Cellular responses to endoplasmic reticulum stress and apoptosis (original) (raw)

• Adesnik M, Lande M, Martin T, Sabatini DD (1976) Retention of mRNA on the endoplasmic reticulum membranes after in vivo disassembly of polysomes by an inhibitor of initiation. J Cell Biol 71:307–313. doi:10.1083/jcb.71.1.307
  Article PubMed CAS Google Scholar
• Lande MA, Adesnik M, Sumida M, Tashiro Y, Sabatini DD (1975) Direct association of messenger RNA with microsomal membranes in human diploid fibroblasts. J Cell Biol 65:513–528. doi:10.1083/jcb.65.3.513
  Article PubMed CAS Google Scholar
• Dobson CM (2004) Principles of protein folding, misfolding and aggregation. Semin Cell Dev Biol 15:3–16. doi:10.1016/j.semcdb.2003.12.008
  Article PubMed CAS Google Scholar
• Karplus M, Weaver DL (1994) Protein folding dynamics: the diffusion-collision model and experimental data. Protein Sci 3:650–668
  Article PubMed CAS Google Scholar
• Cheung MS, Garcia AE, Onuchic JN (2002) Protein folding mediated by solvation: water expulsion and formation of the hydrophobic core occur after the structural collapse. Proc Natl Acad Sci USA 99:685–690. doi:10.1073/pnas.022387699
  Article PubMed CAS Google Scholar
• Saliba RS, Munro PM, Luthert PJ, Cheetham ME (2002) The cellular fate of mutant rhodopsin: quality control, degradation and aggresome formation. J Cell Sci 115:2907–2918
  PubMed CAS Google Scholar
• Koo EH, Lansbury PT Jr, Kelly JW (1999) Amyloid diseases: abnormal protein aggregation in neurodegeneration. Proc Natl Acad Sci USA 96:9989–9990. doi:10.1073/pnas.96.18.9989
  Article PubMed CAS Google Scholar
• Petkova AT, Ishii Y, Balbach JJ et al (2002) A structural model for Alzheimer’s beta -amyloid fibrils based on experimental constraints from solid state NMR. Proc Natl Acad Sci USA 99:16742–16747. doi:10.1073/pnas.262663499
  Article PubMed CAS Google Scholar
• Lomas DA, Evans DL, Finch JT, Carrell RW (1992) The mechanism of Z alpha 1-antitrypsin accumulation in the liver. Nature 357:605–607. doi:10.1038/357605a0
  Article PubMed CAS Google Scholar
• Celotto AM, Palladino MJ (2005) Drosophila: a “model” model system to study neurodegeneration. Mol Interv 5:292–303. doi:10.1124/mi.5.5.9
  Article PubMed CAS Google Scholar
• Bilen J, Bonini NM (2005) Drosophila as a model for human neurodegenerative disease. Annu Rev Genet 39:153–171. doi:10.1146/annurev.genet.39.110304.095804
  Article PubMed CAS Google Scholar
• Lu B, Vogel H (2008) Drosophila models of neurodegenerative diseases. Annu Rev Pathol 4:315–342. doi:10.1146/annurev.pathol.3.121806.151529
  Article CAS Google Scholar
• Haas IG, Wabl M (1983) Immunoglobulin heavy chain binding protein. Nature 306:387–389. doi:10.1038/306387a0
  Article PubMed CAS Google Scholar
• Munro S, Pelham HR (1986) An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46:291–300. doi:10.1016/0092-8674(86)90746-4
  Article PubMed CAS Google Scholar
• Hendershot L, Wei J, Gaut J, Melnick J, Aviel S, Argon Y (1996) Inhibition of immunoglobulin folding and secretion by dominant negative BiP ATPase mutants. Proc Natl Acad Sci USA 93:5269–5274. doi:10.1073/pnas.93.11.5269
  Article PubMed CAS Google Scholar
• Feldheim D, Rothblatt J, Schekman R (1992) Topology and functional domains of Sec63p, an endoplasmic reticulum membrane protein required for secretory protein translocation. Mol Cell Biol 12:3288–3296
  PubMed CAS Google Scholar
• Schlenstedt G, Harris S, Risse B, Lill R, Silver PA (1995) A yeast DnaJ homologue, Scj1p, can function in the endoplasmic reticulum with BiP/Kar2p via a conserved domain that specifies interactions with Hsp70s. J Cell Biol 129:979–988. doi:10.1083/jcb.129.4.979
  Article PubMed CAS Google Scholar
• Chevalier M, Rhee H, Elguindi EC, Blond SY (2000) Interaction of murine BiP/GRP78 with the DnaJ homologue MTJ1. J Biol Chem 275:19620–19627. doi:10.1074/jbc.M001333200
  Article PubMed CAS Google Scholar
• Cunnea PM, Miranda-Vizuete A, Bertoli G et al (2003) ERdj5, an endoplasmic reticulum (ER)-resident protein containing DnaJ and thioredoxin domains, is expressed in secretory cells or following ER stress. J Biol Chem 278:1059–1066. doi:10.1074/jbc.M206995200
  Article PubMed CAS Google Scholar
• Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4:181–191. doi:10.1038/nrm1052
