IRE1α Induces Thioredoxin-Interacting Protein to Activate the NLRP3 Inflammasome and Promote Programmed Cell Death under Irremediable ER Stress

Cell Metabolism - Tập 16 - Trang 250-264 - 2012
Alana G. Lerner1,2,3,4, John-Paul Upton5, P.V.K. Praveen1,2,3,4, Rajarshi Ghosh1,5,2,3,4, Yoshimi Nakagawa1,2,3,4, Aeid Igbaria1,2,3,4, Sarah Shen1,2,3,4, Vinh Nguyen6, Bradley J. Backes1,3, Myriam Heiman7,8,9, Nathaniel Heintz8, Paul Greengard9, Simon Hui10, Qizhi Tang6, Ala Trusina11, Scott A. Oakes5, Feroz R. Papa1,2,3,4
1Department of Medicine, University of California San Francisco, San Francisco, CA 94143, USA
2Diabetes Center, University of California, San Francisco, San Francisco, CA 94143, USA
3Lung Biology Center, University of California, San Francisco, San Francisco, CA 94143, USA
4California Institute for Quantitative Biosciences, University of California, San Francisco, San Francisco, CA 94143, USA
5Department of Pathology, University of California, San Francisco, San Francisco, CA 94143, USA
6Department of Surgery, University of California, San Francisco, San Francisco, CA 94143, USA
7Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA
8Howard Hughes Medical Institute, The Rockefeller University, New York, NY 10021 USA
9Laboratory of Molecular and Cellular Neuroscience, The Rockefeller University, New York, NY 10021, USA
10Department of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA
11Center for Models of Life, Niels Bohr Institute, University of Copenhagen, Blegdamsvej 17, 2100 Copenhagen, Denmark

Tài liệu tham khảo

Aragón, 2009, Messenger RNA targeting to endoplasmic reticulum stress signalling sites, Nature, 457, 736, 10.1038/nature07641 Calfon, 2002, IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA, Nature, 415, 92, 10.1038/415092a Cha-Molstad, 2009, Glucose-stimulated expression of Txnip is mediated by carbohydrate response element-binding protein, p300, and histone H4 acetylation in pancreatic beta cells, J. Biol. Chem., 284, 16898, 10.1074/jbc.M109.010504 Chen, 2008, Thioredoxin-interacting protein: a critical link between glucose toxicity and beta-cell apoptosis, Diabetes, 57, 938, 10.2337/db07-0715 Credle, 2005, On the mechanism of sensing unfolded protein in the endoplasmic reticulum, Proc. Natl. Acad. Sci. USA, 102, 18773, 10.1073/pnas.0509487102 Fabian, 2010, Regulation of mRNA translation and stability by microRNAs, Annu. Rev. Biochem., 79, 351, 10.1146/annurev-biochem-060308-103103 Gardner, 2011, Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response, Science, 333, 1891, 10.1126/science.1209126 Gething, 1990, Transport and assembly processes in the endoplasmic reticulum, Semin. Cell Biol., 1, 65 Han, 2008, A kinase inhibitor activates the IRE1alpha RNase to confer cytoprotection against ER stress, Biochem. Biophys. Res. Commun., 365, 777, 10.1016/j.bbrc.2007.11.040 Han, 2009, IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates, Cell, 138, 562, 10.1016/j.cell.2009.07.017 Harding, 1999, Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase, Nature, 397, 271, 10.1038/16729 Harding, 2001, Translational regulation in the cellular response to biosynthetic load on the endoplasmic reticulum, Cold Spring Harb. Symp. Quant. Biol., 66, 499, 10.1101/sqb.2001.66.499 Heiman, 2008, A translational profiling approach for the molecular characterization of CNS cell types, Cell, 135, 738, 10.1016/j.cell.2008.10.028 Hui, 2004, Mice lacking thioredoxin-interacting protein provide evidence linking cellular redox state to appropriate response to nutritional signals, J. Biol. Chem., 279, 24387, 10.1074/jbc.M401280200 Hui, 2008, Txnip balances metabolic and growth signaling via PTEN disulfide reduction, Proc. Natl. Acad. Sci. USA, 105, 3921, 10.1073/pnas.0800293105 Jousse, 2001, Inhibition of CHOP translation by a peptide encoded by an open reading frame localized in the chop 5'UTR, Nucleic Acids Res., 29, 4341, 10.1093/nar/29.21.4341 Lee, 2003, XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response, Mol. Cell. Biol., 23, 7448, 10.1128/MCB.23.21.7448-7459.2003 Lee, 2008, Regulation of hepatic lipogenesis by the transcription factor XBP1, Science, 320, 1492, 10.1126/science.1158042 Lipson, 2006, Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1, Cell Metab., 4, 245, 10.1016/j.cmet.2006.07.007 Merksamer, 2010, The UPR and cell fate at a glance, J. Cell Sci., 123, 1003, 10.1242/jcs.035832 Merksamer, 2008, Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions, Cell, 135, 933, 10.1016/j.cell.2008.10.011 Minn, 2005, Thioredoxin-interacting protein is stimulated by glucose through a carbohydrate response element and induces beta-cell apoptosis, Endocrinology, 146, 2397, 10.1210/en.2004-1378 Nishiyama, 1999, Identification of thioredoxin-binding protein-2/vitamin D(3) up-regulated protein 1 as a negative regulator of thioredoxin function and expression, J. Biol. Chem., 274, 21645, 10.1074/jbc.274.31.21645 Oslowski, 2012, Thioredoxin-interacting protein mediates ER stress-induced β cell death through initiation of the inflammasome, Cell Metab., 16, 265, 10.1016/j.cmet.2012.07.005 Oyadomari, 2002, Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes, J. Clin. Invest., 109, 525, 10.1172/JCI0214550 Palam, 2011, Phosphorylation of eIF2 facilitates ribosomal bypass of an inhibitory upstream ORF to enhance CHOP translation, J. Biol. Chem., 286, 10939, 10.1074/jbc.M110.216093 Papa, 2003, Bypassing a kinase activity with an ATP-competitive drug, Science, 302, 1533, 10.1126/science.1090031 Papandreou, 2011, Identification of an Ire1alpha endonuclease specific inhibitor with cytotoxic activity against human multiple myeloma, Blood, 117, 1311, 10.1182/blood-2010-08-303099 Parikh, 2007, TXNIP regulates peripheral glucose metabolism in humans, PLoS Med., 4, e158, 10.1371/journal.pmed.0040158 Patwari, 2006, The interaction of thioredoxin with Txnip. Evidence for formation of a mixed disulfide by disulfide exchange, J. Biol. Chem., 281, 21884, 10.1074/jbc.M600427200 Ron, 2002, Proteotoxicity in the endoplasmic reticulum: lessons from the Akita diabetic mouse, J. Clin. Invest., 109, 443, 10.1172/JCI0215020 Rutkowski, 2006, Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins, PLoS Biol., 4, e374, 10.1371/journal.pbio.0040374 Scheuner, 2008, The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes, Endocr. Rev., 29, 317, 10.1210/er.2007-0039 Shalev, 2008, Lack of TXNIP protects beta-cells against glucotoxicity, Biochem. Soc. Trans., 36, 963, 10.1042/BST0360963 Shalev, 2002, Oligonucleotide microarray analysis of intact human pancreatic islets: identification of glucose-responsive genes and a highly regulated TGFbeta signaling pathway, Endocrinology, 143, 3695, 10.1210/en.2002-220564 Shore, 2011, Signaling cell death from the endoplasmic reticulum stress response, Curr. Opin. Cell Biol., 23, 143, 10.1016/j.ceb.2010.11.003 Støy, 2007, Insulin gene mutations as a cause of permanent neonatal diabetes, Proc. Natl. Acad. Sci. USA, 104, 15040, 10.1073/pnas.0707291104 Strowig, 2012, Inflammasomes in health and disease, Nature, 481, 278, 10.1038/nature10759 Thomas, 2004, Pattern of genes influenced by conditional expression of the transcription factors HNF6, HNF4alpha and HNF1beta in a pancreatic beta-cell line, Nucleic Acids Res., 32, e150, 10.1093/nar/gnh144 Tirasophon, 1998, A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells, Genes Dev., 12, 1812, 10.1101/gad.12.12.1812 Vembar, 2008, One step at a time: endoplasmic reticulum-associated degradation, Nat. Rev. Mol. Cell Biol., 9, 944, 10.1038/nrm2546 Volkmann, 2011, Potent and selective inhibitors of the inositol-requiring enzyme 1 endoribonuclease, J. Biol. Chem., 286, 12743, 10.1074/jbc.M110.199737 Wang, 1998, Cloning of mammalian Ire1 reveals diversity in the ER stress responses, EMBO J., 17, 5708, 10.1093/emboj/17.19.5708 Wang, 1999, A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse, J. Clin. Invest., 103, 27, 10.1172/JCI4431 Yamanaka, 2000, A possible interaction of thioredoxin with VDUP1 in HeLa cells detected in a yeast two-hybrid system, Biochem. Biophys. Res. Commun., 271, 796, 10.1006/bbrc.2000.2699 Yoshida, 1998, Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors, J. Biol. Chem., 273, 33741, 10.1074/jbc.273.50.33741 Yoshida, 2001, XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor, Cell, 107, 881, 10.1016/S0092-8674(01)00611-0 Yu, 2009, Tandem ChoRE and CCAAT motifs and associated factors regulate Txnip expression in response to glucose or adenosine-containing molecules, PLoS ONE, 4, e8397, 10.1371/journal.pone.0008397 Zhou, 2006, The crystal structure of human IRE1 luminal domain reveals a conserved dimerization interface required for activation of the unfolded protein response, Proc. Natl. Acad. Sci. USA, 103, 14343, 10.1073/pnas.0606480103 Zhou, 2010, Thioredoxin-interacting protein links oxidative stress to inflammasome activation, Nat. Immunol., 11, 136, 10.1038/ni.1831