Inhibition of mitochondrial genome expression triggers the activation of CHOP-10 by a cell signaling dependent on the integrated stress response but not the mitochondrial unfolded protein response

Mitochondrion - Tập 21 - Trang 58-68 - 2015
Sebastien Michel1, Morgane Canonne1, Thierry Arnould1, Patricia Renard1
1Laboratory of Biochemistry and Cell Biology (URBC), NAmur Research Institute for LIfe Sciences (NARILIS), University of Namur (UNamur), 61 rue de Bruxelles, 5000 Namur, Belgium

Tài liệu tham khảo

Acharya, 2009, Mol. Pharmacol., 76, 503, 10.1124/mol.109.056002 Aldridge, 2007, Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements, PLoS One, 2, e874, 10.1371/journal.pone.0000874 Alemi, 2007, Mitochondrial DNA deletions inhibit proteasomal activity and stimulate an autophagic transcript, Free Radic. Biol. Med., 42, 32, 10.1016/j.freeradbiomed.2006.09.014 Arnould, 2002, CREB activation induced by mitochondrial dysfunction is a new signaling pathway that impairs cell proliferation, EMBO J., 21, 53, 10.1093/emboj/21.1.53 Averous, 2004, Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation, J. Biol. Chem., 279, 5288, 10.1074/jbc.M311862200 Back, 2009, Translation attenuation through eIF2alpha phosphorylation prevents oxidative stress and maintains the differentiated state in beta cells, Cell Metab., 10, 13, 10.1016/j.cmet.2009.06.002 Baker, 2012, Protective coupling of mitochondrial function and protein synthesis via the eIF2alpha kinase GCN-2, PLoS Genet., 8, e1002760, 10.1371/journal.pgen.1002760 Balbi, 2004, Chloramphenicol: a review, Pediatr. Rev., 25, 284, 10.1542/pir.25-8-284 Biswas, 1999, Retrograde Ca2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: a novel mode of inter-organelle crosstalk, EMBO J., 18, 522, 10.1093/emboj/18.3.522 Biswas, 2003, Mitochondria to nucleus stress signaling: a distinctive mechanism of NFkappaB/Rel activation through calcineurin-mediated inactivation of IkappaBbeta, J. Cell Biol., 161, 507, 10.1083/jcb.200211104 Black, 2012, Cross-species comparisons of transcriptomic alterations in human and rat primary hepatocytes exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin, Toxicol. Sci., 127, 199, 10.1093/toxsci/kfs069 Boczonadi, 2014, Mitochondria: impaired mitochondrial translation in human disease, Int. J. Biochem. Cell Biol., 48, 77, 10.1016/j.biocel.2013.12.011 Bruhat, 1997, Amino acid limitation induces expression of CHOP, a CCAAT/enhancer binding protein-related gene, at both transcriptional and post-transcriptional levels, J. Biol. Chem., 272, 17588, 10.1074/jbc.272.28.17588 Bruning, 2014, Tetracyclines cause cell stress-dependent ATF4 activation and mTOR inhibition, Exp. Cell Res., 320, 281, 10.1016/j.yexcr.2013.11.012 Calvo, 2010, The mitochondrial proteome and human disease, Annu. Rev. Genomics Hum. Genet., 11, 25, 10.1146/annurev-genom-082509-141720 Castilho, 2014, Keeping the eIF2 alpha kinase Gcn2 in check, Biochim. Biophys. Acta, 1843, 1948, 10.1016/j.bbamcr.2014.04.006 Chandel, 1999, Cells depleted of mitochondrial DNA (rho0) yield insight into physiological mechanisms, FEBS Lett., 454, 173, 10.1016/S0014-5793(99)00783-8 Chopra, 1992, Tetracyclines, molecular and clinical aspects, J. Antimicrob. Chemother., 29, 245, 10.1093/jac/29.3.245 Cortopassi, 2006, Mitochondrial disease activates transcripts of the unfolded protein response and cell cycle and inhibits vesicular secretion and oligodendrocyte-specific transcripts, Mitochondrion, 6, 161, 10.1016/j.mito.2006.05.002 Dogan, 2014, Tissue-specific loss of DARS2 activates stress responses independently of respiratory chain deficiency in the heart, Cell Metab., 19, 458, 10.1016/j.cmet.2014.02.004 Donnelly, 2013, The eIF2alpha kinases: their structures and functions, Cell. Mol. Life Sci., 70, 3493, 10.1007/s00018-012-1252-6 Fujihara, 2009, A human apoB100 transgenic mouse expresses human apoB100 in the RPE and develops features of early AMD, Exp. Eye Res., 88, 1115, 10.1016/j.exer.2009.01.017 Fujita, 2007, CHOP (C/EBP