ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death (original) (raw)
Walter, P. & Ron, D. The unfolded protein response: from stress pathway to homeostatic regulation. Science334, 1081–1086 (2011). ArticleCAS Google Scholar
Hetz, C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol.13, 89–102 (2012). ArticleCAS Google Scholar
Wang, S. & Kaufman, R. J. The impact of the unfolded protein response on human disease. J. Cell Biol.197, 857–867 (2012). ArticleCAS Google Scholar
Harding, H. P. et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell6, 1099–1108 (2000). ArticleCAS Google Scholar
Scheuner, D. et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell7, 1165–1176 (2001). ArticleCAS Google Scholar
Hai, T. W., Liu, F., Coukos, W. J. & Green, M. R. Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers. Genes Dev.3, 2083–2090 (1989). ArticleCAS Google Scholar
Lu, P. D., Harding, H. P. & Ron, D. Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol.167, 27–33 (2004). ArticleCAS Google Scholar
Vattem, K. M. & Wek, R. C. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl Acad. Sci. USA101, 11269–11274 (2004). ArticleCAS Google Scholar
Fornace, A. J. Jr, Alamo, I. Jr & Hollander, M. C. DNA damage-inducible transcripts in mammalian cells. Proc. Natl Acad. Sci. USA85, 8800–8804 (1988). ArticleCAS Google Scholar
Ron, D. & Habener, J. F. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes. Dev.6, 439–453 (1992). ArticleCAS Google Scholar
Ma, Y., Brewer, J. W., Diehl, J. A. & Hendershot, L. M. Two distinct stress signalling pathways converge on the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol.318, 1351–1365 (2002). ArticleCAS Google Scholar
Zinszner, H. et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev.12, 982–995 (1998). ArticleCAS Google Scholar
Oyadomari, S. et al. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Invest.109, 525–532 (2002). ArticleCAS Google Scholar
Song, B., Scheuner, D., Ron, D., Pennathur, S. & Kaufman, R. J. Chop deletion reduces oxidative stress, improves β cell function, and promotes cell survival in multiple mouse models of diabetes. J. Clin. Invest.118, 3378–3389 (2008). ArticleCAS Google Scholar
Malhotra, J. D. et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc. Natl Acad. Sci. USA105, 18525–18530 (2008). ArticleCAS Google Scholar
Thorp, E. et al. Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe-/- and Ldlr-/- mice lacking CHOP. Cell Metab.9, 474–481 (2009). ArticleCAS Google Scholar
Tabas, I. & Ron, D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol.13, 184–190 (2011). ArticleCAS Google Scholar
Pennuto, M. et al. Ablation of the UPR-mediator CHOP restores motor function and reduces demyelination in Charcot-Marie-Tooth 1B mice. Neuron57, 393–405 (2008). ArticleCAS Google Scholar
McCullough, K. D., Martindale, J. L., Klotz, L. O., Aw, T. Y. & Holbrook, N. J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell Biol.21, 1249–1259 (2001). ArticleCAS Google Scholar
Chikka, M. R., McCabe, D. D., Tyra, H. M. & Rutkowski, D. T. C/EBP Homologous Protein (CHOP) contributes to suppression of metabolic genes during endoplasmic reticulum stress in the liver. J. Biol. Chem.288, 4405–4415 (2013). ArticleCAS Google Scholar
Rutkowski, D. T. et al. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol.4, e374 (2006). Article Google Scholar
Wang, X. Z. et al. Identification of novel stress-induced genes downstream of chop. EMBO J.17, 3619–3630 (1998). ArticleCAS Google Scholar
Harding, H. P. et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell11, 619–633 (2003). ArticleCAS Google Scholar
Sun, X. et al. ATF4 protects against neuronal death in cellular Parkinson’s disease models by maintaining levels of parkin. J. Neurosci.33, 2398–2407 (2013). ArticleCAS Google Scholar
