دورية أكاديمية
أعرض في EDS

NINJ1 mediates plasma membrane rupture during lytic cell death.

التفاصيل البيبلوغرافية
العنوان: NINJ1 mediates plasma membrane rupture during lytic cell death.
المؤلفون: Kayagaki N; Department of Physiological Chemistry, Genentech Inc., South San Francisco, CA, USA. kayagaki@gene.com., Kornfeld OS; Department of Physiological Chemistry, Genentech Inc., South San Francisco, CA, USA., Lee BL; Department of Physiological Chemistry, Genentech Inc., South San Francisco, CA, USA., Stowe IB; Department of Physiological Chemistry, Genentech Inc., South San Francisco, CA, USA., O'Rourke K; Department of Physiological Chemistry, Genentech Inc., South San Francisco, CA, USA., Li Q; Department of Microchemistry, Proteomics and Lipidomics, Genentech Inc., South San Francisco, CA, USA., Sandoval W; Department of Microchemistry, Proteomics and Lipidomics, Genentech Inc., South San Francisco, CA, USA., Yan D; Department of Translational Immunology, Genentech Inc., South San Francisco, CA, USA., Kang J; Department of Translational Immunology, Genentech Inc., South San Francisco, CA, USA., Xu M; Department of Translational Immunology, Genentech Inc., South San Francisco, CA, USA., Zhang J; Department of Translational Immunology, Genentech Inc., South San Francisco, CA, USA., Lee WP; Department of Translational Immunology, Genentech Inc., South San Francisco, CA, USA., McKenzie BS; Department of Translational Immunology, Genentech Inc., South San Francisco, CA, USA., Ulas G; Department of Biochemical and Cellular Pharmacology, Genentech Inc., South San Francisco, CA, USA., Payandeh J; Department of Structural Biology, Genentech Inc., South San Francisco, CA, USA., Roose-Girma M; Department of Molecular Biology, Genentech Inc., South San Francisco, CA, USA., Modrusan Z; Department of Microchemistry, Proteomics and Lipidomics, Genentech Inc., South San Francisco, CA, USA., Reja R; Department of Bioinformatics, Genentech Inc., South San Francisco, CA, USA., Sagolla M; Department of Pathology, Genentech Inc., South San Francisco, CA, USA., Webster JD; Department of Pathology, Genentech Inc., South San Francisco, CA, USA., Cho V; The Australian Phenomics Facility, The John Curtin School of Medical Research, The Australian National University, Canberra, Australian Capital Territory, Australia.; Department of Immunology and Infectious Diseases, The John Curtin School of Medical Research, The Australian National University, Canberra, Australian Capital Territory, Australia., Andrews TD; Department of Immunology and Infectious Diseases, The John Curtin School of Medical Research, The Australian National University, Canberra, Australian Capital Territory, Australia., Morris LX; The Australian Phenomics Facility, The John Curtin School of Medical Research, The Australian National University, Canberra, Australian Capital Territory, Australia., Miosge LA; The Australian Phenomics Facility, The John Curtin School of Medical Research, The Australian National University, Canberra, Australian Capital Territory, Australia.; Department of Immunology and Infectious Diseases, The John Curtin School of Medical Research, The Australian National University, Canberra, Australian Capital Territory, Australia., Goodnow CC; Garvan Institute of Medical Research, Sydney, New South Wales, Australia.; Cellular Genomics Futures Institute, UNSW Sydney, Sydney, New South Wales, Australia., Bertram EM; The Australian Phenomics Facility, The John Curtin School of Medical Research, The Australian National University, Canberra, Australian Capital Territory, Australia.; Department of Immunology and Infectious Diseases, The John Curtin School of Medical Research, The Australian National University, Canberra, Australian Capital Territory, Australia., Dixit VM; Department of Physiological Chemistry, Genentech Inc., South San Francisco, CA, USA. dixit@gene.com.
المصدر: Nature [Nature] 2021 Mar; Vol. 591 (7848), pp. 131-136. Date of Electronic Publication: 2021 Jan 20.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE
أسماء مطبوعة: Publication: Basingstoke : Nature Publishing Group
Original Publication: London, Macmillan Journals ltd.
