ABIN1 is a signal-induced autophagy receptor that attenuates NF-κB activation by recognizing linear ubiquitin chains.
ABIN1
MyDDosome
NF-κB
autophagy
linear ubiquitination
toll-like receptors
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
revised:
03
02
2022
received:
21
11
2021
accepted:
15
02
2022
pubmed:
26
2
2022
medline:
20
5
2022
entrez:
25
2
2022
Statut:
ppublish
Résumé
Linear ubiquitin chains play pivotal roles in immune signaling by augmenting NF-κB activation and suppressing programmed cell death induced by various stimuli. A20-binding inhibitor of NF-κB 1 (ABIN1) binds to linear ubiquitin chains and attenuates NF-κB activation and cell death induction. Although interactions with linear ubiquitin chains are thought to play a role in ABIN1-mediated suppression of NF-κB and cell death, the underlying molecular mechanisms remain unclear. Here, we show that upon stimulation by Toll-like receptor (TLR) ligands, ABIN1 is phosphorylated on Ser 83 and functions as a selective autophagy receptor. ABIN1 recognizes components of the MyD88 signaling complex via interaction with linear ubiquitin chains conjugated to components of the complex in TLR signaling, which leads to autophagic degradation of signaling proteins and attenuated NF-κB signaling. Our current findings indicate that phosphorylation and linear ubiquitination also play a role in downregulation of signaling via selective induction of autophagy.
Identifiants
pubmed: 35213742
doi: 10.1002/1873-3468.14323
doi:
Substances chimiques
NF-kappa B
0
Toll-Like Receptors
0
Ubiquitin
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1147-1164Informations de copyright
© 2022 Federation of European Biochemical Societies.
Références
Ciehanover A, Hod Y, Hershko A. A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes. Biochem Biophys Res Commun. 1978;81:1100-5.
Kornitzer D, Ciechanover A. Modes of regulation of ubiquitin-mediated protein degradation. J Cell Physiol. 2000;182:1-11.
Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem. 1998;67:425-79.
Kirisako T, Kamei K, Murata S, Kato M, Fukumoto H, Kanie M, et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 2006;25:4877-87.
Tokunaga F, Sakata S, Saeki Y, Satomi Y, Kirisako T, Kamei K, et al. Involvement of linear polyubiquitylation of NEMO in NF-κB activation. Nat Cell Biol. 2009;11:123-32.
Iwai K, Fujita H, Sasaki Y. Linear ubiquitin chains: NF-κB signalling, cell death and beyond. Nat Rev Mol Cell Biol. 2014;15:503-8.
Fujita H, Tokunaga A, Shimizu S, Whiting AL, Aguilar-Alonso F, Takagi K, et al. Cooperative domain formation by homologous motifs in HOIL-1L and SHARPIN plays A crucial role in LUBAC stabilization. Cell Rep. 2018;23:1192-204.
Rahighi S, Ikeda F, Kawasaki M, Akutsu M, Suzuki N, Kato R, et al. Specific recognition of linear ubiquitin chains by NEMO is important for NF-κB activation. Cell. 2009;136:1098-109.
Lo YC, Lin SC, Rospigliosi CC, Conze DB, Wu CJ, Ashwell JD, et al. Structural basis for recognition of diubiquitins by NEMO, Mol. Cell. 2009;33:602-15.
Wagner S, Carpentier I, Rogov V, Kreike M, Ikeda F, Lohr F, et al. Ubiquitin binding mediates the NF-κB inhibitory potential of ABIN proteins. Oncogene. 2008;27:3739-45.
Maruyama H, Morino H, Ito H, Izumi Y, Kato H, Watanabe Y, et al. Mutations of optineurin in amyotrophic lateral sclerosis. Nature. 2010;465:223-6.
Wong YC, Holzbaur EL. Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc Natl Acad Sci USA. 2014;111:E4439-48.
Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science. 2011;333:228-33.
