Caspase-8 inhibition improves the outcome of bacterial infections in mice by promoting neutrophil activation

Cell Reports Medicine - Tập 4 - Trang 101098 - 2023
Germana Lentini1, Agata Famà1, Giuseppe Valerio De Gaetano1,2, Francesco Coppolino3, Ahlem Khachroub Mahjoub1, Liv Ryan4, Egil Lien4,5, Terje Espevik4, Concetta Beninati1,2, Giuseppe Teti2
1Department of Human Pathology, University of Messina, Messina, Italy
2Scylla Biotech Srl, Messina, Italy
3Department of Chemical, Biological and Pharmaceutical Sciences, University of Messina, Messina, Italy
4Centre of Molecular Inflammation Research, Department of Cancer Research and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway
5Division of Infectious Diseases and Immunology, Program in Innate Immunity, Department of Medicine, University of Massachusetts Chan Medical School, Worcester, MA, USA

Tài liệu tham khảo

Van Opdenbosch, 2019, Caspases in cell death, inflammation, and disease, Immunity, 50, 1352, 10.1016/j.immuni.2019.05.020 Julien, 2017, Caspases and their substrates, Cell Death Differ., 24, 1380, 10.1038/cdd.2017.44 Orning, 2021, Multiple roles of caspase-8 in cell death, inflammation, and innate immunity, J. Leukoc. Biol., 109, 121, 10.1002/JLB.3MR0420-305R Tummers, 2017, Caspase-8: regulating life and death, Immunol. Rev., 277, 76, 10.1111/imr.12541 Newton, 2021, Dying cells fan the flames of inflammation, Science, 374, 1076, 10.1126/science.abi5934 Orning, 2018, Pathogen blockade of TAK1 triggers caspase-8-dependent cleavage of gasdermin D and cell death, Science, 362, 1064, 10.1126/science.aau2818 Shi, 2017, Pyroptosis: gasdermin-mediated programmed necrotic cell death, Trends Biochem. Sci., 42, 245, 10.1016/j.tibs.2016.10.004 Newton, 2019, Cleavage of RIPK1 by caspase-8 is crucial for limiting apoptosis and necroptosis, Nature, 574, 428, 10.1038/s41586-019-1548-x Oberst, 2011, Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis, Nature, 471, 363, 10.1038/nature09852 Chun, 2002, Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency, Nature, 419, 395, 10.1038/nature01063 Lehle, 2019, Intestinal inflammation and dysregulated immunity in patients with inherited caspase-8 deficiency, Gastroenterology, 156, 275, 10.1053/j.gastro.2018.09.041 Allam, 2014, Mitochondrial apoptosis is dispensable for NLRP3 inflammasome activation but non-apoptotic caspase-8 is required for inflammasome priming, EMBO Rep., 15, 982, 10.15252/embr.201438463 DeLaney, 2019, Caspase-8 promotes c-Rel-dependent inflammatory cytokine expression and resistance against Toxoplasma gondii, Proc. Natl. Acad. Sci. USA, 116, 11926, 10.1073/pnas.1820529116 Ganesan, 2014, Caspase-8 modulates dectin-1 and complement receptor 3-driven IL-1beta production in response to beta-glucans and the fungal pathogen, Candida albicans, J. Immunol., 193, 2519, 10.4049/jimmunol.1400276 Gurung, 2014, FADD and caspase-8 mediate priming and activation of the canonical and noncanonical Nlrp3 inflammasomes, J. Immunol., 192, 1835, 10.4049/jimmunol.1302839 Man, 2013, Salmonella infection induces recruitment of Caspase-8 to the inflammasome to modulate IL-1beta production, J. Immunol., 191, 5239, 10.4049/jimmunol.1301581 Philip, 2016, Activity of uncleaved caspase-8 controls anti-bacterial immune defense and TLR-induced cytokine production independent of cell death, PLoS Pathog., 12, 10.1371/journal.ppat.1005910 Weng, 2014, Caspase-8 and RIP kinases regulate bacteria-induced innate immune responses and cell death, Proc. Natl. Acad. Sci. USA, 111, 7391, 10.1073/pnas.1403477111 Fritsch, 2019, Caspase-8 is the molecular switch for apoptosis, necroptosis and pyroptosis, Nature, 575, 683, 10.1038/s41586-019-1770-6 Holmes, 2016, Understanding the mechanisms and drivers of antimicrobial resistance, Lancet, 387, 176, 10.1016/S0140-6736(15)00473-0 Lentini, 