homologous protein) and ASNS (asparagine synthetase) induction in cybrid cells harboring MELAS and NARP mitochondrial DNA mutations, Mitochondrion, 7, 80, 10.1016/j.mito.2006.11.003 Goto, 1990, A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies, Nature, 348, 651, 10.1038/348651a0 Guyton, 1996, Induction of the mammalian stress response gene GADD153 by oxidative stress: role of AP-1 element, Biochem. J., 314, 547, 10.1042/bj3140547 Han, 2013, ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death, Nat. Cell Biol., 15, 481, 10.1038/ncb2738 Harding, 2000, Perk is essential for translational regulation and cell survival during the unfolded protein response, Mol. Cell, 5, 897, 10.1016/S1097-2765(00)80330-5 Harding, 2003, An integrated stress response regulates amino acid metabolism and resistance to oxidative stress, Mol. Cell, 11, 619, 10.1016/S1097-2765(03)00105-9 Horibe, 2007, The chop gene contains an element for the positive regulation of the mitochondrial unfolded protein response, PLoS One, 2, e835, 10.1371/journal.pone.0000835 Houtkooper, 2013, Mitonuclear protein imbalance as a conserved longevity mechanism, Nature, 497, 451, 10.1038/nature12188 Ishikawa, 2009, Gene expression profiling identifies a role for CHOP during inhibition of the mitochondrial respiratory chain, J. Biochem., 146, 123, 10.1093/jb/mvp052 James, 1996, Altered mitochondrial function in fibroblasts containing MELAS or MERRF mitochondrial DNA mutations, Biochem. J., 318, 401, 10.1042/bj3180401 Jiang, 2005, Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition, J. Biol. Chem., 280, 14189, 10.1074/jbc.M413660200 Kilberg, 2009, ATF4-dependent transcription mediates signaling of amino acid limitation, Trends Endocrinol. Metab., 20, 436, 10.1016/j.tem.2009.05.008 Kotokorpi, 2007, Physiological differences between human and rat primary hepatocytes in response to liver X receptor activation by 3-[3-[N-(2-chloro-3-trifluoromethylbenzyl)-(2,2-diphenylethyl)amino]propyloxy]phe nylacetic acid hydrochloride (GW3965), Mol. Pharmacol., 72, 947, 10.1124/mol.107.037358 Lenaz, 2004, Bioenergetics of mitochondrial diseases associated with mtDNA mutations, Biochim. Biophys. Acta, 1658, 89, 10.1016/j.bbabio.2004.03.013 Liu, 2010, Reduction of protein translation and activation of autophagy protect against PINK1 pathogenesis in Drosophila melanogaster, PLoS Genet., 6, e1001237, 10.1371/journal.pgen.1001237 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method, Methods, 25, 402, 10.1006/meth.2001.1262 Maceluch, 2006, The clinical diagnosis and molecular genetics of Kearns–Sayre syndrome: a complex mitochondrial encephalomyopathy, Pediatr. Endocrinol. Rev., 4, 117 Martinus, 1996, Selective induction of mitochondrial chaperones in response to loss of the mitochondrial genome, Eur. J. Biochem., 240, 98, 10.1111/j.1432-1033.1996.0098h.x Mascarenhas, 2008, Gcn4 is required for the response to peroxide stress in the yeast Saccharomyces cerevisiae, Mol. Biol. Cell, 19, 2995, 10.1091/mbc.E07-11-1173 Mercy, 2005, Mitochondrial biogenesis in mtDNA-depleted cells involves a Ca2+-dependent pathway and a reduced mitochondrial protein import, FEBS J., 272, 5031, 10.1111/j.1742-4658.2005.04913.x Mineri, 2009, How do human cells react to the absence of mitochondrial DNA?, PLoS One, 4, e5713, 10.1371/journal.pone.0005713 Miranda, 1999, Oxidative stress and upregulation of mitochondrial biogenesis genes in mitochondrial DNA-depleted HeLa cells, Biochem. Biophys. Res. Commun., 258, 44, 10.1006/bbrc.1999.0580 Moisoi, 2009, Mitochondrial dysfunction triggered by loss of HtrA2 results in the activation of a brain-specific transcriptional stress response, Cell Death Differ., 16, 449, 10.1038/cdd.2008.166 Mouchiroud, 2013, The NAD(+)/sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling, Cell, 154, 430, 10.1016/j.cell.2013.06.016 Moudy, 1995, Abnormal calcium homeostasis and mitochondrial polarization in a human encephalomyopathy, Proc. Natl. Acad. Sci. U. S. A., 92, 729, 10.1073/pnas.92.3.729 