(11):1055-62.
Smith SM, Freeley M, Moynagh PN, Kelleher DP. Differential modulation of Helicobacter pylori lipopolysaccharide-mediated TLR2 signaling by individual Pellino proteins. Helicobacter. 2017;22(1):1-14.
Murphy MB, Xiong Y, Pattabiraman G, Manavalan TT, Qiu F, Medvedev AE. Pellino-3 promotes endotoxin tolerance and acts as a negative regulator of TLR2 and TLR4 signaling. J Leukoc Biol. 2015;98(6):963-74.
Yang S, Wang B, Tang LS, Siednienko J, Callanan JJ, Moynagh PN. Pellino3 targets RIP1 and regulates the pro-apoptotic effects of TNF-α. Nat Commun. 2013;4:2583.
Yang S, Wang B, Humphries F, Jackson R, Healy ME, Bergin R, et al. Pellino3 ubiquitinates RIP2 and mediates Nod2-induced signaling and protective effects in colitis. Nat Immunol. 2013;14(9):927-36.
Herold S, Becker C, Ridge KM, Budinger GRS. Influenza virus-induced lung injury: pathogenesis and implications for treatment. Eur Respir J. 2015;45(5):1463-78.
Dumm RE, Fiege JK, Waring BM, Kuo CT, Langlois RA, Heaton NS. Non-lytic clearance of influenza B virus from infected cells preserves epithelial barrier function. Nat Commun. 2019;10(1):1-15.
Watson A, Spalluto CM, McCrae C, Cellura D, Burke H, Cunoosamy D, et al. Dynamics of IFN-β responses during respiratory viral infection insights for therapeutic strategies. Am J Respir Crit Care Med. 2020;201(1):83-94.
Li W, Wang H, Zheng SJ. Roles of RNA sensors in host innate response to influenza virus and coronavirus infections. Int J Mol Sci. 2022;23(15):8285.
Tissari J, Sirén J, Meri S, Julkunen I, Matikainen S. IFN-α enhances TLR3-mediated antiviral cytokine expression in human endothelial and epithelial cells by up-regulating TLR3 expression. J Immunol. 2005;174(7):4289-94.
Mikkelsen SS, Jensen SB, Chiliveru S, Melchjorsen J, Julkunen I, Gaestel M, et al. RIG-I-mediated activation of p38 MAPK is essential for viral induction of interferon and activation of dendritic cells. Dependence on TRAF2 and TAK1. J Biol Chem. 2009;284(16):10774-82.
Huang MT, Chen ST, Wu HY, Chen YJ, Chou TY, Hsieh SL. DcR3 suppresses influenza virus-induced macrophage activation and attenuates pulmonary inflammation and lethality. J Mol Med. 2015;93(10):1131-43.
Lee JC, Young PR. Role of CSBP/p38/RK stress response kinase in LPS and cytokine signaling mechanisms. J Leukoc Biol. 1996;59(2):152-7.
Panne D, Maniatis T, Harrison SC. Crystal structure of ATF-2/c-Jun and IRF-3 bound to the interferon-β enhancer. EMBO J. 2004;23(22):4384-93.
Paz S, Vilasco M, Werden SJ, Arguello M, Joseph-Pillai D, Zhao T, et al. A functional C-terminal TRAF3-binding site in MAVS participates in positive and negative regulation of the IFN antiviral response. Cell Res. 2011;21(6):895-910.
Buttmann M, Berberich-Siebelt F, Serfling E, Rieckmann P. Interferon-β is a potent inducer of interferon regulatory factor-1/2-dependent IP-10/CXCL10 expression in primary human endothelial cells. J Vasc Res. 2007;44(1):51-60.
Tolomeo M, Cavalli A, Cascio A. STAT1 and its crucial role in the control of viral infections. Int J Mol Sci. 2022;23:4095.
Zhang Y, Xu Z, Cao Y. Host antiviral responses against avian infectious bronchitis virus (Ibv): focus on innate immunity. Viruses. 2021;13(9):1698.
Bowie AG, Unterholzner L. Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol. 2008;8(12):911-22.
Liu GQ, Lu Y, Thulasi Raman SN, Xu F, Wu Q, Li Z, et al. Nuclear-resident RIG-I senses viral replication inducing antiviral immunity. Nat Commun. 2018;9(1):3199.
García-Sastre A. Induction and evasion of type I interferon responses by influenza viruses. Virus Res. 2011;162(1-2):12-8.