Pike, L. R. et al. Transcriptional up-regulation of ULK1 by ATF4 contributes to cancer cell survival. Biochem. J.449, 389–400 (2013). ArticleCAS Google Scholar
Ord, D., Meerits, K. & Ord, T. TRB3 protects cells against the growth inhibitory and cytotoxic effect of ATF4. Exp. Cell Res.313, 3556–3567 (2007). Article Google Scholar
Lange, P. S. et al. ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J. Exp. Med.205, 1227–1242 (2008). ArticleCAS Google Scholar
Galehdar, Z. et al. Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4-CHOP-mediated induction of the Bcl-2 homology 3-only member PUMA. J. Neurosci.30, 16938–16948 (2010). ArticleCAS Google Scholar
Armstrong, J. L., Flockhart, R., Veal, G. J., Lovat, P. E. & Redfern, C. P. Regulation of endoplasmic reticulum stress-induced cell death by ATF4 in neuroectodermal tumour cells. J. Biol. Chem.285, 6091–6100 (2010). ArticleCAS Google Scholar
Qing, G. et al. ATF4 regulates MYC-mediated neuroblastoma cell death on glutamine deprivation. Cancer Cell22, 631–644 (2012). ArticleCAS Google Scholar
Ubeda, M. et al. Stress-induced binding of the transcriptional factor CHOP to a novel DNA control element. Mol. Cell Biol.16, 1479–1489 (1996). ArticleCAS Google Scholar
Chen, B. P., Wolfgang, C. D. & Hai, T. Analysis of ATF3, a transcription factor induced by physiological stresses and modulated by gadd153/Chop10. Mol. Cell Biol.16, 1157–1168 (1996). Article Google Scholar
Marciniak, S. J. et al. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Gen. Dev.18, 3066–3077 (2004). ArticleCAS Google Scholar
Ma, Y. & Hendershot, L. M. Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J. Biol. Chem.278, 34864–34873 (2003). ArticleCAS Google Scholar
Ohoka, N., Yoshii, S., Hattori, T., Onozaki, K. & Hayashi, H. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J.24, 1243–1255 (2005). ArticleCAS Google Scholar
Gill, G. & Ptashne, M. Negative effect of the transcriptional activator GAL4. Nature334, 721–724 (1988). ArticleCAS Google Scholar
Valouev, A. et al. Genome-wide analysis of transcription factor binding sites based on ChIP-seq data. Nat. Methods5, 829–834 (2008). ArticleCAS Google Scholar
Su, N. & Kilberg, M. S. C/EBP Homology Protein (CHOP) Interacts with Activating Transcription Factor 4 (ATF4) and negatively regulates the stress-dependent induction of the asparagine synthetase gene. J. Biol. Chem.283, 35106–35117 (2008). ArticleCAS Google Scholar
Bromati, C. R. et al. UPR induces transient burst of apoptosis in islets of early lactating rats through reduced AKT phosphorylation via ATF4/CHOP stimulation of TRB3 expression. Am. J. Physiol. Regul. Integr. Comp. Physiol.300, R92–R100 (2011). ArticleCAS Google Scholar
Novoa, I., Zeng, H., Harding, H. P. & Ron, D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol.153, 1011–1022 (2001). ArticleCAS Google Scholar
Kimball, S. R., Farrell, P. A. & Jefferson, L. S. Invited review: Role of insulin in translational control of protein synthesis in skeletal muscle by amino acids or exercise. J. Appl. Physiol.93, 1168–1180 (2002). ArticleCAS Google Scholar
Anderson, L. L., Mao, X., Scott, B. A. & Crowder, C. M. Survival from hypoxia in C. elegans by inactivation of aminoacyl-tRNA synthetases. Science323, 630–633 (2009). ArticleCAS Google Scholar
Back, S. H. et al. Translation attenuation through eIF2α phosphorylation prevents oxidative stress and maintains the differentiated state in β cells. Cell Metab.10, 13–26 (2009). ArticleCAS Google Scholar
Boyce, M. et al. A selective inhibitor of eIF2α dephosphorylation protects cells from ER stress. Science307, 935–939 (2005). ArticleCAS Google Scholar
