RIPK1 Mediates TNF-Induced Intestinal Crypt Apoptosis During Chronic NF-κB Activation

Jerry Wong1,2,3, Ricard Garcia-Carbonell1,2,3,4, Matija Zelic5, Samuel B. Ho6,7, Brigid S. Boland6,8, Shih-Jing Yao1,2,3, Shalin A. Desai1,2,3, Soumita Das3, Núria Planell9, Philip A. Harris10, Joan Font-Burgada1,2,3, Koji Taniguchi1,2,3, John Bertin5, Azucena Salas9, Manolis Pasparakis11, Pete J. Gough10, Michelle Kelliher5, Michael Karin1,2,3, Monica Guma12,13
1Laboratory of Gene Regulation and Signal Transduction, San Diego, California
2Department of Pharmacology, San Diego, California
3Department Pathology, San Diego, California
4Department of Biochemistry and Molecular Biology, Faculty of Pharmacy, University of Barcelona, Barcelona, Spain
5Department of Molecular, Cell and Cancer Biology, University of Massachusetts Medical School, Worcester, Massachusetts
6Division of Gastroenterology, San Diego, California
7Department of Medicine, VA San Diego Healthcare System, San Diego, California
8San Diego Digestive Disease Research Center, San Diego, California
9Department of Gastroenterology, IDIBAPS, Hospital Clínic, CIBER-EHD, Barcelona, Spain
10Pattern Recognition Receptor Discovery Performance Unit, Immuno-Inflammation Therapeutic Area, GlaxoSmithKline, Collegeville, Pennsylvania
11Institute for Genetics, Centre for Molecular Medicine and Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases, University of Cologne, Cologne, Germany
12Department Rheumatology, San Diego, California
13Department of Medicine, Autonomous University of Barcelona, Plaça Cívica, Bellaterra, Barcelona, Spain