Neznanov, 2008, Different effect of proteasome inhibition on vesicular stomatitis virus and poliovirus replication, PLoS One, 3, e1887, 10.1371/journal.pone.0001887 Pearce, 2013, Mitochondrial diseases: translation matters, Mol. Cell. Neurosci., 55, 1, 10.1016/j.mcn.2012.08.013 Pellegrino, 2013, Signaling the mitochondrial unfolded protein response, Biochim. Biophys. Acta, 1833, 410, 10.1016/j.bbamcr.2012.02.019 Piechota, 2006, Nuclear and mitochondrial genome responses in HeLa cells treated with inhibitors of mitochondrial DNA expression, Acta Biochim. Pol., 53, 485, 10.18388/abp.2006_3319 Rainbolt, 2013, Stress-regulated translational attenuation adapts mitochondrial protein import through Tim17A degradation, Cell Metab., 18, 908, 10.1016/j.cmet.2013.11.006 Rath, 2012, Induction of dsRNA-activated protein kinase links mitochondrial unfolded protein response to the pathogenesis of intestinal inflammation, Gut, 61, 1269, 10.1136/gutjnl-2011-300767 Richter, 2013, A mitochondrial ribosomal and RNA decay pathway blocks cell proliferation, Curr. Biol., 23, 535, 10.1016/j.cub.2013.02.019 Ryan, 2007, Mitochondrial-nuclear communications, Annu. Rev. Biochem., 76, 701, 10.1146/annurev.biochem.76.052305.091720 Schroder, 2005, The mammalian unfolded protein response, Annu. Rev. Biochem., 74, 739, 10.1146/annurev.biochem.73.011303.074134 Seidel-Rogol, 2002, Modulation of mitochondrial transcription in response to mtDNA depletion and repletion in HeLa cells, Nucleic Acids Res., 30, 1929, 10.1093/nar/30.9.1929 Seok, 2013, Genomic responses in mouse models poorly mimic human inflammatory diseases, Proc. Natl. Acad. Sci. U. S. A., 110, 3507, 10.1073/pnas.1222878110 Shoffner, 1990, Myoclonic epilepsy and ragged-red fiber disease (MERRF) is associated with a mitochondrial DNA tRNA(Lys) mutation, Cell, 61, 931, 10.1016/0092-8674(90)90059-N Siegelin, 2011, Exploiting the mitochondrial unfolded protein response for cancer therapy in mice and human cells, J. Clin. Invest., 121, 1349, 10.1172/JCI44855 Silva, 2009, Inhibition of mitochondrial function induces an integrated stress response in oligodendroglia, Neurobiol. Dis., 34, 357, 10.1016/j.nbd.2009.02.005 Ubeda, 2000, CHOP gene expression in response to endoplasmic-reticular stress requires NFY interaction with different domains of a conserved DNA-binding element, Nucleic Acids Res., 28, 4987, 10.1093/nar/28.24.4987 Ubeda, 2003, CHOP transcription factor phosphorylation by casein kinase 2 inhibits transcriptional activation, J. Biol. Chem., 278, 40514, 10.1074/jbc.M306404200 Vafai, 2012, Mitochondrial disorders as windows into an ancient organelle, Nature, 491, 374, 10.1038/nature11707 van den Bogert, 1986, Inhibition of mitochondrial protein synthesis leads to proliferation arrest in the G1-phase of the cell cycle, Cancer Lett., 32, 41, 10.1016/0304-3835(86)90037-6 van der Sanden, 2004, J. Biol. Chem., 279, 52007, 10.1074/jbc.M405577200 Vankoningsloo, 2006, CREB activation induced by mitochondrial dysfunction triggers triglyceride accumulation in 3T3-L1 preadipocytes, J. Cell Sci., 119, 1266, 10.1242/jcs.02848 Vattem, 2004, Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells, Proc. Natl. Acad. Sci. U. S. A., 101, 11269, 10.1073/pnas.0400541101 Vives-Bauza, 2006, Enhanced ROS production and antioxidant defenses in cybrids harbouring mutations in mtDNA, Neurosci. Lett., 391, 136, 10.1016/j.neulet.2005.08.049 Wang, 1996, Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP kinase, Science, 272, 1347, 10.1126/science.272.5266.1347 Wang, 2008, Reduced cytosolic protein synthesis suppresses mitochondrial degeneration, Nat. Cell Biol., 10, 1090, 10.1038/ncb1769 Wek, 2006, Coping with stress: eIF2 kinases and translational control, Biochem. Soc. Trans., 34, 7, 10.1042/BST0340007 Zhao, 2002, A mitochondrial specific stress response in mammalian cells, EMBO J., 21, 4411, 10.1093/emboj/cdf445 Zinszner, 1998, CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum, Genes Dev., 12, 982, 10.1101/gad.12.7.982