  Article PubMed CAS Google Scholar
• Bourbon HM, Gonzy-Treboul G, Peronnet F et al (2002) A P-insertion screen identifying novel X-linked essential genes in Drosophila. Mech Dev 110:71–83. doi:10.1016/S0925-4773(01)00566-4
  Article PubMed CAS Google Scholar
• Christodoulou S, Lockyer AE, Foster JM, Hoheisel JD, Roberts DB (1997) Nucleotide sequence of a Drosophila melanogaster cDNA encoding a calnexin homologue. Gene 191:143–148. doi:10.1016/S0378-1119(97)00025-5
  Article PubMed CAS Google Scholar
• Hong CS, Ganetzky B (1996) Molecular characterization of neurally expressing genes in the para sodium channel gene cluster of drosophila. Genetics 142:879–892
  PubMed CAS Google Scholar
• Rosenbaum EE, Hardie RC, Colley NJ (2006) Calnexin is essential for rhodopsin maturation, Ca2+ regulation, and photoreceptor cell survival. Neuron 49:229–241. doi:10.1016/j.neuron.2005.12.011
  Article PubMed CAS Google Scholar
• Price ER, Zydowsky LD, Jin MJ, Baker CH, McKeon FD, Walsh CT (1991) Human cyclophilin B: a second cyclophilin gene encodes a peptidyl-prolyl isomerase with a signal sequence. Proc Natl Acad Sci USA 88:1903–1907. doi:10.1073/pnas.88.5.1903
  Article PubMed CAS Google Scholar
• Bryant Z, Subrahmanyan L, Tworoger M et al (1999) Characterization of differentially expressed genes in purified Drosophila follicle cells: toward a general strategy for cell type-specific developmental analysis. Proc Natl Acad Sci USA 96:5559–5564. doi:10.1073/pnas.96.10.5559
  Article PubMed CAS Google Scholar
• Freedman RB (1989) Protein disulfide isomerase: multiple roles in the modification of nascent secretory proteins. Cell 57:1069–1072. doi:10.1016/0092-8674(89)90043-3
  Article PubMed CAS Google Scholar
• Anelli T, Alessio M, Bachi A et al (2003) Thiol-mediated protein retention in the endoplasmic reticulum: the role of ERp44. EMBO J 22:5015–5022. doi:10.1093/emboj/cdg491
  Article PubMed CAS Google Scholar
• Tien AC, Rajan A, Schulze KL et al (2008) Ero1L, a thiol oxidase, is required for Notch signaling through cysteine bridge formation of the Lin12-Notch repeats in Drosophila melanogaster. J Cell Biol 182:1113–1125. doi:10.1083/jcb.200805001
  Article PubMed CAS Google Scholar
• Schroder M, Kaufman RJ (2005) The mammalian unfolded protein response. Annu Rev Biochem 74:739–789. doi:10.1146/annurev.biochem.73.011303.074134
  Article PubMed CAS Google Scholar
• Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519–529. doi:10.1038/nrm2199
  Article PubMed CAS Google Scholar
• Bonifacino JS, Weissman AM (1998) Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu Rev Cell Dev Biol 14:19–57. doi:10.1146/annurev.cellbio.14.1.19
  Article PubMed CAS Google Scholar
• Tsai B, Ye Y, Rapoport TA (2002) Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat Rev Mol Cell Biol 3:246–255. doi:10.1038/nrm780
  Article PubMed CAS Google Scholar
• Cox JS, Shamu CE, Walter P (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73:1197–1206. doi:10.1016/0092-8674(93)90648-A
  Article PubMed CAS Google Scholar
• Mori K, Ma W, Gething MJ, Sambrook J (1993) A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74:743–756. doi:10.1016/0092-8674(93)90521-Q
  Article PubMed CAS Google Scholar
• Koizumi N, Martinez IM, Kimata Y, Kohno K, Sano H, Chrispeels MJ (2001) Molecular characterization of two Arabidopsis Ire1 homologs, endoplasmic reticulum-located transmembrane protein kinases. Plant Physiol 127:949–962. doi:10.1104/pp.010636
  Article PubMed CAS Google Scholar
• Sidrauski C, Walter P (1997) The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90:1031–1039. doi:10.1016/S0092-8674(00)80369-4
  Article PubMed CAS Google Scholar
• Liu CY, Schroder M, Kaufman RJ (2000) Ligand-independent dimerization activates the stress response kinases IRE1 and PERK in the lumen of the endoplasmic reticulum. J Biol Chem 275:24881–24885. doi:10.1074/jbc.M004454200
  Article PubMed CAS Google Scholar
• Plongthongkum N, Kullawong N, Panyim S, Tirasophon W (2007) Ire1 regulated XBP1 mRNA splicing is essential for the unfolded protein response (UPR) in Drosophila melanogaster. Biochem Biophys Res Commun 354:789–794. doi:10.1016/j.bbrc.2007.01.056
  Article PubMed CAS Google Scholar
• Hollien J, Weissman JS (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313:104–107. doi:10.1126/science.1129631
