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Endoplasmic Reticulum Stress in Diseases

Ed. by Blumental-Perry, Anna / Wang, X. Robert

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Emerging Science

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Possible involvement of endoplasmic reticulum stress in the pathogenesis of Alzheimer’s disease

Toru Hosoi
  • Corresponding author
  • Department of Pharmacotherapy, Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima 734-8553, Japan
  • Other articles by this author:
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/ Jun Nomura
  • Corresponding author
  • Department of Biomedical Research, Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima 734-8553, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Koichiro Ozawa
  • Corresponding author
  • Department of Pharmacotherapy, Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima 734-8553, Japan
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  • De Gruyter OnlineGoogle Scholar
/ Akinori Nishi
  • Corresponding author
  • Department of Pharmacology, Kurume University School of Medicine, Kurume, Fukuoka 830-0011, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Yasuyuki Nomura
  • Corresponding author
  • Department of Pharmacology, Kurume University School of Medicine, Kurume, Fukuoka 830-0011, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2015-10-19 | DOI: https://doi.org/10.1515/ersc-2015-0008

Abstract

The endoplasmic reticulum (ER) is an organelle that plays a crucial role in protein quality control such as protein folding. Evidence to indicate the involvement of ER in maintaining cellular homeostasis is increasing. However, when cells are exposed to stressful conditions, which perturb ER function, unfolded proteins accumulate leading to ER stress. Cells then activate the unfolded protein response (UPR) to cope with this stressful condition. In the present review, we will discuss and summarize recent advances in research on the basic mechanisms of the UPR. We also discuss the possible involvement of ER stress in the pathogenesis of Alzheimer’s disease (AD). Potential therapeutic opportunities for diseases targeting ER stress is also described.

Keywords : Alzheimer’s disease; pathogenesis; therapeutics development; endoplasmic reticulum stress; unfolded protein response

References

  • [1] Koumenis C., Naczki C., Koritzinsky M., Rastani S., Diehl A., Sonenberg N., et al., Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2α, Mol. Cell Biol., 2002, 22, 7405-7416 CrossrefGoogle Scholar

  • [2] Kumar R., Azam S., Sullivan J.M., Owen C., Cavener D.R., Zhang P., et al., Brain ischemia and reperfusion activates the eukaryotic initiation factor 2α kinase, PERK, J. Neurochem., 2001, 77, 1418-1421 CrossrefGoogle Scholar

  • [3] Tajiri S., Oyadomari S., Yano S., Morioka M., Gotoh T., Hamada J.I., et al., Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP, Cell Death Differ., 2004, 11, 403-415 CrossrefGoogle Scholar

  • [4] Ikesugi K., Mulhern M.L., Madson C.J., Hosoya K., Terasaki T., Kador P.F., et al., Induction of endoplasmic reticulum stress in retinal pericytes by glucose deprivation, Curr. Eye Res., 2006, 31, 947-953 CrossrefGoogle Scholar

  • [5] Hosoi T., Inoue Y., Nakatsu K., Matsushima N., Kiyose N., Shimamoto A., et al., TERT attenuated ER stress-induced cell death, Biochem. Biophys. Res. Commun., 2014, 447, 378-382 Google Scholar

  • [6] Hosoi T., Oba T., Ozawa K., ER stress-mediated regulation of immune function under glucose-deprived condition in glial cells: up- and down-regulation of PGE2 + IFNγ-induced IL-6 and iNOS expressions, Biochem. Biophys. Res. Commun., 2013, 441, 525-528 Google Scholar

  • [7] Haga N., Saito S., Tsukumo Y., Sakurai J., Furuno A., Tsuruo T., et al., Mitochondria regulate the unfolded protein response leading to cancer cell survival under glucose deprivation conditions, Cancer Sci., 2010, 101, 1125-1132 CrossrefGoogle Scholar

  • [8] Outinen P.A., Sood S.K., Pfeifer S.I., Pamidi S., Podor T.J., Li J., et al., Homocysteine-induced endoplasmic reticulum stress and growth arrest leads to specific changes in gene expression in human vascular endothelial cells, Blood, 1999, 94, 959-967 Google Scholar

  • [9] Outinen P.A., Sood S.K., Liaw P.C., Sarge K.D., Maeda N., Hirsh J., et al., Characterization of the stress-inducing effects of homocysteine, Biochem J. 1998, 332, 213-221 Google Scholar

  • [10] Werstuck G.H., Lentz S.R., Dayal S., Hossain G.S., Sood S.K., Shi Y.Y., et al., Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways, J. Clin. Invest., 2001, 107, 1263-1273 CrossrefGoogle Scholar