2022, Neutrophils discriminate live from dead bacteria by integrating signals initiated by Fprs and TLRs, EMBO J., 41, 10.15252/embj.2021109386 Ley, 2018, Neutrophils: new insights and open questions, Sci. Immunol., 3, 10.1126/sciimmunol.aat4579 Theilgaard-Mönch, 2005, The transcriptional program of terminal granulocytic differentiation, Blood, 105, 1785, 10.1182/blood-2004-08-3346 Grieshaber-Bouyer, 2021, The neutrotime transcriptional signature defines a single continuum of neutrophils across biological compartments, Nat. Commun., 12, 2856, 10.1038/s41467-021-22973-9 Landwehr-Kenzel, 2014, Interaction of Streptococcus agalactiae and cellular innate immunity in colonization and disease, Front. Immunol., 5, 519, 10.3389/fimmu.2014.00519 Mancuso, 2009, Bacterial recognition by TLR7 in the lysosomes of conventional dendritic cells, Nat. Immunol., 10, 587, 10.1038/ni.1733 Mancuso, 2004, Dual role of TLR2 and myeloid differentiation factor 88 in a mouse model of invasive group B streptococcal disease, J. Immunol., 172, 6324, 10.4049/jimmunol.172.10.6324 Teti, 1993, Cytokine appearance and effects of anti-tumor necrosis factor alpha antibodies in a neonatal rat model of group B streptococcal infection, Infect. Immun., 61, 227, 10.1128/iai.61.1.227-235.1993 Poreba, 2013, Caspase substrates and inhibitors, Cold Spring Harb. Perspect. Biol., 5, 10.1101/cshperspect.a008680 Newton, 2020, Multitasking kinase RIPK1 regulates cell death and inflammation, Cold Spring Harb. Perspect. Biol., 12, 10.1101/cshperspect.a036368 Pham, 2008, Neutrophil serine proteases fine-tune the inflammatory response, Int. J. Biochem. Cell Biol., 40, 1317, 10.1016/j.biocel.2007.11.008 Biondo, 2019, The dual role of innate immunity during influenza, Biomed. J., 42, 8, 10.1016/j.bj.2018.12.009 Patel, 2020, RIP1 inhibition blocks inflammatory diseases but not tumor growth or metastases, Cell Death Differ., 27, 161, 10.1038/s41418-019-0347-0 Signorino, 2014, Role of Toll-like receptor 13 in innate immune recognition of group B streptococci, Infect. Immun., 82, 5013, 10.1128/IAI.02282-14 Teti, 1997, Age-related sensitivity of neonatal mice to toxicity induced by heat-killed group B streptococci, Adv. Exp. Med. Biol., 418, 945, 10.1007/978-1-4899-1825-3_222 Mancuso, 2007, Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria, J. Immunol., 178, 3126, 10.4049/jimmunol.178.5.3126 Watson, 1993, A brief history of the pneumococcus in biomedical research: a panoply of scientific discovery, Clin. Infect. Dis., 17, 913, 10.1093/clinids/17.5.913 Famà, 2020, Nucleic acid-sensing toll-like receptors play a dominant role in innate immune recognition of pneumococci, mBio, 11, 10.1128/mBio.00415-20 Kovalenko, 2009, Caspase-8 deficiency in epidermal keratinocytes triggers an inflammatory skin disease, J. Exp. Med., 206, 2161, 10.1084/jem.20090616 Yuan, 2016, Roles of caspases in necrotic cell death, Cell, 167, 1693, 10.1016/j.cell.2016.11.047 Tecchio, 2014, Neutrophil-derived cytokines: facts beyond expression, Front. Immunol., 5, 508, 10.3389/fimmu.2014.00508 Thornberry, 1997, A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis, J. Biol. Chem., 272, 17907, 10.1074/jbc.272.29.17907 Pereira, 2008, Some commonly used caspase substrates and inhibitors lack the specificity required to monitor individual caspase activity, Biochem. Biophys. Res. Commun., 377, 873, 10.1016/j.bbrc.2008.10.101 Poreba, 2019, Caspase selective reagents for diagnosing apoptotic mechanisms, Cell Death Differ., 26, 229, 10.1038/s41418-018-0110-y Feng, 2007, Cleavage of RIP3 inactivates its caspase-independent apoptosis pathway by removal of kinase domain, Cell. Signal., 19, 2056, 10.1016/j.cellsig.2007.05.016 Lin, 1999, Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis, Genes Dev., 13, 2514, 10.1101/gad.13.19.2514 Pasparakis, 