  Article PubMed CAS Google Scholar
• Wang XZ, Harding HP, Zhang Y, Jolicoeur EM, Kuroda M, Ron D (1998) Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J 17:5708–5717. doi:10.1093/emboj/17.19.5708
  Article PubMed CAS Google Scholar
• Tirasophon W, Welihinda AA, Kaufman RJ (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 12:1812–1824. doi:10.1101/gad.12.12.1812
  Article PubMed CAS Google Scholar
• Bertolotti A, Wang X, Novoa I et al (2001) Increased sensitivity to dextran sodium sulfate colitis in IRE1beta-deficient mice. J Clin Invest 107:585–593. doi:10.1172/JCI11476
  Article PubMed CAS Google Scholar
• Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2:326–332. doi:10.1038/35014014
  Article PubMed CAS Google Scholar
• Okamura K, Kimata Y, Higashio H, Tsuru A, Kohno K (2000) Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem Biophys Res Commun 279:445–450. doi:10.1006/bbrc.2000.3987
  Article PubMed CAS Google Scholar
• Kimata Y, Oikawa D, Shimizu Y, Ishiwata-Kimata Y, Kohno K (2004) A role for BiP as an adjustor for the endoplasmic reticulum stress-sensing protein Ire1. J Cell Biol 167:445–456. doi:10.1083/jcb.200405153
  Article PubMed CAS Google Scholar
• Oikawa D, Kimata Y, Kohno K (2007) Self-association and BiP dissociation are not sufficient for activation of the ER stress sensor Ire1. J Cell Sci 120:1681–1688. doi:10.1242/jcs.002808
  Article PubMed CAS Google Scholar
• Credle JJ, Finer-Moore JS, Papa FR, Stroud RM, Walter P (2005) On the mechanism of sensing unfolded protein in the endoplasmic reticulum. Proc Natl Acad Sci USA 102:18773–18784. doi:10.1073/pnas.0509487102
  Article PubMed CAS Google Scholar
• Shamu CE, Walter P (1996) Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J 15:3028–3039
  PubMed CAS Google Scholar
• Welihinda AA, Kaufman RJ (1996) The unfolded protein response pathway in Saccharomyces cerevisiae. Oligomerization and trans-phosphorylation of Ire1p (Ern1p) are required for kinase activation. J Biol Chem 271:18181–18187. doi:10.1074/jbc.271.30.18181
  Article PubMed CAS Google Scholar
• Liu CY, Wong HN, Schauerte JA, Kaufman RJ (2002) The protein kinase/endoribonuclease IRE1alpha that signals the unfolded protein response has a luminal N-terminal ligand-independent dimerization domain. J Biol Chem 277:18346–18356. doi:10.1074/jbc.M112454200
  Article PubMed CAS Google Scholar
• Papa FR, Zhang C, Shokat K, Walter P (2003) Bypassing a kinase activity with an ATP-competitive drug. Science 302:1533–1537. doi:10.1126/science.1090031
  Article PubMed CAS Google Scholar
• Cox JS, Walter P (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87:391–404. doi:10.1016/S0092-8674(00)81360-4
  Article PubMed CAS Google Scholar
• Mori K, Kawahara T, Yoshida H, Yanagi H, Yura T (1996) Signalling from endoplasmic reticulum to nucleus: transcription factor with a basic-leucine zipper motif is required for the unfolded protein-response pathway. Genes Cells 1:803–817. doi:10.1046/j.1365-2443.1996.d01-274.x
  Article PubMed CAS Google Scholar
• Nikawa J, Akiyoshi M, Hirata S, Fukuda T (1996) Saccharomyces cerevisiae IRE2/HAC1 is involved in IRE1-mediated KAR2 expression. Nucleic Acids Res 24:4222–4226. doi:10.1093/nar/24.21.4222
  Article PubMed CAS Google Scholar
• Shen X, Ellis RE, Lee K, Liu CY, Yang K, Solomon A, Yoshida H, Morimoto R, Kurnit DM, Mori K, Kaufman RJ (2001) Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107:893–903. doi:10.1016/S0092-8674(01)00612-2
  Article PubMed CAS Google Scholar
• Yoshida H, Okada T, Haze K et al (2001) Endoplasmic reticulum stress-induced formation of transcription factor complex ERSF including NF-Y (CBF) and activating transcription factors 6alpha and 6beta that activates the mammalian unfolded protein response. Mol Cell Biol 21:1239–1248. doi:10.1128/MCB.21.4.1239-1248.2001
  Article PubMed CAS Google Scholar
• Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92–96. doi:10.1038/415092a
  Article PubMed CAS Google Scholar
• Sidrauski C, Cox JS, Walter P (1996) tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell 87:405–413. doi:10.1016/S0092-8674(00)81361-6
  Article PubMed CAS Google Scholar
• Chapman RE, Walter P (1997) Translational attenuation mediated by an mRNA intron. Curr Biol 7:850–859. doi:10.1016/S0960-9822(06)00373-3