Tsaytler, P., Harding, H. P., Ron, D. & Bertolotti, A. Selective inhibition of aregulatory subunit of protein phosphatase 1 restores proteostasis. Science332, 91–94 (2011). ArticleCAS Google Scholar
Yamaguchi, S. et al. ATF4-Mediated Induction of 4E-BP1 contributes to pancreatic beta cell survival under endoplasmic reticulum stress. Cell Metab.7, 269–276 (2008). ArticleCAS Google Scholar
Oliver, E. R., Saunders, T. L., Tarle, S. A. & Glaser, T. Ribosomal protein L24defect in belly spot and tail (Bst), a mouse Minute. Development131, 3907–3920 (2004). ArticleCAS Google Scholar
Lu, P. D. et al. Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J.23, 169–179 (2004). ArticleCAS Google Scholar
Enyedi, B., Varnai, P. & Geiszt, M. Redox state of the endoplasmic reticulum is controlled by Ero1L- α and intraluminal calcium. Antioxid. Redox Signal.13, 721–729 (2010). ArticleCAS Google Scholar
Yuan, C. L. et al. Preserved protein synthesis in the heart in response to acute fasting and chronic food restriction despite reductions in liver and skeletal muscle. Am. J. Physiol. Endocrinol. Metabol.295, E216–E222 (2008). ArticleCAS Google Scholar
Puthalakath, H. et al. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell129, 1337–1349 (2007). ArticleCAS Google Scholar
Ghosh, A. P., Klocke, B. J., Ballestas, M. E. & Roth, K. A. CHOP potentially co-operates with FOXO3a in neuronal cells to regulate PUMA and BIM expression in response to ER stress. PloS One7, e39586 (2012). ArticleCAS Google Scholar
Li, G. et al. Role of ERO1- α-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. J. Cell Biol.186, 783–792 (2009). ArticleCAS Google Scholar
Huang, C. C. et al. A bifunctional intronic element regulates the expression of the arginine/lysine transporter Cat-1 via mechanisms involving the purine-rich element binding protein A (Pur α). J. Biol. Chem.284, 32312–32320 (2009). ArticleCAS Google Scholar
Kilberg, M. S., Balasubramanian, M., Fu, L. & Shan, J. The transcription factor network associated with the amino acid response in mammalian cells. Adv. Nutr.3, 295–306 (2012). ArticleCAS Google Scholar
Harding, H. P., Zyryanova, A. F. & Ron, D. Uncoupling proteostasis and development in vitro with a small molecule inhibitor of the pancreatic endoplasmic reticulum kinase, PERK. J. Biol. Chem.287, 44338–44344 (2012). ArticleCAS Google Scholar
Palam, L. R., Baird, T. D. & Wek, R. C. Phosphorylation of eIF2 facilitates ribosomal bypass of an inhibitory upstream ORF to enhance CHOP translation. J. Biol. Chem.286, 10939–10949 (2011). ArticleCAS Google Scholar
Johnson, D. S., Mortazavi, A., Myers, R. M. & Wold, B. Genome-Wide Mapping of in vivo Protein-DNA Interactions. Science316, 1497–1502 (2007). ArticleCAS Google Scholar
Wilbanks, E. G. & Facciotti, M. T. Evaluation of algorithm performance in ChIP-seq peak detection. PLoS One5, e11471 (2010). Article Google Scholar
Sartor, M. et al. Intensity-based hierarchical Bayes method improves testing for differentially expressed genes in microarray experiments. BMC Bioinformatics7, 538 (2006). Article Google Scholar
Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc.4, 44–57 (2009). Article Google Scholar
Sartor, M. A. et al. ConceptGen: a gene set enrichment and gene set relation mapping tool. Bioinformatics26, 456–463 (2010). ArticleCAS Google Scholar
Bailey, T., Boden, M., Whitington, T. & Machanick, P. The value of position-specific priors in motif discovery using MEME. BMC Bioinformatics11, 179 (2010). Article Google Scholar
Hettmann, T., Barton, K. & Leiden, J. M. Microphthalmia due to p53-mediated apoptosis of anterior lens epithelial cells in mice lacking the CREB-2 transcription factor. Dev. Biol.222, 110–123 (2000). ArticleCAS Google Scholar