2015, Necroptosis and its role in inflammation, Nature, 517, 311, 10.1038/nature14191 Daniels, 2019, The nucleotide sensor ZBP1 and kinase RIPK3 induce the enzyme IRG1 to promote an antiviral metabolic state in neurons, Immunity, 50, 64, 10.1016/j.immuni.2018.11.017 Daniels, 2017, RIPK3 restricts viral pathogenesis via cell death-independent neuroinflammation, Cell, 169, 301, 10.1016/j.cell.2017.03.011 Najjar, 2016, RIPK1 and RIPK3 kinases promote cell-death-independent inflammation by toll-like receptor 4, Immunity, 45, 46, 10.1016/j.immuni.2016.06.007 Saleh, 2017, Kinase activities of RIPK1 and RIPK3 can direct IFN-beta synthesis induced by lipopolysaccharide, J. Immunol., 198, 4435, 10.4049/jimmunol.1601717 Moriwaki, 2014, The necroptosis adaptor RIPK3 promotes injury-induced cytokine expression and tissue repair, Immunity, 41, 567, 10.1016/j.immuni.2014.09.016 Kang, 2013, Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome, Immunity, 38, 27, 10.1016/j.immuni.2012.09.015 Moriwaki, 2016, Necroptosis-independent signaling by the RIP kinases in inflammation, Cell. Mol. Life Sci., 73, 2325, 10.1007/s00018-016-2203-4 Newton, 2019, Activity of caspase-8 determines plasticity between cell death pathways, Nature, 575, 679, 10.1038/s41586-019-1752-8 Günther, 2015, Caspase-8 controls the gut response to microbial challenges by Tnf-alpha-dependent and independent pathways, Gut, 64, 601, 10.1136/gutjnl-2014-307226 Biondo, 2014, The interleukin-1beta/CXCL1/2/neutrophil axis mediates host protection against group B streptococcal infection, Infect. Immun., 82, 4508, 10.1128/IAI.02104-14 Lentini, 2020, Neutrophils enhance their own influx to sites of bacterial infection via endosomal TLR-dependent Cxcl2 production, J. Immunol., 204, 660, 10.4049/jimmunol.1901039 Mohammadi, 2016, Neutrophils directly recognize group B streptococci and contribute to interleukin-1beta production during infection, PLoS One, 11, 10.1371/journal.pone.0160249 Mandal, 2018, Caspase-8 collaborates with caspase-11 to drive tissue damage and execution of endotoxic shock, Immunity, 49, 42, 10.1016/j.immuni.2018.06.011 Wallis, 2022, Host-directed immunotherapy of viral and bacterial infections: past, present and future, Nat. Rev. Immunol., 23, 121, 10.1038/s41577-022-00734-z Alphonse, 2021, Pan-caspase inhibition as a potential host-directed immunotherapy against MRSA and other bacterial skin infections, Sci. Transl. Med., 13, 10.1126/scitranslmed.abe9887 Man, 2017, Molecular mechanisms and functions of pyroptosis, inflammatory caspases and inflammasomes in infectious diseases, Immunol. Rev., 277, 61, 10.1111/imr.12534 Li, 1995, Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock, Cell, 80, 401, 10.1016/0092-8674(95)90490-5 Newton, 2004, Kinase RIP3 is dispensable for normal NF-kappa Bs, 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, 10.1128/MCB.24.4.1464-1469.2004 Murphy, 2013, The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism, Immunity, 39, 443, 10.1016/j.immuni.2013.06.018 Erlandsson, 1998, Interferon-beta is required for interferon-alpha production in mouse fibroblasts, Curr. Biol., 8, 223, 10.1016/S0960-9822(98)70086-7 Salmena, 2003, Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity, Genes Dev., 17, 883, 10.1101/gad.1063703 Costa, 2012, Activation of the NLRP3 inflammasome by group B streptococci, J. Immunol., 188, 1953, 10.4049/jimmunol.1102543 Huet, 2013, Ensuring animal welfare while meeting scientific aims using a murine pneumonia model of septic shock, Shock, 39, 488, 10.1097/SHK.0b013e3182939831 Lentini, 2021, Role of endosomal TLRs in Staphylococcus aureus infection, J. Immunol., 207, 1448, 10.4049/jimmunol.2100389 Biondo, 2005, MyD88 and TLR2, but not TLR4, are required for host defense against Cryptococcus neoformans, Eur. J. Immunol., 35, 870, 10.1002/eji.200425799