  Article PubMed CAS Google Scholar
• Ruegsegger U, Leber JH, Walter P (2001) Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107:103–114. doi:10.1016/S0092-8674(01)00505-0
  Article PubMed CAS Google Scholar
• Yoshida H, Oku M, Suzuki M, Mori K (2006) pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J Cell Biol 172:565–575. doi:10.1083/jcb.200508145
  Article PubMed CAS Google Scholar
• Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101:249–258. doi:10.1016/S0092-8674(00)80835-1
  Article PubMed CAS Google Scholar
• Friedlander R, Jarosch E, Urban J, Volkwein C, Sommer T (2000) A regulatory link between ER-associated protein degradation and the unfolded-protein response. Nat Cell Biol 2:379–384. doi:10.1038/35017001
  Article PubMed CAS Google Scholar
• Yoshida H, Matsui T, Hosokawa N, Kaufman RJ, Nagata K, Mori K (2003) A time-dependent phase shift in the mammalian unfolded protein response. Dev Cell 4:265–271. doi:10.1016/S1534-5807(03)00022-4
  Article PubMed CAS Google Scholar
• Lee AH, Iwakoshi NN, Glimcher LH (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23:7448–7459. doi:10.1128/MCB.23.21.7448-7459.2003
  Article PubMed CAS Google Scholar
• Oda Y, Okada T, Yoshida H, Kaufman RJ, Nagata K, Mori K (2006) Derlin-2 and Derlin-3 are regulated by the mammalian unfolded protein response and are required for ER-associated degradation. J Cell Biol 172:383–393. doi:10.1083/jcb.200507057
  Article PubMed CAS Google Scholar
• Sriburi R, Jackowski S, Mori K, Brewer JW (2004) XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J Cell Biol 167:35–41. doi:10.1083/jcb.200406136
  Article PubMed CAS Google Scholar
• Acosta-Alvear D, Zhou Y, Blais A et al (2007) XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol Cell 27:53–66. doi:10.1016/j.molcel.2007.06.011
  Article PubMed CAS Google Scholar
• Reimold AM, Iwakoshi NN, Manis J, Vallabhajosyula P, Szomolanyi-Tsuda E, Gravallese EM, Friend D, Grusby MJ, Alt F, Glimcher LH (2001) Plasma cell differentiation requires the transcription factor XBP-1. Nature 412:300–307. doi:10.1038/35085509
  Article PubMed CAS Google Scholar
• Reimold AM, Etkin A, Clauss I et al (2000) An essential role in liver development for transcription factor XBP-1. Genes Dev 14:152–157
  PubMed CAS Google Scholar
• Niwa M, Patil CK, DeRisi J, Walter P (2005) Genome-scale approaches for discovering novel nonconventional splicing substrates of the Ire1 nuclease. Genome Biol 6:R3. doi:10.1186/gb-2004-6-1-r3
  Article PubMed Google Scholar
• Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinase by transmembrane protein kinase IRE1. Science 287:664–666. doi:10.1126/science.287.5453.664
  Article PubMed CAS Google Scholar
• Haze K, Yoshida H, Yanagi H, Yura T, Mori K (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10:3787–3799
  PubMed CAS Google Scholar
• Wang Y, Shen J, Arenzana N, Tirasophon W, Kaufman RJ, Prywes R (2000) Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J Biol Chem 275:27013–27020
  PubMed CAS Google Scholar
• Yoshida H, Okada T, Haze K et al (2000) ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol Cell Biol 20:6755–6767. doi:10.1128/MCB.20.18.6755-6767.2000
  Article PubMed CAS Google Scholar
• Shen J, Snapp EL, Lippincott-Schwartz J, Prywes R (2005) Stable binding of ATF6 to BiP in the endoplasmic reticulum stress response. Mol Cell Biol 25:921–932. doi:10.1128/MCB.25.3.921-932.2005
  Article PubMed CAS Google Scholar
• Ye J, Rawson RB, Komuro R et al (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6:1355–1364. doi:10.1016/S1097-2765(00)00133-7
  Article PubMed CAS Google Scholar
• Shen J, Chen X, Hendershot L, Prywes R (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3:99–111. doi:10.1016/S1534-5807(02)00203-4
  Article PubMed CAS Google Scholar
• Hong M, Luo S, Baumeister P et al (2004) Underglycosylation of ATF6 as a novel sensing mechanism for activation of the unfolded protein response. J Biol Chem 279:11354–11363. doi:10.1074/jbc.M309804200
  Article PubMed CAS Google Scholar
• Yoshida H, Haze K, Yanagi H, Yura T, Mori K (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 273:33741–33749. doi:10.1074/jbc.273.50.33741
  Article PubMed CAS Google Scholar