Tài liệu tham khảo

Abraham, 2009, Inflammatory bowel disease, N Engl J Med, 361, 2066, 10.1056/NEJMra0804647 Gunther, 2013, Apoptosis, necrosis and necroptosis: cell death regulation in the intestinal epithelium, Gut, 62, 1062, 10.1136/gutjnl-2011-301364 Khor, 2011, Genetics and pathogenesis of inflammatory bowel disease, Nature, 474, 307, 10.1038/nature10209 Okamoto, 2016, Role of epithelial cells in the pathogenesis and treatment of inflammatory bowel disease, J Gastroenterol, 51, 11, 10.1007/s00535-015-1098-4 Neurath, 2012, Mucosal healing in inflammatory bowel diseases: a systematic review, Gut, 61, 1619, 10.1136/gutjnl-2012-302830 Vereecke, 2009, The ubiquitin-editing enzyme A20 (TNFAIP3) is a central regulator of immunopathology, Trends Immunol, 30, 383, 10.1016/j.it.2009.05.007 Kaser, 2010, Inflammatory bowel disease, Ann Rev Immunol, 28, 573, 10.1146/annurev-immunol-030409-101225 Zeissig, 2004, Downregulation of epithelial apoptosis and barrier repair in active Crohn's disease by tumour necrosis factor alpha antibody treatment, Gut, 53, 1295, 10.1136/gut.2003.036632 Lin, 2003, NF-kappaB in cancer: a marked target, Semin Cancer Biol, 13, 107, 10.1016/S1044-579X(02)00128-1 Egan, 2004, IkappaB-kinasebeta-dependent NF-kappaB activation provides radioprotection to the intestinal epithelium, Proc Natl Acad Sci U S A, 101, 2452, 10.1073/pnas.0306734101 Chen, 2003, The two faces of IKK and NF-kappaB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion, Nat Med, 9, 575, 10.1038/nm849 Nenci, 2007, Epithelial NEMO links innate immunity to chronic intestinal inflammation, Nature, 446, 557, 10.1038/nature05698 Garcia-Carbonell, 2018, Elevated A20 promotes TNF-induced and RIPK1-dependent intestinal epithelial cell death, Proc Natl Acad Sci U S A, 115, E9192, 10.1073/pnas.1810584115 Guma, 2011, Constitutive intestinal NF-kappaB does not trigger destructive inflammation unless accompanied by MAPK activation, J Exp Med, 208, 1889, 10.1084/jem.20110242 Pasparakis, 2015, Necroptosis and its role in inflammation, Nature, 517, 311, 10.1038/nature14191 Weinlich, 2014, The two faces of receptor interacting protein kinase-1, Mol Cell, 56, 469, 10.1016/j.molcel.2014.11.001 Wang, 2008, TNF-alpha induces two distinct caspase-8 activation pathways, Cell, 133, 693, 10.1016/j.cell.2008.03.036 Kanayama, 2004, TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains, Mol Cell, 15, 535, 10.1016/j.molcel.2004.08.008 Micheau, 2002, The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex, J Biol Chem, 277, 45162, 10.1074/jbc.M206882200 Feng, 2007, A novel inhibitory mechanism of mitochondrion-dependent apoptosis by a herpesviral protein, PLoS Pathog, 3, e174, 10.1371/journal.ppat.0030174 O'Donnell, 2011, Caspase 8 inhibits programmed necrosis by processing CYLD, Nat Cell Biol, 13, 1437, 10.1038/ncb2362 Rogler, 1998, Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa, Gastroenterology, 115, 357, 10.1016/S0016-5085(98)70202-1 Leal, 2015, Identification of inflammatory mediators in patients with Crohn's disease unresponsive to anti-TNFalpha therapy, Gut, 64, 233, 10.1136/gutjnl-2013-306518 Sato, 2009, Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche, Nature, 459, 262, 10.1038/nature07935 Kreuz, 2001, NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling, Mol Cell Biol, 21, 3964, 10.1128/MCB.21.12.3964-3973.2001 Kawakami, 2005, Transcriptional activation of survivin through the NF-kappaB pathway by human T-cell leukemia virus type I tax, Int J Cancer, 115, 967, 10.1002/ijc.20954 Ofengeim, 2013, Regulation of RIP1 kinase signalling at the crossroads of inflammation and cell death, Nat Rev Cell Biol, 14, 727, 10.1038/nrm3683 Degterev, 2008, Identification of RIP1 kinase as a specific cellular target of necrostatins, Nat Chem Biol, 4, 313, 10.1038/nchembio.83 Takahashi, 2012, Necrostatin-1 analogues: critical issues on the specificity, activity and in vivo use in experimental disease models, Cell Death Dis, 3, e437, 10.1038/cddis.2012.176 Mandal, 2014, RIP3 induces apoptosis independent of pronecrotic kinase activity, Mol Cell, 56, 481, 10.1016/j.molcel.2014.10.021 Berger, 2015, Characterization of GSK’963: a structurally distinct, potent and selective inhibitor of RIP1 kinase, Cell Death Discov, 1, 10.1038/cddiscovery.2015.9 Polykratis, 2014, Cutting edge: RIPK1 Kinase inactive mice are viable and protected from TNF-induced necroptosis in vivo, J Immunol, 193, 1539, 10.4049/jimmunol.1400590 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 Zhang, 2009, RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis, Science, 325, 332, 10.1126/science.1172308 Vandenabeele, 2010, The role of the kinases RIP1 and RIP3 in TNF-induced necrosis, Sci Signal, 3, re4, 10.1126/scisignal.3115re4 Vanden Berghe, 2014, Regulated necrosis: the expanding network of non-apoptotic cell death pathways, Nat Rev Mol Cell Biol, 15, 135, 10.1038/nrm3737 Kim, 2007, TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death, Mol Cell, 26, 675, 10.1016/j.molcel.2007.04.021 Shindo, 2013, Critical contribution of oxidative stress to TNFalpha-induced necroptosis downstream of RIPK1 activation, Biochem Biophys Res Commun, 436, 212, 10.1016/j.bbrc.2013.05.075 Zhang, 2017, RIP1 autophosphorylation is promoted by mitochondrial ROS and is essential for RIP3 recruitment into necrosome, Nat Commun, 8, 14329, 10.1038/ncomms14329 Matsuzawa-Ishimoto, 2017, Autophagy protein ATG16L1 prevents necroptosis in the intestinal epithelium, J Exp Med, 214, 3687, 10.1084/jem.20170558 Pott, 2018, Intestinal epithelial cell autophagy is required to protect against TNF-induced apoptosis during chronic colitis in mice, Cell Host Microbe, 23, 191, 10.1016/j.chom.2017.12.017 Aden, 2018, ATG16L1 orchestrates interleukin-22 signaling in the intestinal epithelium via cGAS-STING, J Exp Med, 215, 2868, 10.1084/jem.20171029 Anderson, 2011, Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47, Nat Genet, 43, 246, 10.1038/ng.764 Franke, 2010, Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci, Nat Genet, 42, 1118, 10.1038/ng.717 Liu, 2015, Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations, Nat Genet, 47, 979, 10.1038/ng.3359 Greten, 2004, IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer, Cell, 118, 285, 10.1016/j.cell.2004.07.013 Pereira, 2015, Oxidative stress and DNA damage: implications in inflammatory bowel disease, Inflamm Bowel Dis, 21, 2403 Shaked, 2012, Chronic epithelial NF-kappaB activation accelerates APC loss and intestinal tumor initiation through iNOS up-regulation, Proc Natl Acad Sci U S A, 109, 14007, 10.1073/pnas.1211509109 Lakatos, 2008, Risk for colorectal cancer in ulcerative colitis: changes, causes and management strategies, World J Gastroenterol, 14, 3937, 10.3748/wjg.14.3937 Abraham, 2016, Cancer surveillance in ulcerative colitis and Crohn's disease: new strategies, Curr Opin Gastroenterol, 32, 32, 10.1097/MOG.0000000000000234 Brain, 2010, NOD2-mediated autophagy and Crohn disease, Autophagy, 6, 412, 10.4161/auto.6.3.11389 Newton, 2014, Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis, Science, 343, 1357, 10.1126/science.1249361 Rott, 1991, Tuberous sclerosis in two sibs of normal parents, Clin Genet, 39, 306, 10.1111/j.1399-0004.1991.tb03031.x Dobin, 2013, STAR: ultrafast universal RNA-seq aligner, Bioinformatics, 29, 15, 10.1093/bioinformatics/bts635 Li, 2011, RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome, BMC Bioinformatics, 12, 323, 10.1186/1471-2105-12-323 Anders, 2010, Differential expression analysis for sequence count data, Genome Biol, 11, R106, 10.1186/gb-2010-11-10-r106 Delhase, 1999, Positive and negative regulation of IkappaB kinase activity through IKKbeta subunit phosphorylation, Science, 284, 309, 10.1126/science.284.5412.309 Wertz, 2004, De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling, Nature, 430, 694, 10.1038/nature02794 Lu, 2013, Dimerization and ubiquitin mediated recruitment of A20, a complex deubiquitinating enzyme, Immunity, 38, 896, 10.1016/j.immuni.2013.03.008 Meerbrey, 2011, The pINDUCER lentiviral toolkit for inducible RNA interference in vitro and in vivo, Proc Natl Acad Sci U S A, 108, 3665, 10.1073/pnas.1019736108 Koo, 2012, Controlled gene expression in primary Lgr5 organoid cultures, Nat Methods, 9, 81, 10.1038/nmeth.1802