  • [11] Seshadri S., Beiser A., Selhub J., Jacques P.F., Rosenberg I.H., D’Agostino R.B., et al., Plasma homocysteine as a risk factor for dementia and Alzheimer’s disease. N. Engl. J. Med., 2002, 346, 476-483 Google Scholar

  • [12] Morris M.S., Homocysteine and Alzheimer’s disease, Lancet Neurol., 2003, 2, 425-428 CrossrefGoogle Scholar

  • [13] Hosoi T., Ogawa K., Ozawa K., Homocysteine induces X-boxbinding protein 1 splicing in the mice brain, Neurochem. Int., 2010, 56, 216-220 CrossrefGoogle Scholar

  • [14] Tang C.H., Chiu Y.C., Huang C.F., Chen Y.W., Chen P.C., Arsenic induces cell apoptosis in cultured osteoblasts through endoplasmic reticulum stress, Toxicol. Appl. Pharmacol., 2009, 241, 173-181 Google Scholar

  • [15] Gong Y., Wu J., Huang Y., Shen S., Han X., Nonylphenol induces apoptosis in rat testicular Sertoli cells via endoplasmic reticulum stress, Toxicol Lett., 2009, 186, 84-95 Google Scholar

  • [16] Isomura M., Kotake Y., Masuda K., Miyara M., Okuda K., Samizo S., et al., Tributyltin-induced endoplasmic reticulum stress and its Ca(2+)-mediated mechanism, Toxicol. Appl. Pharmacol. 2013, 272, 137-146 Google Scholar

  • [17] Ron D., Walter P., Signal integration in the endoplasmic reticulum unfolded protein response, Nat. Rev. Mol. Cell Biol. 2007, 8, 519-529 CrossrefGoogle Scholar

  • [18] Hosoi T., Hyoda K., Okuma Y., Nomura Y., Ozawa K., Akt up- and down-regulation in response to endoplasmic reticulum stress, Brain Res., 2007, 1152, 27-31 Google Scholar

  • [19] Hosoi T., Tamubo T., Horie N., Okuma Y., Nomura Y., Ozawa K., TEK/Tie2 is a novel gene involved in endoplasmic reticulum stress, J. Pharmacol. Sci., 2010, 114, 230-233 CrossrefGoogle Scholar

  • [20] Hosoi T., Ozawa K., Endoplasmic reticulum stress in disease: mechanisms and therapeutic opportunities, Clin Sci (Lond), 2010, 118, 19-29 CrossrefGoogle Scholar

  • [21] Hosoi T., Korematsu K., Horie N., Suezawa T., Okuma Y., Nomura Y., et al., Inhibition of casein kinase 2 modulates XBP1-GRP78 arm of unfolded protein responses in cultured glial cells, PLoS One, 2012, 7, e40144 Google Scholar

  • [22] Hyoda K., Hosoi T., Horie N., Okuma Y., Ozawa K., Nomura Y., PI3K-Akt inactivation induced CHOP expression in endoplasmic reticulum-stressed cells. Biochem. Biophys. Res. Commun. 2006, 340, 286-290 Google Scholar

  • [23] Bertolotti A., Zhang Y., Hendershot L.M., Harding H.P., Ron D., Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response, Nat. Cell Biol., 2000, 2, 326-332 Google Scholar

  • [24] Carrara M., Prischi F., Nowak P.R., Kopp M.C., Ali M.M., Noncanonical binding of BiP ATPase domain to Ire1 and Perk is dissociated by unfolded protein CH1 to initiate ER stress signaling, Elife, 2015, 18, 4 Google Scholar

  • [25] Shen J., Chen X., Hendershot L., Prywes R., ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals, Dev. Cell, 2002, 3, 99-111 CrossrefGoogle Scholar

  • [26] Credle J.J., Finer-Moore J.S., Papa F.R., Stroud R.M., Walter P., On the mechanism of sensing unfolded protein in the endoplasmic reticulum, Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 18773-18784 CrossrefGoogle Scholar

  • [27] Gardner B.M., Walter P., Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response, Science, 2011, 333, 1891-1894 Google Scholar

  • [28] Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., et al., Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1, Science, 2000, 287, 664-666 Google Scholar

  • [29] Ogata M., Hino S., Saito A., Morikawa K., Kondo S., Kanemoto S., et al., Autophagy is activated for cell survival after endoplasmic reticulum stress, Mol. Cell Biol., 2006, 26, 9220-9231 CrossrefGoogle Scholar

  • [30] Nishitoh H., Matsuzawa A., Tobiume K., Saegusa K., Takeda K., Inoue K., et al., ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats, Genes Dev., 2002, 16, 1345-1355 Google Scholar