• van Huizen R, Martindale JL, Gorospe M, Holbrook NJ (2003) P58IPK, a novel endoplasmic reticulum stress-inducible protein and potential negative regulator of eIF2alpha signaling. J Biol Chem 278:15558–15564. doi:10.1074/jbc.M212074200
  Article PubMed Google Scholar
• Kokame K, Kato H, Miyata T (2001) Identification of ERSE-II, a new cis-acting element responsible for the ATF6-dependent mammalian unfolded protein response. J Biol Chem 276:9199–9205. doi:10.1074/jbc.M010486200
  Article PubMed CAS Google Scholar
• Shi Y, Vattem KM, Sood R et al (1998) Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol 18:7499–7509
  PubMed CAS Google Scholar
• Shi Y, An J, Liang J et al (1999) Characterization of a mutant pancreatic eIF-2alpha kinase, PEK, and co-localization with somatostatin in islet delta cells. J Biol Chem 274:5723–5730. doi:10.1074/jbc.274.9.5723
  Article PubMed CAS Google Scholar
• Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271–274. doi:10.1038/16729
  Article PubMed CAS Google Scholar
• Marciniak SJ, Garcia-Bonilla L, Hu J, Harding HP, Ron D (2006) Activation-dependent substrate recruitment by the eukaryotic translation initiation factor 2 kinase PERK. J Cell Biol 172:201–209. doi:10.1083/jcb.200508099
  Article PubMed CAS Google Scholar
• Harding HP, Novoa I, Zhang Y et al (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099–1108. doi:10.1016/S1097-2765(00)00108-8
  Article PubMed CAS Google Scholar
• Lu PD, Harding HP, Ron D (2004) Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol 167:27–33. doi:10.1083/jcb.200408003
  Article PubMed CAS Google Scholar
• Vattem KM, Wek RC (2004) Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci USA 101:11269–11274. doi:10.1073/pnas.0400541101
  Article PubMed CAS Google Scholar
• Harding HP, Zhang Y, Zeng H et al (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11:619–633. doi:10.1016/S1097-2765(03)00105-9
  Article PubMed CAS Google Scholar
• Jiang HY, Wek SA, McGrath BC et al (2004) Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol Cell Biol 24:1365–1377. doi:10.1128/MCB.24.3.1365-1377.2004
  Article PubMed CAS Google Scholar
• Ma Y, Brewer JW, Diehl JA, Hendershot LM (2002) Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J Mol Biol 318:1351–1365. doi:10.1016/S0022-2836(02)00234-6
  Article PubMed CAS Google Scholar
• Pomar N, Berlanga JJ, Campuzano S, Hernandez G, Elias M, de Haro C (2003) Functional characterization of Drosophila melanogaster PERK eukaryotic initiation factor 2alpha (eIF2alpha) kinase. Eur J Biochem 270:293–306. doi:10.1046/j.1432-1033.2003.03383.x
  Article PubMed CAS Google Scholar
• Yan W, Frank CL, Korth MJ et al (2002) Control of PERK eIF2alpha kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc Natl Acad Sci USA 99:15920–15925. doi:10.1073/pnas.252341799
  Article PubMed CAS Google Scholar
• Brush MH, Weiser DC, Shenolikar S (2003) Growth arrest and DNA damage-inducible protein GADD34 targets protein phosphatase 1 alpha to the endoplasmic reticulum and promotes dephosphorylation of the alpha subunit of eukaryotic translation initiation factor 2. Mol Cell Biol 23:1292–1303. doi:10.1128/MCB.23.4.1292-1303.2003
  Article PubMed CAS Google Scholar
• Ma Y, Hendershot LM (2003) Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J Biol Chem 278:34864–34873. doi:10.1074/jbc.M301107200
  Article PubMed CAS Google Scholar
• Novoa I, Zhang Y, Zeng H, Jungreis R, Harding HP, Ron D (2003) Stress-induced gene expression requires programmed recovery from translational repression. EMBO J 22:1180–1187. doi:10.1093/emboj/cdg112
  Article PubMed CAS Google Scholar
• Meusser B, Hirsch C, Jarosch E, Sommer T (2005) ERAD: the long road to destruction. Nat Cell Biol 7:766–772. doi:10.1038/ncb0805-766
  Article PubMed CAS Google Scholar
• Ruddock LW, Molinari M (2006) N-glycan processing in ER quality control. J Cell Sci 119:4373–4380. doi:10.1242/jcs.03225
  Article PubMed CAS Google Scholar
• Hosokawa N, Wada I, Hasegawa K et al (2001) A novel ER alpha-mannosidase-like protein accelerates ER-associated degradation. EMBO Rep 2:415–422
  PubMed CAS Google Scholar
• Molinari M, Calanca V, Galli C, Lucca P, Paganetti P (2003) Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299:1397–1400. doi:10.1126/science.1079474
  Article PubMed CAS Google Scholar
• Oda Y, Hosokawa N, Wada I, Nagata K (2003) EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299:1394–1397. doi:10.1126/science.1079181
  Article PubMed CAS Google Scholar
• Szathmary R, Bielmann R, Nita-Lazar M, Burda P, Jakob CA (2005) Yos9 protein is essential for degradation of misfolded glycoproteins and may function as lectin in ERAD. Mol Cell 19:765–775. doi:10.1016/j.molcel.2005.08.015
  Article PubMed CAS Google Scholar
• Plemper RK, Bohmler S, Bordallo J, Sommer T, Wolf DH (1997) Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature 388:891–895. doi:10.1038/42276
  Article PubMed CAS Google Scholar
• Pilon M, Schekman R, Romisch K (1997) Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. EMBO J 16:4540–4548. doi:10.1093/emboj/16.15.4540
  Article PubMed CAS Google Scholar
• Zhou M, Schekman R (1999) The engagement of Sec61p in the ER dislocation process. Mol Cell 4:925–934. doi:10.1016/S1097-2765(00)80222-1
  Article PubMed CAS Google Scholar
• Ye Y, Shibata Y, Yun C, Ron D, Rapoport TA (2004) A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429:841–847. doi:10.1038/nature02656
  Article PubMed CAS Google Scholar
• Lilley BN, Ploegh HL (2004) A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429:834–840. doi:10.1038/nature02592
  Article PubMed CAS Google Scholar
• Carvalho P, Goder V, Rapoport TA (2006) Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126:361–373. doi:10.1016/j.cell.2006.05.043
  Article PubMed CAS Google Scholar
• Denic V, Quan EM, Weissman JS (2006) A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation. Cell 126:349–359. doi:10.1016/j.cell.2006.05.045
  Article PubMed CAS Google Scholar
• Gauss R, Jarosch E, Sommer T, Hirsch C (2006) A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery. Nat Cell Biol 8:849–854. doi:10.1038/ncb1445
  Article PubMed CAS Google Scholar
• Elsasser S, Finley D (2005) Delivery of ubiquitinated substrates to protein-unfolding machines. Nat Cell Biol 7:742–749. doi:10.1038/ncb0805-742
  Article PubMed CAS Google Scholar
• Nakagawa T, Yuan J (2000) Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol 150:887–894. doi:10.1083/jcb.150.4.887
  Article PubMed CAS Google Scholar
• Nakagawa T, Zhu H, Morishima N et al (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98–103. doi:10.1038/47513
  Article PubMed CAS Google Scholar
• Tan Y, Dourdin N, Wu C, De Veyra T, Elce JS, Greer PA (2006) Ubiquitous calpains promote caspase-12 and JNK activation during endoplasmic reticulum stress-induced apoptosis. J Biol Chem 281:16016–16024. doi:10.1074/jbc.M601299200
  Article PubMed CAS Google Scholar
• Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y (2002) An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 277:34287–34294. doi:10.1074/jbc.M204973200
  Article PubMed CAS Google Scholar
• Rao RV, Castro-Obregon S, Frankowski H et al (2002) Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J Biol Chem 277:21836–21842. doi:10.1074/jbc.M202726200
  Article PubMed CAS Google Scholar
• Fischer H, Koenig U, Eckhart L, Tschachler E (2002) Human caspase 12 has acquired deleterious mutations. Biochem Biophys Res Commun 293:722–726. doi:10.1016/S0006-291X(02)00289-9
  Article PubMed CAS Google Scholar
• Hitomi J, Katayama T, Eguchi Y et al (2004) Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death. J Cell Biol 165:347–356. doi:10.1083/jcb.200310015
  Article PubMed CAS Google Scholar
• Fawcett TW, Martindale JL, Guyton KZ, Hai T, Holbrook NJ (1999) Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem J 339(Pt 1):135–141. doi:10.1042/0264-6021:3390135
  Article PubMed CAS Google Scholar
• Lin JH, Li H, Zhang Y, Ron D, Walter P (2009) Divergent effects of PERK and IRE1 signaling on cell viability. PLoS ONE 4:e4170. doi:10.1371/journal.pone.0004170
  Article PubMed CAS Google Scholar
• Zinszner H, Kuroda M, Wang X et al (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12:982–995. doi:10.1101/gad.12.7.982
  Article PubMed CAS Google Scholar
• McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21:1249–1259. doi:10.1128/MCB.21.4.1249-1259.2001
  Article PubMed CAS Google Scholar
• Puthalakath H, O’Reilly LA, Gunn P et al (2007) ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129:1337–1349. doi:10.1016/j.cell.2007.04.027
  Article PubMed CAS Google Scholar
• Haynes CM, Titus EA, Cooper AA (2004) Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol Cell 15:767–776. doi:10.1016/j.molcel.2004.08.025
  Article PubMed CAS Google Scholar
• Marciniak SJ, Yun CY, Oyadomari S et al (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 18:3066–3077. doi:10.1101/gad.1250704
  Article PubMed CAS Google Scholar
• Cullinan SB, Zhang D, Hannink M, Arvisais E, Kaufman RJ, Diehl JA (2003) Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol 23:7198–7209. doi:10.1128/MCB.23.20.7198-7209.2003
  Article PubMed CAS Google Scholar
• Venugopal R, Jaiswal AK (1998) Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 17:3145–3156. doi:10.1038/sj.onc.1202237
  Article PubMed CAS Google Scholar
• He CH, Gong P, Hu B et al (2001) Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. J Biol Chem 276:20858–20865. doi:10.1074/jbc.M101198200
  Article PubMed CAS Google Scholar
• Nguyen T, Sherratt PJ, Nioi P, Yang CS, Pickett CB (2005) Nrf2 controls constitutive and inducible expression of ARE-driven genes through a dynamic pathway involving nucleocytoplasmic shuttling by Keap1. J Biol Chem 280:32485–32492. doi:10.1074/jbc.M503074200
  Article PubMed CAS Google Scholar
• Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K (2002) Takeda. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 16:1345–1355. doi:10.1101/gad.992302
  Article PubMed CAS Google Scholar
• Lin JH, Li H, Yasumura D et al (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318:944–949. doi:10.1126/science.1146361
  Article PubMed CAS Google Scholar
• Ryoo HD, Domingos PM, Kang MJ, Steller H (2007) Unfolded protein response in a Drosophila model for retinal degeneration. EMBO J 26:242–252. doi:10.1038/sj.emboj.7601477
  Article PubMed CAS Google Scholar
• Colley NJ, Cassill JA, Baker EK, Zuker CS (1995) Defective intracellular transport is the molecular basis of rhodopsin-dependent dominant retinal degeneration. Proc Natl Acad Sci USA 92:3070–3074. doi:10.1073/pnas.92.7.3070
  Article PubMed CAS Google Scholar
• Davidson FF, Steller H (1998) Blocking apoptosis prevents blindness in Drosophila retinal degeneration mutants. Nature 391:587–591. doi:10.1038/35385
  Article PubMed CAS Google Scholar
• Mendes CS, Levet C, Chatelain G, et al. (2009) ER stress protects from retinal degeneration. EMBO J (in press)
• Pizzo P, Pozzan T (2007) Mitochondria-endoplasmic reticulum choreography: structure and signaling dynamics. Trends Cell Biol 17:511–517. doi:10.1016/j.tcb.2007.07.011
  Article PubMed CAS Google Scholar
• Wei MC, Zong WX, Cheng EH et al (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292:727–730. doi:10.1126/science.1059108
  Article PubMed CAS Google Scholar
• Scorrano L, Oakes SA, Opferman JT et al (2003) BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300:135–139. doi:10.1126/science.1081208
  Article PubMed CAS Google Scholar
• Zong WX, Li C, Hatzivassiliou G et al (2003) Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 162:59–69. doi:10.1083/jcb.200302084
  Article PubMed CAS Google Scholar
• Hetz C, Bernasconi P, Fisher J et al (2006) Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 312:572–576. doi:10.1126/science.1123480
  Article PubMed CAS Google Scholar
• Chae HJ, Kim HR, Xu C et al (2004) BI-1 regulates an apoptosis pathway linked to endoplasmic reticulum stress. Mol Cell 15:355–366. doi:10.1016/j.molcel.2004.06.038
  Article PubMed CAS Google Scholar
• Mathai JP, Germain M, Shore GC (2005) BH3-only BIK regulates BAX, BAK-dependent release of Ca2+ from endoplasmic reticulum stores and mitochondrial apoptosis during stress-induced cell death. J Biol Chem 280:23829–23836. doi:10.1074/jbc.M500800200
  Article PubMed CAS Google Scholar
• Sevrioukov EA, Burr J, Huang EW et al (2007) Drosophila Bcl-2 proteins participate in stress-induced apoptosis, but are not required for normal development. Genesis 45:184–193. doi:10.1002/dvg.20279
  Article PubMed CAS Google Scholar
• Galindo KA, Lu WJ, Park JH, Abrams JM (2009) The Bax/Bak ortholog in Drosophila, Debcl, exerts limited control over programmed cell death. Development 136:275–283. doi:10.1242/dev.019042
  Article PubMed CAS Google Scholar
• Doumanis J, Dorstyn L, Kumar S (2007) Molecular determinants of the subcellular localization of the Drosophila Bcl-2 homologues DEBCL and BUFFY. Cell Death Differ 14:907–915