Biondo C, Lentini G, Beninati C, Teti G. The dual role of innate immunity during influenza. Biomed J. 2019;42(1):8-18.
Killip MJ, Fodor E, Randall RE. Influenza virus activation of the interferon system. Virus Res. 2015;209:11-22. https://doi.org/10.1016/j.virusres.2015.02.003
James SJ, Jiao H, Teh HY, Takahashi H, Png CW, Phoon MC, et al. MAPK phosphatase 5 expression induced by influenza and other RNA virus infection negatively regulates IRF3 activation and type I interferon response. Cell Rep. 2015;10(10):1722-34. https://doi.org/10.1016/j.celrep.2015.02.030
Dhillon B, Aleithan F, Abdul-Sater Z, Abdul-Sater AA. The evolving role of TRAFs in mediating inflammatory responses. Front Immunol. 2019;10:1-8.
Gu L, Fullam A, McCormack N, Höhn Y, Schröder M. DDX3 directly regulates TRAF3 ubiquitination and acts as a scaffold to co-ordinate assembly of signalling complexes downstream from MAVS. Biochem J. 2017;474(4):571-87.
Li S, Zheng H, Mao AP, Zhong B, Li Y, Liu Y, et al. Regulation of virus-triggered signaling by OTUB1- and OTUB2-mediated deubiquitination of TRAF3 and TRAF6. J Biol Chem. 2010;285(7):4291-7. https://doi.org/10.1074/jbc.M109.074971
Kayagaki N, Phung Q, Chan S, Chaudhari R, Quan C, O'Rourke KM, et al. DUBA: a deubiquitinase that regulates type I interferon production. Science. 2007;318(5856):1628-32. https://doi.org/10.1126/science.1145918
Nakhaei P, Mesplede T, Solis M, Sun Q, Zhao T, Yang L, et al. The E3 ubiquitin ligase Triad3A negatively regulates the RIG-I/MAVS signaling pathway by targeting TRAF3 for degradation. PLoS Pathog. 2009;5(11):1-14.
Tseng PH, Matsuzawa A, Zhang W, Mino T, Vignali DA, Karin M. Different modes of ubiquitination of the adaptor TRAF3 selectively activate the expression of type I interferons and proinflammatory cytokines. Nat Immunol. 2010;11(1):70-5. https://doi.org/10.1038/ni.1819
Davis ME, Gack MU. Ubiquitination in the antiviral immune response. Virology. 2015;479-480:52-65.
Katze MG, He Y, Gale M. Viruses and interferon: a fight for supremacy. Nat Rev Immunol. 2002;2(9):675-87.
Wang Y, Song Q, Huang W, Lin Y, Wang X, Wang C, et al. A virus-induced conformational switch of STAT1-STAT2 dimers boosts antiviral defenses. Cell Res. 2021;31(2):206-18.
Herzig DS, Luan L, Bohannon JK, Toliver-Kinsky TE, Guo Y, Sherwood ER. The role of CXCL10 in the pathogenesis of experimental septic shock. Crit Care. 2014;18(3):1-18.
Li X, Liu S, Rai KR, Zhou W, Wang S, Chi X, et al. Initial activation of STAT2 induced by IAV infection is critical for innate antiviral immunity. Front Immunol. 2022;13:960544. https://doi.org/10.3389/fimmu.2022.960544

Auteurs

Anna Kula (A)

Bioengineering Research Group, Łukasiewicz Research Network - PORT Polish Center for Technology Development, Wroclaw, Poland.
Laboratory of Medical Microbiology, Ludwik Hirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of Sciences, Wroclaw, Poland.

Edyta Makuch (E)

Bioengineering Research Group, Łukasiewicz Research Network - PORT Polish Center for Technology Development, Wroclaw, Poland.

Marta Lisowska (M)

Bioengineering Research Group, Łukasiewicz Research Network - PORT Polish Center for Technology Development, Wroclaw, Poland.

Patryk Reniewicz (P)

Bioengineering Research Group, Łukasiewicz Research Network - PORT Polish Center for Technology Development, Wroclaw, Poland.

Tomasz Lipiński (T)

Bioengineering Research Group, Łukasiewicz Research Network - PORT Polish Center for Technology Development, Wroclaw, Poland.

Jakub Siednienko (J)

Bioengineering Research Group, Łukasiewicz Research Network - PORT Polish Center for Technology Development, Wroclaw, Poland.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH