Necroptosis blockade prevents lung injury in severe influenza

  • Kalil, A. C. & Thomas, P. G. Influenza virus-related critical illness: pathophysiology and epidemiology. Crit. Care 23, 258 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Korteweg, C. & Gu, J. Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am. J. Pathol. 172, 1155–1170 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mauad, T. et al. Lung pathology in fatal novel human influenza A (H1N1) infection. Am. J. Respir. Crit. Care Med. 181, 72–79 (2010).

    Article 
    PubMed 

    Google Scholar
     

  • Kash, J. C. et al. Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443, 578–581 (2006).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Flerlage, T., Boyd, D. F., Meliopoulos, V., Thomas, P. G. & Schultz-Cherry, S. Influenza virus and SARS-CoV-2: pathogenesis and host responses in the respiratory tract. Nat. Rev. Microbiol. 19, 425–441 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nogusa, S. et al. RIPK3 activates parallel pathways of MLKL-driven necroptosis and FADD-mediated apoptosis to protect against influenza A virus. Cell Host Microbe 20, 13–24 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rodrigue-Gervais, I. G. et al. Cellular inhibitor of apoptosis protein cIAP2 protects against pulmonary tissue necrosis during influenza virus infection to promote host survival. Cell Host Microbe 15, 23–35 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhang, T. et al. Influenza virus Z-RNAs induce ZBP1-mediated necroptosis. Cell 180, 1115–1129.e1113 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schrauwen, E. J. & Fouchier, R. A. Host adaptation and transmission of influenza A viruses in mammals. Emerg. Microbes Infect. 3, e9 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Herfst, S., Imai, M., Kawaoka, Y. & Fouchier, R. A. Avian influenza virus transmission to mammals. Curr. Top. Microbiol. Immunol. 385, 137–155 (2014).

    CAS 
    PubMed 

    Google Scholar
     

  • Sun, H. et al. Airborne transmission of human-isolated avian H3N8 influenza virus between ferrets. Cell 186, 4074–4084.e4011 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Thomas, P. G., Shubina, M. & Balachandran, S. in Curr. Top Microbiol. Immunol. Vol. 442 (eds Mocarski, E.S. & Mandal, P.) 41–63 (2020).

  • Balachandran, S. & Rall, G. F. Benefits and perils of necroptosis in influenza virus infection. J. Virol. 94, e01101–19 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sanders, C. J., Doherty, P. C. & Thomas, P. G. Respiratory epithelial cells in innate immunity to influenza virus infection. Cell Tissue Res. 343, 13–21 (2011).

    Article 
    PubMed 

    Google Scholar
     

  • Sanders, C. J. et al. Compromised respiratory function in lethal influenza infection is characterized by the depletion of type I alveolar epithelial cells beyond threshold levels. Am. J. Physiol. 304, L481–L488 (2013).

    CAS 

    Google Scholar
     

  • Shubina, M. et al. Necroptosis restricts influenza A virus as a stand-alone cell death mechanism. J. Exp. Med. 217, e20191259 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Upton, J. W., Shubina, M. & Balachandran, S. RIPK3-driven cell death during virus infections. Immunol. Rev. 277, 90–101 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Thapa, R. J. et al. DAI senses influenza A virus genomic RNA and activates RIPK3-dependent cell death. Cell Host Microbe 20, 674–681 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kuriakose, T. et al. ZBP1/DAI is an innate sensor of influenza virus triggering the NLRP3 inflammasome and programmed cell death pathways. Science Immunol. 1, aag2045 (2016).

    Article 

    Google Scholar
     

  • Mandal, P. et al. RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol. Cell 56, 481–495 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Newton, K. et al. Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis. Science 343, 1357–1360 (2014).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Najjar, M. et al. Structure guided design of potent and selective ponatinib-based hybrid inhibitors for RIPK1. Cell Rep. 10, 1850–1860 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fauster, A. et al. A cellular screen identifies ponatinib and pazopanib as inhibitors of necroptosis. Cell Death Dis. 6, e1767 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, J. X. et al. The B-RafV600E inhibitor dabrafenib selectively inhibits RIP3 and alleviates acetaminophen-induced liver injury. Cell Death Dis. 5, e1278 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wissing, J. et al. Chemical proteomic analysis reveals alternative modes of action for pyrido[2,3-d]pyrimidine kinase inhibitors. Mol. Cell Proteomics 3, 1181–1193 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Meng, Y. et al. Human RIPK3 maintains MLKL in an inactive conformation prior to cell death by necroptosis. Nat. Commun. 12, 6783 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sarhan, J. et al. Caspase-8 induces cleavage of gasdermin D to elicit pyroptosis during Yersinia infection. Proc. Natl Acad. Sci. USA 115, E10888–E10897 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rodriguez, D. A. et al. Caspase-8 and FADD prevent spontaneous ZBP1 expression and necroptosis. Proc. Natl Acad. Sci. USA 119, e2207240119 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, J., Chen, Z., Narasaraju, T., Jin, N. & Liu, L. Isolation of highly pure alveolar epithelial type I and type II cells from rat lungs. Lab Invest. 84, 727–735 (2004).

    Article 
    PubMed 

    Google Scholar
     

  • Wang, S. & Hubmayr, R. D. Type I alveolar epithelial phenotype in primary culture. Am. J. Respir. Cell Mol. Biol. 44, 692–699 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rishi, A. K. et al. Cloning, characterization, and development expression of a rat lung alveolar type I cell gene in embryonic endodermal and neural derivatives. Dev. Biol. 167, 294–306 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hrdinka, M. et al. Small molecule inhibitors reveal an indispensable scaffolding role of RIPK2 in NOD2 signaling. EMBO J. 37, e99372 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tan, Y. et al. Somatic epigenetic silencing of RIPK3 inactivates necroptosis and contributes to chemoresistance in malignant mesothelioma. Clin. Cancer Res. 27, 1200–1213 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Xie, T. et al. Structural insights into RIP3-mediated necroptotic signaling. Cell Rep. 5, 70–78 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen, W. et al. Diverse sequence determinants control human and mouse receptor interacting protein 3 (RIP3) and mixed lineage kinase domain-like (MLKL) interaction in necroptotic signaling. J. Biol. Chem. 288, 16247–16261 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bantia, S. et al. Comparison of the anti-influenza virus activity of RWJ-270201 with those of oseltamivir and zanamivir. Antimicrob. Agents Chemother. 45, 1162–1167 (2001).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Groeneveld, G. H. et al. Effectiveness of oseltamivir in reduction of complications and 30-day mortality in severe seasonal influenza infection. Int. J. Antimicrob. Agents 56, 106155 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zuliani-Alvarez, L. & Piccinini, A. M. A virological view of tenascin-C in infection. Am. J. Physiol. Cell Physiol. 324, C1–C9 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pillay, J. et al. A subset of neutrophils in human systemic inflammation inhibits T cell responses through Mac-1. J. Clin. Invest. 122, 327–336 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tak, T. et al. Neutrophil-mediated suppression of influenza-induced pathology requires CD11b/CD18 (MAC-1). Am. J. Respir. Cell Mol. Biol. 58, 492–499 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nikhar, S. et al. Design of pyrido[2,3-d]pyrimidin-7-one inhibitors of receptor interacting protein kinase-2 (RIPK2) and nucleotide-binding oligomerization domain (NOD) cell signaling. Eur. J. Med. Chem. 215, 113252 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Suebsuwong, C. et al. Activation loop targeting strategy for design of receptor-interacting protein kinase 2 (RIPK2) inhibitors. Bioorg. Med. Chem. Lett. 28, 577–583 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Muraro, S. P. et al. Respiratory syncytial virus induces the classical ROS-dependent NETosis through PAD-4 and necroptosis pathways activation. Sci Rep. 8, 14166 (2018).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang, L. et al. Necroptosis in pulmonary diseases: a new therapeutic target. Front. Pharmacol. 12, 737129 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ishii, K. J. et al. TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature 451, 725–729 (2008).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Murphy, J. M. et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39, 443–453 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Newton, K., Sun, X. & Dixit, V. M. Kinase RIP3 is dispensable for normal NF-κBs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Toll-like receptors 2 and 4. Mol. Cell. Biol. 24, 1464–1469 (2004).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Berger, S. B. et al. Cutting edge: RIP1 kinase activity is dispensable for normal development but is a key regulator of inflammation in SHARPIN-deficient mice. J Immunol 192, 5476–5480 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Laskowski, R. A. & Swindells, M. B. LigPlot+: multiple ligand–protein interaction diagrams for drug discovery. J. Chem. Inf. Model. 51, 2778–2786 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Boyd, D. F. et al. Exuberant fibroblast activity compromises lung function via ADAMTS4. Nature 587, 466–471 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902.e1821 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rodriguez, D. A. et al. Characterization of RIPK3-mediated phosphorylation of the activation loop of MLKL during necroptosis. Cell Death Differ. 23, 76–88 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Matute-Bello, G. et al. An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. Am. J. Respir. Cell Mol. Biol. 44, 725–738 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     


  • Source link

    Total
    0
    Shares
    Leave a Reply

    Your email address will not be published. Required fields are marked *

    Related Posts