  PubMed CAS Google Scholar
• Chami M, Oules B, Szabadkai G, Tacine R, Rizzuto R, Paterlini-Brechot P (2008) Role of SERCA1 truncated isoform in the proapoptotic calcium transfer from ER to mitochondria during ER stress. Mol Cell 32:641–651. doi:10.1016/j.molcel.2008.11.014
  Article PubMed CAS Google Scholar
• Rutkowski DT, Arnold SM, Miller CN et al (2006) Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol 4:e374. doi:10.1371/journal.pbio.0040374
  Article PubMed CAS Google Scholar
• Bence NF, Sampat RM, Kopito RR (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292:1552–1555. doi:10.1126/science.292.5521.1552
  Article PubMed CAS Google Scholar
• Cooper AA, Gitler AD, Cashikar A et al (2006) Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson’s models. Science 313:324–328. doi:10.1126/science.1129462
  Article PubMed CAS Google Scholar
• Humphries P, Kenna P, Farrar GJ (1992) On the molecular genetics of retinitis pigmentosa. Science 256:804–808. doi:10.1126/science.1589761
  Article PubMed CAS Google Scholar
• Colley NJ, Cassill JA, Baker EK, Zuker CS (1995) Defective intracellular transport is the molecular basis of rhodopsin-dependent dominant retinal degeneration. Proc Natl Acad Sci USA 92:3070–3074. doi:10.1073/pnas.92.7.3070
  Article PubMed CAS Google Scholar
• Kurada P, O’Tousa JE (1995) Retinal degeneration caused by dominant rhodopsin mutations in Drosophila. Neuron 14:571–579. doi:10.1016/0896-6273(95)90313-5
  Article PubMed CAS Google Scholar
• Galy A, Roux MJ, Sahel JA, Leveillard T, Giangrande A (2005) Rhodopsin maturation defects induce photoreceptor death by apoptosis: a fly model for RhodopsinPro23His human retinitis pigmentosa. Hum Mol Genet 14:2547–2557. doi:10.1093/hmg/ddi258
  Article PubMed CAS Google Scholar
• Delepine M, Nicolino M, Barrett T, Golamaully M, Lathrop GM, Julier C (2000) EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat Genet 25:406–409. doi:10.1038/78085
  Article PubMed CAS Google Scholar
• Harding HP, Zeng H, Zhang Y et al (2001) Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol Cell 7:1153–1163. doi:10.1016/S1097-2765(01)00264-7
  Article PubMed CAS Google Scholar
• Fonseca SG, Fukuma M, Lipson KL et al (2005) WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic beta-cells. J Biol Chem 280:39609–39615. doi:10.1074/jbc.M507426200
  Article PubMed CAS Google Scholar
• Yamada T, Ishihara H, Tamura A et al (2006) WFS1-deficiency increases endoplasmic reticulum stress, impairs cell cycle progression and triggers the apoptotic pathway specifically in pancreatic beta-cells. Hum Mol Genet 15:1600–1609. doi:10.1093/hmg/ddl081
  Article PubMed CAS Google Scholar
• Lee AH, Chu GC, Iwakoshi NN, Glimcher LH (2005) XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J 24:4368–4380. doi:10.1038/sj.emboj.7600903
  Article PubMed CAS Google Scholar
• Ma Y, Hendershot LM (2004) The role of the unfolded protein response in tumour development: friend or foe? Nat Rev Cancer 4:966–977. doi:10.1038/nrc1505
  Article PubMed CAS Google Scholar
• Koumenis C, Naczki C, Koritzinsky M et al (2002) Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 22:7405–7416. doi:10.1128/MCB.22.21.7405-7416.2002
  Article PubMed CAS Google Scholar
• Koritzinsky M, Magagnin MG, van den Beucken T et al (2006) Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control. EMBO J 25:1114–1125. doi:10.1038/sj.emboj.7600998
  Article PubMed CAS Google Scholar
• Blais JD, Filipenko V, Bi M et al (2004) Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol Cell Biol 24:7469–7482. doi:10.1128/MCB.24.17.7469-7482.2004
  Article PubMed CAS Google Scholar
• Feldman DE, Chauhan V, Koong AC (2005) The unfolded protein response: a novel component of the hypoxic stress response in tumors. Mol Cancer Res 3:597–605. doi:10.1158/1541-7786.MCR-05-0221
  Article PubMed CAS Google Scholar
• Romero-Ramirez L, Cao H, Nelson D et al (2004) XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res 64:5943–5947. doi:10.1158/0008-5472.CAN-04-1606
  Article PubMed CAS Google Scholar
• Carrasco DR, Sukhdeo K, Protopopova M et al (2007) The differentiation and stress response factor XBP-1 drives multiple myeloma pathogenesis. Cancer Cell 11:349–360. doi:10.1016/j.ccr.2007.02.015
  Article PubMed CAS Google Scholar