  • [31] Groenendyk J., Peng Z., Dudek E., Fan X., Mizianty M.J., Dufey E., et al., Interplay between the oxidoreductase PDIA6 and microRNA-322 controls the response to disrupted endoplasmic reticulum calcium homeostasis, Sci. Signal, 2014, 7, ra54 Google Scholar

  • [32] Yoshida H., Haze K., Yanagi H., Yura T., Mori K., 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. 1998, 273, 33741-33749 Google Scholar

  • [33] Hollien J., Weissman J.S., Decay of endoplasmic reticulumlocalized mRNAs during the unfolded protein response, Science, 2006, 313, 104-107 Google Scholar

  • [34] Pavitt G.D., Ramaiah K.V., Kimball S.R., Hinnebusch A.G., eIF2 independently binds two distinct eIF2B subcomplexes that catalyze and regulate guanine-nucleotide exchange, Genes Dev., 1998, 12, 514-526 Google Scholar

  • [35] Ma Y., Hendershot L.M., Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress, J. Biol. Chem., 2003, 278, 34864-34873 Google Scholar

  • [36] Brush M.H., Weiser D.C., Shenolikar S., Growth arrest and DNA damage-inducible protein GADD34 targets protein phosphatase 1α to the endoplasmic reticulum and promotes dephosphorylation of the α subunit of eukaryotic translation initiation factor 2, Mol. Cell Biol., 2003, 23, 1292-1303 Google Scholar

  • [37] Novoa I., Zhang Y., Zeng H., Jungreis R., Harding H.P., Ron D., Stress-induced gene expression requires programmed recovery from translational repression, EMBO J., 2003, 22, 1180-1187 CrossrefGoogle Scholar

  • [38] Harding H.P., Zeng H., Zhang Y., Jungries R., Chung P., Plesken H., et al., Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival, Mol. Cell, 2001, 7, 1153-1163 CrossrefGoogle Scholar

  • [39] Jousse C., Oyadomari S., Novoa I., Lu P., Zhang Y., Harding H.P., et al., Inhibition of a constitutive translation initiation factor 2α phosphatase, CReP, promotes survival of stressed cells, J. Cell Biol., 2003, 163, 767-775 Google Scholar

  • [40] Haze K., Yoshida H., Yanagi H., Yura T., Mori K., Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress, Mol Biol Cell. 1999, 10, 3787-3799 CrossrefGoogle Scholar

  • [41] Sato Y., Nadanaka S., Okada T., Okawa K., Mori K., Luminal domain of ATF6 alone is sufficient for sensing endoplasmic reticulum stress and subsequent transport to the Golgi apparatus, Cell Struct. Funct., 2011, 36, 35-47 CrossrefGoogle Scholar

  • [42] Shen J., Chen X., Hendershot L., Prywes R. et al., ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals, Dev. Cell 2002, 3, 99-111 CrossrefGoogle Scholar

  • [43] Yoshida H., Matsui T., Yamamoto A., Okada T., Mori K., XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor, Cell, 2001, 107, 881-891 CrossrefGoogle Scholar

  • [44] Kondo S., Murakami T., Tatsumi K., Ogata M., Kanemoto S., Otori K., et al., OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes, Nat. Cell Biol. 2005, 7, 186-194 CrossrefGoogle Scholar

  • [45] Kondo S., Saito A., Hino S., Murakami T., Ogata M., Kanemoto S., et al., BBF2H7, a novel transmembrane bZIP transcription factor, is a new type of endoplasmic reticulum stress transducer, Mol. Cell Biol. 2007, 27, 1716-1729 CrossrefGoogle Scholar

  • [46] Zhang K., Shen X., Wu J., Sakaki K., Saunders T., Rutkowski D.T., et al., Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response, Cell, 2006, 124, 587-599 CrossrefGoogle Scholar

  • [47] Hoozemans J.J., Veerhuis R., Van Haastert E.S., Rozemuller J.M., Baas F., Eikelenboom P., et al., The unfolded protein response is activated in Alzheimer’s disease, Acta Neuropathol., 2005, 110, 165-172 CrossrefGoogle Scholar

  • [48] Hoozemans J.J., van Haastert E.S., Nijholt D.A., Rozemuller A.J., Eikelenboom P., Scheper W., The unfolded protein response is activated in pretangle neurons in Alzheimer’s disease hippocampus, Am. J. Pathol., 2009, 174, 1241-1251 CrossrefGoogle Scholar

  • [49] Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., et al., Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-β. Nature, 2000, 403, 98-103 Google Scholar

  • [50] Hitomi J., Katayama T., Eguchi Y., Kudo T., Taniguchi M., Koyama Y., et al., Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death, J. Cell Biol., 2004, 165, 347-356 Google Scholar