مواضيع طبية MeSH: Cell Death*/genetics, Cell Adhesion Molecules, Neuronal/*metabolism , Cell Membrane/*metabolism , Nerve Growth Factors/*metabolism, Animals ; Apoptosis ; Cell Adhesion Molecules, Neuronal/chemistry ; Cell Adhesion Molecules, Neuronal/genetics ; Female ; Humans ; Macrophages ; Male ; Mice ; Mutation ; Necrosis ; Nerve Growth Factors/chemistry ; Nerve Growth Factors/genetics ; Protein Multimerization ; Pyroptosis/genetics
مستخلص: Plasma membrane rupture (PMR) is the final cataclysmic event in lytic cell death. PMR releases intracellular molecules known as damage-associated molecular patterns (DAMPs) that propagate the inflammatory response 1-3 . The underlying mechanism of PMR, however, is unknown. Here we show that the cell-surface NINJ1 protein 4-8 , which contains two transmembrane regions, has an essential role in the induction of PMR. A forward-genetic screen of randomly mutagenized mice linked NINJ1 to PMR. Ninj1 -/- macrophages exhibited impaired PMR in response to diverse inducers of pyroptotic, necrotic and apoptotic cell death, and were unable to release numerous intracellular proteins including HMGB1 (a known DAMP) and LDH (a standard measure of PMR). Ninj1 -/- macrophages died, but with a distinctive and persistent ballooned morphology, attributable to defective disintegration of bubble-like herniations. Ninj1 -/- mice were more susceptible than wild-type mice to infection with Citrobacter rodentium, which suggests a role for PMR in anti-bacterial host defence. Mechanistically, NINJ1 used an evolutionarily conserved extracellular domain for oligomerization and subsequent PMR. The discovery of NINJ1 as a mediator of PMR overturns the long-held idea that cell death-related PMR is a passive event.
التعليقات: Comment in: Nature. 2021 Mar;591(7848):36-37. (PMID: 33558750)
Comment in: Mol Cell. 2021 Apr 1;81(7):1370-1371. (PMID: 33798414)
Comment in: Fac Rev. 2022 Dec 30;11:41. (PMID: 36644292)
References: Fink, S. L. & Cookson, B. T. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 73, 1907–1916 (2005). (PMID: 15784530108741310.1128/IAI.73.4.1907-1916.2005)
Gaidt, M. M. & Hornung, V. Pore formation by GSDMD is the effector mechanism of pyroptosis. EMBO J. 35, 2167–2169 (2016). (PMID: 27572465506955410.15252/embj.201695415)
Kayagaki, N. & Dixit, V. M. Rescue from a fiery death: a therapeutic endeavor. Science 366, 688–689 (2019). (PMID: 3169992410.1126/science.aaw1177)
Araki, T. & Milbrandt, J. Ninjurin, a novel adhesion molecule, is induced by nerve injury and promotes axonal growth. Neuron 17, 353–361 (1996). (PMID: 878065810.1016/S0896-6273(00)80166-X)
Araki, T., Zimonjic, D. B., Popescu, N. C. & Milbrandt, J. Mechanism of homophilic binding mediated by ninjurin, a novel widely expressed adhesion molecule. J. Biol. Chem. 272, 21373–21380 (1997). (PMID: 926115110.1074/jbc.272.34.21373)
Ahn, B. J. et al. The N-terminal ectodomain of Ninjurin1 liberated by MMP9 has chemotactic activity. Biochem. Biophys. Res. Commun. 428, 438–444 (2012). (PMID: 23142597371284510.1016/j.bbrc.2012.10.099)
Lee, H. J. et al. Ninjurin1 mediates macrophage-induced programmed cell death during early ocular development. Cell Death Differ. 16, 1395–1407 (2009). (PMID: 1955700810.1038/cdd.2009.78)
Yang, H. J. et al. Ninjurin 1 has two opposing functions in tumorigenesis in a p53-dependent manner. Proc. Natl Acad. Sci. USA 114, 11500–11505 (2017). (PMID: 29073078566454110.1073/pnas.1711814114)
Cookson, B. T. & Brennan, M. A. Pro-inflammatory programmed cell death. Trends Microbiol. 9, 113–114 (2001). (PMID: 1130350010.1016/S0966-842X(00)01936-3)
Shi, J. et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526, 660–665 (2015). (PMID: 2637500310.1038/nature15514)
Kayagaki, N. et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526, 666–671 (2015). (PMID: 2637525910.1038/nature15541)
Ding, J. et al. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535, 111–116 (2016). (PMID: 2728121610.1038/nature18590)
Liu, X. et al. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535, 153–158 (2016). (PMID: 27383986553998810.1038/nature18629)
Fink, S. L. & Cookson, B. T. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol. 8, 1812–1825 (2006). (PMID: 1682404010.1111/j.1462-5822.2006.00751.x)
Ruan, J., Xia, S., Liu, X., Lieberman, J. & Wu, H. Cryo-EM structure of the gasdermin A3 membrane pore. Nature 557, 62–67 (2018). (PMID: 29695864600797510.1038/s41586-018-0058-6)
Kayagaki, N. et al. Non-canonical inflammasome activation targets caspase-11. Nature 479, 117–121 (2011). (PMID: 2200260810.1038/nature10558)
de Vasconcelos, N. M., Van Opdenbosch, N., Van Gorp, H., Parthoens, E. & Lamkanfi, M. Single-cell analysis of pyroptosis dynamics reveals conserved GSDMD-mediated subcellular events that precede plasma membrane rupture. Cell Death Differ. 26, 146–161 (2019). (PMID: 2966647710.1038/s41418-018-0106-7)
DiPeso, L., Ji, D. X., Vance, R. E. & Price, J. V. Cell death and cell lysis are separable events during pyroptosis. Cell Death Discov. 3, 17070 (2017). (PMID: 29147575568287910.1038/cddiscovery.2017.70)
Andersson, U. & Tracey, K. J. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu. Rev. Immunol. 29, 139–162 (2011). (PMID: 21219181453655110.1146/annurev-immunol-030409-101323)
Štros, M. HMGB proteins: interactions with DNA and chromatin. Biochim. Biophys. Acta 1799, 101–113 (2010). (PMID: 2012307210.1016/j.bbagrm.2009.09.008)
Silva, M. T. Secondary necrosis: the natural outcome of the complete apoptotic program. FEBS Lett. 584, 4491–4499 (2010). (PMID: 2097414310.1016/j.febslet.2010.10.046)
Ashkenazi, A., Fairbrother, W. J., Leverson, J. D. & Souers, A. J. From basic apoptosis discoveries to advanced selective BCL-2 family inhibitors. Nat. Rev. Drug Discov. 16, 273–284 (2017). (PMID: 2820999210.1038/nrd.2016.253)
Dijkstra, K., Hofmeijer, J., van Gils, S. A. & van Putten, M. J. A biophysical model for cytotoxic cell swelling. J. Neurosci. 36, 11881–11890 (2016). (PMID: 27881775660491810.1523/JNEUROSCI.1934-16.2016)
Sun, L. et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148, 213–227 (2012). (PMID: 2226541310.1016/j.cell.2011.11.031)
Grootjans, S., Vanden Berghe, T. & Vandenabeele, P. Initiation and execution mechanisms of necroptosis: an overview. Cell Death Differ. 24, 1184–1195 (2017). (PMID: 28498367552017210.1038/cdd.2017.65)
Drin, G. & Antonny, B. Amphipathic helices and membrane curvature. FEBS Lett. 584, 1840–1847 (2010). (PMID: 1983706910.1016/j.febslet.2009.10.022)
Peter, B. J. et al. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495–499 (2004). (PMID: 1464585610.1126/science.1092586)
Auluck, P. K., Caraveo, G. & Lindquist, S. α-Synuclein: membrane interactions and toxicity in Parkinson’s disease. Annu. Rev. Cell Dev. Biol. 26, 211–233 (2010). (PMID: 2050009010.1146/annurev.cellbio.042308.113313)
Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 415, 389–395 (2002). (PMID: 1180754510.1038/415389a)
Hatzakis, N. S. et al. How curved membranes recruit amphipathic helices and protein anchoring motifs. Nat. Chem. Biol. 5, 835–841 (2009). (PMID: 1974974310.1038/nchembio.213)
Nelms, K. A. & Goodnow, C. C. Genome-wide ENU mutagenesis to reveal immune regulators. Immunity 15, 409–418 (2001). (PMID: 1156763110.1016/S1074-7613(01)00199-6)
Kayagaki, N. et al. IRF2 transcriptionally induces GSDMD expression for pyroptosis. Sci. Signal. 12, eaax4917 (2019). (PMID: 3111385110.1126/scisignal.aax4917)
Andrews, T. D. et al. Massively parallel sequencing of the mouse exome to accurately identify rare, induced mutations: an immediate source for thousands of new mouse models. Open Biol. 2, 120061 (2012). (PMID: 22724066337674010.1098/rsob.120061)
Murphy, J. M. et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39, 443–453 (2013). (PMID: 2401242210.1016/j.immuni.2013.06.018)
Modzelewski, A. J. et al. Efficient mouse genome engineering by CRISPR-EZ technology. Nat. Protocols 13, 1253–1274 (2018). (PMID: 2974864910.1038/nprot.2018.012)
Aglietti, R. A. et al. GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proc. Natl Acad. Sci. USA 113, 7858–7863 (2016). (PMID: 27339137494833810.1073/pnas.1607769113)
Kayagaki, N. et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341, 1246–1249 (2013). (PMID: 2388787310.1126/science.1240248)
Contrepois, K. et al. Cross-platform comparison of untargeted and targeted lipidomics approaches on aging mouse plasma. Sci. Rep. 8, 17747 (2018). (PMID: 30532037628811110.1038/s41598-018-35807-4)
Bakalarski, C. E. et al. The impact of peptide abundance and dynamic range on stable-isotope-based quantitative proteomic analyses. J. Proteome Res. 7, 4756–4765 (2008). (PMID: 18798661274602810.1021/pr800333e)
Wang, G. G. et al. Quantitative production of macrophages or neutrophils ex vivo using conditional Hoxb8. Nat. Methods 3, 287–293 (2006). (PMID: 1655483410.1038/nmeth865)
Wittig, I., Braun, H. P. & Schägger, H. Blue native PAGE. Nat. Protocols 1, 418–428 (2006). (PMID: 1740626410.1038/nprot.2006.62)
Waterhouse, A. et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 46 (W1), W296–W303 (2018). (PMID: 29788355603084810.1093/nar/gky427)
Ashkenazy, H., Erez, E., Martz, E., Pupko, T. & Ben-Tal, N. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38, W529–W533 (2010). (PMID: 20478830289609410.1093/nar/gkq399)
Ashkenazy, H. et al. ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res. 44, W344–W350 (2016). (PMID: 27166375498794010.1093/nar/gkw408)
UniProt Consortium. UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res. 47 (D1), D506–D515 (2019). (PMID: 10.1093/nar/gky1049)
Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011). (PMID: 21988835326169910.1038/msb.2011.75)
Robert, X. & Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320-4 (2014). (PMID: 2475342110.1093/nar/gku316)
المشرفين على المادة: 0 (Cell Adhesion Molecules, Neuronal)
0 (NINJ1 protein, human)
0 (Nerve Growth Factors)
0 (Ninj1 protein, mouse)
تواريخ الأحداث: Date Created: 20210120 Date Completed: 20210722 Latest Revision: 20230116
رمز التحديث: 20240628
DOI: 10.1038/s41586-021-03218-7
PMID: 33472215
قاعدة البيانات: MEDLINE
الوصف
تدمد:1476-4687
DOI:10.1038/s41586-021-03218-7