Nanda SK, Venigalla RK, Ordureau A, Patterson-Kane JC, Powell DW, Toth R, et al. Polyubiquitin binding to ABIN1 is required to prevent autoimmunity. J Exp Med. 2011;208:1215-28.
G'Sell RT, Gaffney PM, Powell DW. A20-binding inhibitor of NF-kappaB activation 1 is a physiologic inhibitor of NF-κB: a molecular switch for inflammation and autoimmunity. Arthritis Rheumatol. 2015;67:2292-302.
Gateva V, Sandling JK, Hom G, Taylor KE, Chung SA, Sun X, et al. A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet. 2009;41:1228-33.
Tsoi LC, Spain SL, Knight J, Ellinghaus E, Stuart PE, Capon F, et al. Identification of 15 new psoriasis susceptibility loci highlights the role of innate immunity. Nat Genet. 2012;44:1341-8.
Zhou J, Wu R, High AA, Slaughter CA, Finkelstein D, Rehg JE, et al. A20-binding inhibitor of NF-κB (ABIN1) controls Toll-like receptor-mediated CCAAT/enhancer-binding protein β activation and protects from inflammatory disease. Proc Natl Acad Sci USA. 2011;108:E998-1006.
Santiago-Raber ML, Kikuchi S, Borel P, Uematsu S, Akira S, Kotzin BL, et al. Evidence for genes in addition to Tlr7 in the Yaa translocation linked with acceleration of systemic lupus erythematosus. J Immunol. 2008;181:1556-62.
Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8:2281-308.
Sanjana NE, Shalem O, Zhang F. Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods. 2014;11:783-4.
Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW, Levy JM, et al. Search-and-replace genome editing without double-strand breaks or donor DNA. Nature. 2019;576:149-57.
Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol. 2013;31:822-6.
Herhaus L, van den Bedem H, Tang S, Maslennikov I, Wakatsuki S, Dikic I, et al. Molecular recognition of M1-linked ubiquitin chains by native and phosphorylated UBAN domains. J Mol Biol. 2019;431:3146-56.
Hjerpe R, Aillet F, Lopitz-Otsoa F, Lang V, England P, Rodriguez MS. Efficient protection and isolation of ubiquitylated proteins using tandem ubiquitin-binding entities. EMBO Rep. 2009;10:1250-8.
van Wijk SJ, Fiskin E, Dikic I. Selective monitoring of ubiquitin signals with genetically encoded ubiquitin chain-specific sensors. Nat Protoc. 2013;8:1449-58.
Masuda T, Tomita M, Ishihama Y. Phase transfer surfactant-aided trypsin digestion for membrane proteome analysis. J Proteome Res. 2008;7:731-40.
Rappsilber J, Mann M, Ishihama Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc. 2007;2:1896-906.
Ishihama Y, Rappsilber J, Andersen JS, Mann M. Microcolumns with self-assembled particle frits for proteomics. J Chromatogr A. 2002;979:233-9.
Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011;10:1794-805.
Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods. 2016;13:731-40.
Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147:728-41.
Rogov V, Dotsch V, Johansen T, Kirkin V. Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol Cell. 2014;53:167-78.
Zhu Y, Massen S, Terenzio M, Lang V, Chen-Lindner S, Eils R, et al. Modulation of serines 17 and 24 in the LC3-interacting region of Bnip3 determines pro-survival mitophagy versus apoptosis. J Biol Chem. 2013;288:1099-113.
Balka KR, De Nardo D. Understanding early TLR signaling through the Myddosome. J Leukoc Biol. 2019;105:339-51.
Doyle SL, O'Neill LA. Toll-like receptors: from the discovery of NFκB to new insights into transcriptional regulations in innate immunity. Biochem Pharmacol. 2006;72:1102-13.
Emmerich CH, Ordureau A, Strickson S, Arthur JS, Pedrioli PG, Komander D, et al. Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc Natl Acad Sci USA. 2013;110:15247-52.