  • [51] Ohta K., Mizuno A., Li S., Itoh M., Ueda M., Ohta E., et al., Endoplasmic reticulum stress enhances γ-secretase activity, Biochem. Biophys. Res. Commun. 2011, 416, 362-366 Google Scholar

  • [52] Katayama T., Imaizumi K., Honda A., Yoneda T., Kudo T., Takeda M., et al., Disturbed activation of endoplasmic reticulum stress transducers by familial Alzheimer’s disease-linked presenilin-1 mutations, J. Biol. Chem. 2001, 276, 43446-43454 Google Scholar

  • [53] Katayama T., Imaizumi K., Sato N., Miyoshi K., Kudo T., Hitomi J., et al., Presenilin-1 mutations downregulate the signalling pathway of the unfolded-protein response, Nat. Cell Biol., 1999, 1, 479-485 Google Scholar

  • [54] Tomiyama T., Nagata T., Shimada H., Teraoka R., Fukushima A., Kanemitsu H., et al., A new amyloid beta variant favoring oligomerization in Alzheimer’s-type dementia, Ann. Neurol., 2008, 63, 377-387 CrossrefGoogle Scholar

  • [55] Nishitsuji K., Tomiyama T., Ishibashi K., Ito K., Teraoka R., Lambert M.P., et al., The E693Delta mutation in amyloid precursor protein increases intracellular accumulation of amyloid beta oligomers and causes endoplasmic reticulum stress-induced apoptosis in cultured cells, Am. J. Pathol. 2009,174, 957-969 CrossrefGoogle Scholar

  • [56] Kondo T., Asai M., Tsukita K., Kutoku Y., Ohsawa Y., Sunada Y., et al., Modeling Alzheimer’s disease with iPSCs reveals stress phenotypes associated with intracellular Aβ and differential drug responsiveness, Cell Stem Cell, 2013, 12, 487-496 CrossrefGoogle Scholar

  • [57] Sato N., Hori O., Yamaguchi A., Lambert J.C., Chartier-Harlin M.C., Robinson P.A., et al., A novel presenilin-2 splice variant in human Alzheimer’s disease brain tissue, J. Neurochem., 1999, 72, 2498-2505 Google Scholar

  • [58] Sato N., Imaizumi K., Manabe T., Taniguchi M., Hitomi J., Katayama T., et al., Increased production of beta-amyloid and vulnerability to endoplasmic reticulum stress by an aberrant spliced form of presenilin 2, J. Biol. Chem. 2001, 276, 2108-2114 Google Scholar

  • [59] Uehara T., Kikuchi Y., Nomura Y., Caspase activation accompanying cytochrome c release from mitochondria is possibly involved in nitric oxide-induced neuronal apoptosis in SH-SY5Y cells, J. Neurochem., 1999, 72, 196-205 Google Scholar

  • [60] Nomura Y., Neuronal apoptosis and protection: effects of nitric oxide and endoplasmic reticulum-related proteins, Biol. Pharm. Bull. 2004, 27, 961-963 CrossrefGoogle Scholar

  • [61] Law A., Gauthier S., Quirion R., Say NO to Alzheimer’s disease: the putative links between nitric oxide and dementia of the Alzheimer’s type, Brain Res. Brain Res. Rev., 2001, 35, 73-96 CrossrefGoogle Scholar

  • [62] Uehara T., Nakamura T., Yao D., Shi Z.Q., Gu Z., Ma Y., et al., S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration, Nature, 2006, 441, 513-517 Google Scholar

  • [63] Lazarov O., Demars M.P., All in the Family: How the APPs Regulate Neurogenesis, Front. Neurosci, 2012, 6, 81 Google Scholar

  • [64] Casas-Tinto S., Zhang Y., Sanchez-Garcia J., Gomez-Velazquez M., Rincon-Limas D.E., Fernandez-Funez P., The ER stress factor XBP1s prevents amyloid-β neurotoxicity, Hum Mol Genet., 2011, 20, 2144-2160 CrossrefGoogle Scholar

  • [65] Reinhardt S., Schuck F., Grösgen S., Riemenschneider M., Hartmann T., Postina R., et al., Unfolded protein response signaling by transcription factor XBP-1 regulates ADAM10 and is affected in Alzheimer’s disease, FASEB J. 2014, 28, 978-997 CrossrefGoogle Scholar

  • [66] Kuhn P.H., Wang H., Dislich B., Colombo A., Zeitschel U., Ellwart J.W., et al., ADAM10 is the physiologically relevant, constitutive alpha-secretase of the amyloid precursor protein in primary neurons, EMBO J. 2010, 29, 3020-3032 Google Scholar

  • [67] Jorissen E., Prox J., Bernreuther C., Weber S., Schwanbeck R., Serneels L., et al., The disintegrin/metalloproteinase ADAM10 is essential for the establishment of the brain cortex, J Neurosci. 2010, 30, 4833-4844 CrossrefGoogle Scholar

  • [68] Ring S., Weyer S.W., Kilian S.B., Waldron E., Pietrzik C.U., Filippov M.A., et al., The secreted β-amyloid precursor protein ectodomain APPsα is sufficient to rescue the anatomical, behavioral, and electrophysiological abnormalities of APP-deficient mice, J. Neurosci., 2007, 27, 7817-7826 CrossrefGoogle Scholar

  • [69] Mattson M.P., Cheng B., Culwell A.R., Esch F.S., Lieberburg I., Rydel R.E., Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of the beta-amyloid precursor protein, Neuron 1993, 10, 243-254 CrossrefGoogle Scholar

  • [70] Caillé I., Allinquant B., Dupont E., Bouillot C., Langer A., Müller U., et al., Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development, 2004, 131, 2173-2181 Google Scholar

  • [71] Suh J., Choi S.H., Romano D.M., Gannon M.A., Lesinski A.N., Kim D.Y., et al., ADAM10 missense mutations potentiate β-amyloid accumulation by impairing prodomain chaperone function, Neuron, 2013, 80, 385-401 Google Scholar

  • [72] Ricobaraza A., Cuadrado-Tejedor M., Marco S., Pérez-Otaño I., García-Osta A., Phenylbutyrate rescues dendritic spine loss associated with memory deficits in a mouse model of Alzheimer disease. Hippocampus, 2012, 22, 1040-1050 CrossrefGoogle Scholar

  • [73] Liu S.Y., Wang W., Cai Z.Y., Yao L.F., Chen Z.W., Wang C.Y., et al., Polymorphism -116C/G of human X-box-binding protein 1 promoter is associated with risk of Alzheimer’s disease, CNS Neurosci. Ther., 2013, 19, 229-234 CrossrefGoogle Scholar

  • [74] Kakiuchi C., Iwamoto K., Ishiwata M., Bundo M., Kasahara T., Kusumi I., et al., Impaired feedback regulation of XBP1 as a genetic risk factor for bipolar disorder, Nat. Genet. 2003, 35, 171-175 CrossrefGoogle Scholar

  • [75] Chang R.C., Wong A.K., Ng H.K., Hugon J., Phosphorylation of eukaryotic initiation factor-2α (eIF2α) is associated with neuronal degeneration in Alzheimer’s disease. Neuroreport, 2002, 13, 2429-2432 CrossrefGoogle Scholar

  • [76] Page G., Rioux Bilan A., Ingrand S., Lafay-Chebassier C., Pain S., Perault Pochat M.C., et al., Activated double-stranded RNA-dependent protein kinase and neuronal death in models of Alzheimer’s disease, Neuroscience, 2006, 139, 1343-1354 Google Scholar

  • [77] Kim H.S., Choi Y., Shin K.Y., Joo Y., Lee Y.K,. Jung S.Y., et al., Swedish amyloid precursor protein mutation increases phosphorylation of eIF2alpha in vitro and in vivo, J. Neurosci. Res. 2007, 85, 1528-1537 CrossrefGoogle Scholar

  • [78] O’Connor T., Sadleir K.R., Maus E., Velliquette R.A., Zhao J., Cole S.L., et al., Phosphorylation of the translation initiation factor eIF2alpha increases BACE1 levels and promotes amyloidogenesis, Neuron, 2008, 60, 988-1009 CrossrefGoogle Scholar

  • [79] Ma T., Trinh M.A., Wexler A.J., Bourbon C., Gatti E., Pierre P., et al., Suppression of eIF2α kinases alleviates Alzheimer’s disease-related plasticity and memory deficits. Nat. Neurosci. 2013, 16, 1299-1305 CrossrefGoogle Scholar

  • [80] Costa-Mattioli M., Gobert D., Stern E., Gamache K., Colina R., Cuello C., et al., eIF2α phosphorylation bidirectionally regulates the switch from short- to long-term synaptic plasticity and memory, Cell, 2007, 129, 195-206 Google Scholar

  • [81] Kaneko M., Koike H., Saito R., Kitamura Y., Okuma Y., Nomura Y., Loss of HRD1-mediated protein degradation causes amyloid precursor protein accumulation and amyloid-beta generation, J. Neurosci. 2010, 30, 3924-3932 CrossrefGoogle Scholar

  • [82] Jung E.S., Hong H., Kim C., Mook-Jung I., Acute ER stress regulates amyloid precursor protein processing through ubiquitin-dependent degradation, Sci. Rep. 2015, 5, 8805 CrossrefGoogle Scholar