Oikawa D, Sato Y, Ohtake F, Komakura K, Hanada K, Sugawara K, et al. Molecular bases for HOIPINs-mediated inhibition of LUBAC and innate immune responses. Commun Biol. 2020;3:163.
Heyninck K, De Valck D, Vanden Berghe W, Van Criekinge W, Contreras R, Fiers W, et al. The zinc finger protein A20 inhibits TNF-induced NF-κB-dependent gene expression by interfering with an RIP- or TRAF2-mediated transactivation signal and directly binds to a novel NF-κB-inhibiting protein ABIN. J Cell Biol. 1999;145:1471-82.
Oshima S, Turer EE, Callahan JA, Chai S, Advincula R, Barrera J, et al. ABIN-1 is a ubiquitin sensor that restricts cell death and sustains embryonic development. Nature. 2009;457:906-9.
Mejlvang J, Olsvik H, Svenning S, Bruun JA, Abudu YP, Larsen KB, et al. Starvation induces rapid degradation of selective autophagy receptors by endosomal microautophagy. J Cell Biol. 2018;217:3640-55.
Zellner S, Schifferer M, Behrends C. Systematically defining selective autophagy receptor-specific cargo using autophagosome content profiling. Mol Cell. 2021;81:1337-1354 e1338.
Gentle IE. Supramolecular complexes in cell death and inflammation and their regulation by autophagy. Front Cell Dev Biol. 2019;7:73.
Kelsall IR, Zhang J, Knebel A, Arthur JSC, Cohen P. The E3 ligase HOIL-1 catalyses ester bond formation between ubiquitin and components of the Myddosome in mammalian cells. Proc Natl Acad Sci USA. 2019;116:13293-8.
Goto E, Tokunaga F. Decreased linear ubiquitination of NEMO and FADD on apoptosis with caspase-mediated cleavage of HOIP. Biochem Biophys Res Commun. 2017;485:152-9.
Zhu G, Wu CJ, Zhao Y, Ashwell JD. Optineurin negatively regulates TNFalpha- induced NF-κB activation by competing with NEMO for ubiquitinated RIP. Curr Biol. 2007;17:1438-43.
Nakazawa S, Oikawa D, Ishii R, Ayaki T, Takahashi H, Takeda H, et al. Linear ubiquitination is involved in the pathogenesis of optineurin-associated amyotrophic lateral sclerosis. Nat Commun. 2016;7:12547.
Slowicka K, Vereecke L, Mc Guire C, Sze M, Maelfait J, Kolpe A, et al. Optineurin deficiency in mice is associated with increased sensitivity to Salmonella but does not affect proinflammatory NF-kappaB signaling. Eur J Immunol. 2016;46:971-80.
Pisitkun P, Deane JA, Difilippantonio MJ, Tarasenko T, Satterthwaite AB, Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science. 2006;312:1669-72.
Lee YH, Choi SJ, Ji JD, Song GG. Association between toll-like receptor polymorphisms and systemic lupus erythematosus: a meta-analysis update. Lupus. 2016;25:593-601.
Celhar T, Lu HK, Benso L, Rakhilina L, Lee HY, Tripathi S, et al. TLR7 protein expression in mild and severe lupus-prone models is regulated in a leukocyte, genetic, and IRAK4 dependent manner. Front Immunol. 2019;10:1546.
Nanda SK, Lopez-Pelaez M, Arthur JS, Marchesi F, Cohen P. Suppression of IRAK1 or IRAK4 catalytic activity, but not type 1 IFN signaling, prevents lupus nephritis in mice expressing a ubiquitin binding-defective mutant of ABIN1. J Immunol. 2016;197:4266-73.
Moriya Y, Kawano S, Okuda S, Watanabe Y, Matsumoto M, Takami T, et al. The jPOST environment: an integrated proteomics data repository and database. Nucleic Acids Res. 2019;47:D1218-24.