  • [83] Saito R., Kaneko M., Kitamura Y., Takata K., Kawada K., Okuma Y., et al., Effects of oxidative stress on the solubility of HRD1, a ubiquitin ligase implicated in Alzheimer’s disease, PLoS One. 2014, 9, e94576 CrossrefGoogle Scholar

  • [84] Yang Y., Turner R.S., Gaut J.R., The chaperone BiP/GRP78 binds to amyloid precursor protein and decreases Aβ40 and Aβ42 secretion, J. Biol. Chem., 1998, 273, 25552-25555 Google Scholar

  • [85] Hoshino T., Nakaya T., Araki W., Suzuki K., Suzuki T., Mizushima T., Endoplasmic reticulum chaperones inhibit the production of amyloid-beta peptides, Biochem J. 2007, 402, 581-589 Google Scholar

  • [86] Abisambra J.F., Jinwal U.K., Blair L.J., O’Leary J.C. 3rd, Li Q., Brady S., et al., Tau accumulation activates the unfolded protein response by impairing endoplasmic reticulumassociated degradation, J. Neurosci., 2013, 33, 9498-9507 CrossrefGoogle Scholar

  • [87] Janssens S., Pulendran B., Lambrecht B.N., Emerging functions of the unfolded protein response in immunity, Nat. Immunol., 2014, 15, 910-919 CrossrefGoogle Scholar

  • [88] Iwakoshi N.N., Lee A.H., Vallabhajosyula P., Otipoby K.L., Rajewsky K., Glimcher L.H., Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1, Nat. Immunol., 2003, 4, 321-329 CrossrefGoogle Scholar

  • [89] Martinon F., Chen X., Lee A.H., Glimcher L.H., TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages, Nat. Immunol., 2010, 11, 411-418 CrossrefGoogle Scholar

  • [90] Kemp K.L., Lin Z., Zhao F., Gao B., Song J., Zhang K., et al., The serine-threonine kinase inositol-requiring enzyme 1α (IRE1α) promotes IL-4 production in T helper cells, J. Biol. Chem. 2013, 288, 33272-33282 Google Scholar

  • [91] Xue X., Piao J.H., Nakajima A., Sakon-Komazawa S., Kojima Y., Mori K., et al., Tumor necrosis factor α (TNFα) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFα, J. Biol. Chem., 2005, 280, 33917-33925 Google Scholar

  • [92] Lin W., Harding H.P., Ron D., Popko B., Endoplasmic reticulum stress modulates the response of myelinating oligodendrocytes to the immune cytokine interferon-γ, J. Cell Biol., 2005, 169, 603-612 Google Scholar

  • [93] Heppner F.L., Ransohoff R.M., Becher B., Immune attack: the role of inflammation in Alzheimer disease, Nat. Rev. Neurosci., 2015, 16, 358-372 CrossrefGoogle Scholar

  • [94] von Zahn J., Möller T., Kettenmann H., Nolte C., Microglial phagocytosis is modulated by pro- and anti-inflammatory cytokines, Neuroreport, 1997, 8, 3851-3856 CrossrefGoogle Scholar

  • [95] Chan A., Magnus T., Gold R., Phagocytosis of apoptotic inflammatory cells by microglia and modulation by different cytokines: mechanism for removal of apoptotic cells in the inflamed nervous system, Glia, 2001, 33, 87-95 CrossrefGoogle Scholar

  • [96] Paresce D.M., Ghosh R.N., Maxfield F.R., Microglial cells internalize aggregates of the Alzheimer’s disease amyloid beta-protein via a scavenger receptor, Neuron, 1996, 17, 553-565 CrossrefGoogle Scholar

  • [97] Kakimura J., Kitamura Y., Takata K., Umeki M., Suzuki S., Shibagaki K., et al., Microglial activation and amyloid-beta clearance induced by exogenous heat-shock proteins, FASEB J. 2002, 16, 601-603 Google Scholar

  • [98] Liu B., Gao H.M., Wang J.Y., Jeohn G.H., Cooper C.L., Hong J.S., Role of nitric oxide in inflammation-mediated neurodegeneration, Ann. N. Y. Acad. Sci. 2002, 962, 318-331 Google Scholar

  • [99] Hosoi T., Ozawa K., Molecular approaches to the treatment, prophylaxis, and diagnosis of Alzheimer’s disease: endoplasmic reticulum stress and immunological stress in pathogenesis of Alzheimer’s disease, J. Pharmacol. Sci. 2012, 118, 319-324 CrossrefGoogle Scholar

  • [100] Hosoi T., Honda M., Oba T., Ozawa K., ER stress upregulated PGE₂/IFNγ-induced IL-6 expression and down-regulated iNOS expression in glial cells, Sci. Rep. 2013, 3, 3388 CrossrefGoogle Scholar

  • [101] Mosconi L., Pupi A., De Leon M.J., Brain glucose hypometabolism and oxidative stress in preclinical Alzheimer’s disease, Ann. N. Y. Acad. Sci. 2008, 1147, 180-195 Google Scholar

  • [102] de Leon M.J., Mosconi L., Blennow K., DeSanti S., Zinkowski R., Mehta P.D., et al., Imaging and CSF studies in the preclinical diagnosis of Alzheimer’s disease, Ann. N Y Acad. Sci., 2007, 1097, 114-145 Google Scholar

  • [103] Zhu Z., Yan J., Jiang W., Yao X.G., Chen J., Chen L., et al., Arctigenin effectively ameliorates memory impairment in Alzheimer’s disease model mice targeting both β-amyloid production and clearance, J. Neurosci., 2013, 33, 13138-13149 CrossrefGoogle Scholar

  • [104] Sekine Y., Zyryanova A., Crespillo-Casado A., Fischer P.M., Harding H.P., et al., Mutations in a translation initiation factor identify the target of a memory-enhancing compound, Science, (in press), DOI: 10.1126 Google Scholar

  • [105] Sidrauski C., Tsai J.C., Kampmann M., Hearn B.R., Vedantham P., Jaishankar P., et al., Pharmacological dimerization and activation of the exchange factor eIF2B antagonizes the integrated stress response, Elife, 2015, 4, e07314 Google Scholar

  • [106] Sidrauski C., Acosta-Alvear D., Khoutorsky A., Vedantham P., Hearn B.R., Li H., et al., Pharmacological brake-release of mRNA translation enhances cognitive memory, Elife, 2013, 2, e00498 Google Scholar

  • [107] Halliday M., Radford H., Sekine Y., Moreno J., Verity N., le Quesne J., et al., Partial restoration of protein synthesis rates by the small molecule ISRIB prevents neurodegeneration without pancreatic toxicity, Cell Death Dis., 2015, 6, e1672 Google Scholar

  • [108] Back S.H., Scheuner D., Han J., Song B., Ribick M., Wang J., et al., Translation attenuation through eIF2α phosphorylation prevents oxidative stress and maintains the differentiated state in beta cells, Cell Metab., 2009, 10,13-26 CrossrefGoogle Scholar

  • [109] Burrows J.A., Willis L.K., Perlmutter D.H., Chemical chaperones mediate increased secretion of mutant alpha 1-antitrypsin (α1-AT) Z: A potential pharmacological strategy for prevention of liver injury and emphysema in α 1-AT deficiency, Proc Natl Acad Sci U S A., 2000, 97, 1796-1801 CrossrefGoogle Scholar

  • [110] Perlmutter D.H., Chemical chaperones: a pharmacological strategy for disorders of protein folding and trafficking, Pediatr. Res., 2002, 52, 832-836 CrossrefGoogle Scholar

  • [111] de Almeida S.F., Picarote G., Fleming J.V., Carmo-Fonseca M., Azevedo J.E., de Sousa M., Chemical chaperones reduce endoplasmic reticulum stress and prevent mutant HFE aggregate formation, J. Biol. Chem., 2007, 282, 27905-27912 Google Scholar

  • [112] Hosoi T., Yamaguchi R., Noji K., Matsuo S., Baba S., Toyoda K., et al., Flurbiprofen ameliorated obesity by attenuating leptin resistance induced by endoplasmic reticulum stress, EMBO Mol. Med. 2014, 6, 335-346 Google Scholar

  • [113] Hosoi T., Toyoda K., Nakatsu K., Ozawa K., Caffeine attenuated ER stress-induced leptin resistance in neurons, Neurosci Lett. 2014, 569, 23-26 Google Scholar

  • [114] Ricobaraza A., Cuadrado-Tejedor M., Pérez-Mediavilla A., Frechilla D., Del Río J., García-Osta A., Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer’s disease mouse model, Neuropsychopharmacology, 2009, 34, 1721-1732 CrossrefGoogle Scholar

  • [115] Cuadrado-Tejedor M., Ricobaraza A.L., Torrijo R., Franco R., Garcia-Osta A., Phenylbutyrate is a multifaceted drug that exerts neuroprotective effects and reverses the Alzheimer´s disease-like phenotype of a commonly used mouse model, Curr Pharm Des., 2013, 19, 5076-5084 Google Scholar

  • [116] Mimori S., Okuma Y., Kaneko M., Kawada K., Hosoi T., Ozawa K., et al., Protective effects of 4-phenylbutyrate derivatives on the neuronal cell death and endoplasmic reticulum stress, Biol. Pharm. Bull., 2012, 35, 84-90 CrossrefGoogle Scholar

  • [117] Mimori S., Okuma Y., Kaneko M., Kawada K., Nomura Y., Murakami Y., et al., Discovery of synthetic methoxysubstituted 4-phenylbutyric acid derivatives as chemical chaperons, Chem. Lett. 2013, 42, 1051-1052. CrossrefGoogle Scholar

  • [118] Mimori S., Ohtaka H., Koshikawa Y., Kawada K., Kaneko M., Okuma Y., et al., 4-Phenylbutyric acid protects against neuronal cell death by primarily acting as a chemical chaperone rather than histone deacetylase inhibitor, Bioorg. Med. Chem. Lett. 2013, 23, 6015-6018 Google Scholar

  • [119] Ozcan U., Yilmaz E., Ozcan L., Furuhashi M., Vaillancourt E., Smith R.O., et al., Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes, Science, 2006, 313, 1137-1140 Google Scholar

  • [120] Chen Y., Liu C.P., Xu K.F., Mao X.D., Lu Y.B., Fang L., et al., Effect of taurine-conjugated ursodeoxycholic acid on endoplasmic reticulum stress and apoptosis induced by advanced glycation end products in cultured mouse podocytes, Am. J. Nephrol. 2008, 28, 1014-1022 CrossrefGoogle Scholar

  • [121] Solá S, Castro RE, Laires PA, Steer CJ, Rodrigues CM. Tauroursodeoxycholic acid prevents amyloid-beta peptide-induced neuronal death via a phosphatidylinositol 3-kinasedependent signaling pathway, Mol. Med., 2003, 9, 226-234 Google Scholar

  • [122] in t’ Veld B.A., Ruitenberg A., Hofman A., Launer L.J., van Duijn C.M., Stijnen T., et al., Nonsteroidal antiinflammatory drugs and the risk of Alzheimer’s disease, N. Engl. J. Med. 2001, 345, 1515-1521 Google Scholar

  • [123] Yamazaki T., Muramoto M., Oe T., Morikawa N., Okitsu O., Nagashima T., et al., Diclofenac, a non-steroidal anti-inflammatory drug, suppresses apoptosis induced by endoplasmic reticulum stresses by inhibiting caspase signaling, Neuropharmacology, 2006, 50, 558-567 CrossrefGoogle Scholar

  • [124] Hosoi T., Sasaki M., Baba S., Ozawa K., Effect of pranoprofen on endoplasmic reticulum stress in the primary cultured glial cells, Neurochem. Int., 2009, 54, 1-6 CrossrefGoogle Scholar

  • [125] Ryu E.J., Harding H.P., Angelastro J.M., Vitolo O.V., Ron D., Greene L.A., Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson’s disease, J. Neurosci., 2002, 22, 10690-10698 Google Scholar

  • [126] Kumar R., Krause G.S., Yoshida H., Mori K., DeGracia D.J., Dysfunction of the unfolded protein response during global brain ischemia and reperfusion, J. Cereb. Blood Flow Metab., 2003, 23, 462-471 Google Scholar

  • [127] Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., et al., Regulated translation initiation controls stress-induced gene expression in mammalian cells, Mol. Cell, 2000, 6, 1099-1108 CrossrefGoogle Scholar

  • [128] Hosoi T., Sasaki M., Miyahara T., Hashimoto C., Matsuo S., Yoshii M., et al., Endoplasmic reticulum stress induces leptin resistance, Mol. Pharmacol. 2008, 74, 1610-1619 CrossrefGoogle Scholar

  • [129] Hosoi T., Ozawa K., Possible involvement of endoplasmic reticulum stress in obesity associated with leptin resistance, J. Med. Invest. 2009, 56, 296-298 CrossrefGoogle Scholar

  • [130] Ozcan U., Cao Q., Yilmaz E., Lee A.H., Iwakoshi N.N., Ozdelen E., et al., Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes, Science, 2004, 306, 457-461 Google Scholar

  • [131] Wang M., Kaufman R.J., The impact of the endoplasmic reticulum protein-folding environment on cancer development, Nat. Rev. Cancer., 2014, 14, 581-597 CrossrefGoogle Scholar

  • [132] Wu J., Kaufman R.J., From acute ER stress to physiological roles of the Unfolded Protein Response, Cell Death Differ., 2006, 13, 374-384 CrossrefGoogle Scholar

About the article

Received: 2015-06-30

Accepted: 2015-09-01

Published Online: 2015-10-19


Citation Information: Endoplasmic Reticulum Stress in Diseases, Volume 2, Issue 1, ISSN (Online) 2300-4266, DOI: https://doi.org/10.1515/ersc-2015-0008.

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© 2015 Toru Hosoi et al.. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

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