Eukaryotic translation initiation factor 2 α phosphorylation as a therapeutic target in diabetes

References

• Richter JD, Sonenberg N. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 2005;433(7025):477-80
   PubMed Web of Science ®Google Scholar
• Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012;149(2):274-93
   PubMed Web of Science ®Google Scholar
• Thoreen CC, Chantranupong L, Keys HR, et al. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 2012;485(7396):109-13
   PubMed Web of Science ®Google Scholar
• Nanbru C, Lafon I, Audigier S, et al. Alternative translation of the proto-oncogene c-myc by an internal ribosome entry site. J Biol Chem 1997;272(51):32061-6
   PubMedGoogle Scholar
• Stoneley M, Paulin FE, Le Quesne JP, et al. C-Myc 5’ untranslated region contains an internal ribosome entry segment. Oncogene 1998;16(3):423-8
   PubMedGoogle Scholar
• Stoneley M, Subkhankulova T, Le Quesne JP, et al. Analysis of the c-myc IRES; a potential role for cell-type specific trans-acting factors and the nuclear compartment. Nucleic Acids Res 2000;28(3):687-94
   PubMedGoogle Scholar
• Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009;136(4):731-45
   PubMed Web of Science ®Google Scholar
• Tahara M, Ohsawa A, Saito S, Kimura M. In vitro phosphorylation of initiation factor 2 alpha (aIF2 alpha) from hyperthermophilic archaeon Pyrococcus horikoshii OT3. J Biochem 2004;135(4):479-85
   PubMedGoogle Scholar
• Scheuner D, Song B, McEwen E, et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 2001;7(6):1165-76
   PubMed Web of Science ®Google Scholar
• Scheuner D, Vander Mierde D, Song B, et al. Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis. Nat Med 2005;11(7):757-64
   PubMed Web of Science ®Google Scholar
• Nakamura T, Furuhashi M, Li P, et al. Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell 2010;140(3):338-48
   PubMed Web of Science ®Google Scholar
• Dever TE, Hinnebusch AG. GCN2 whets the appetite for amino acids. Mol Cell 2005;18(2):141-2
   PubMedGoogle Scholar
• Chen JJ. Regulation of protein synthesis by the heme-regulated eIF2alpha kinase: relevance to anemias. Blood 2007;109(7):2693-9
   PubMedGoogle Scholar
• Harding HP, Ron D. Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 2002;51(Suppl 3):S455-61
   Google Scholar
• Novoa I, Zeng H, Harding HP, Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 2001;153(5):1011-22
   PubMed Web of Science ®Google Scholar
• Kaufman RJ. Double-stranded RNA-activated protein kinase mediates virus-induced apoptosis: a new role for an old actor. Proc Natl Acad Sci USA 1999;96(21):11693-5
   PubMedGoogle Scholar
• Harding HP, Zhang Y, Scheuner D, et al. Ppp1r15 gene knockout reveals an essential role for translation initiation factor 2 alpha (eIF2alpha) dephosphorylation in mammalian development. Proc Natl Acad Sci USA 2009;106(6):1832-7
   PubMedGoogle Scholar
• Helenius A. How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticulum. Mol Biol Cell 1994;5(3):253-65
   PubMedGoogle Scholar
• Gething MJ, Sambrook J. Protein folding in the cell. Nature 1992;355(6355):33-45
   PubMed Web of Science ®Google Scholar
• Lindholm D, Wootz H, Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ 2006;13(3):385-92
   PubMed Web of Science ®Google Scholar
• Vij N, Fang S, Zeitlin PL. Selective inhibition of endoplasmic reticulum-associated degradation rescues DeltaF508-cystic fibrosis transmembrane regulator and suppresses interleukin-8 levels: therapeutic implications. J Biol Chem 2006;281(25):17369-78
   PubMed Web of Science ®Google Scholar
• Ozcan U, Cao Q, Yilmaz E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004;306(5695):457-61
   PubMed Web of Science ®Google Scholar
• Scheuner D, Kaufman RJ. The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes. Endocr Rev 2008;29(3):317-33
   PubMed Web of Science ®Google Scholar
• Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005;74:739-89
   PubMed Web of Science ®Google Scholar
• Harding HP, Zhang Y, Bertolotti A, et al. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000;5(5):897-904
   PubMed Web of Science ®Google Scholar
• Lee K, Tirasophon W, Shen X, et al. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 2002;16(4):452-66
   PubMed Web of Science ®Google Scholar
• Wu J, Rutkowski DT, Dubois M, et al. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 2007;13(3):351-64
   PubMed Web of Science ®Google Scholar
• Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 2011;13(3):184-90
   PubMed Web of Science ®Google Scholar
• Baker BM, Nargund AM, Sun T, Haynes CM. Protective coupling of mitochondrial function and protein synthesis via the eIF2alpha kinase GCN-2. PLoS Genet 2012;8(6):e1002760
   Google Scholar
• Rath E, Berger E, Messlik A, et al. Induction of dsRNA-activated protein kinase links mitochondrial unfolded protein response to the pathogenesis of intestinal inflammation. Gut 2012;61(9):1269-78
   PubMedGoogle Scholar
• Malhotra JD, Miao H, Zhang K, et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci USA 2008;105(47):18525-30
   PubMed Web of Science ®Google Scholar
• Cao SS, Kaufman RJ. Unfolded protein response. Curr Biol 2012;22(16):R622-6
   Web of Science ®Google Scholar
• Wang S, Kaufman RJ. The impact of the unfolded protein response on human disease. J Cell Biol 2012;197(7):857-67
   PubMed Web of Science ®Google Scholar
• Jackson RJ, Hellen CU, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 2010;11(2):113-27
   PubMed Web of Science ®Google Scholar
• Vattem KM, Wek RC. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci USA 2004;101(31):11269-74
   PubMed Web of Science ®Google Scholar
• Han J, Back SH, Hur J, et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol 2013;15(5):481-90
   PubMed Web of Science ®Google Scholar
• Lee YY, Cevallos RC, Jan E. An upstream open reading frame regulates translation of GADD34 during cellular stresses that induce eIF2alpha phosphorylation. J Biol Chem 2009;284(11):6661-73
   PubMedGoogle Scholar
• Palam LR, Baird TD, Wek RC. Phosphorylation of eIF2 facilitates ribosomal bypass of an inhibitory upstream ORF to enhance CHOP translation. J Biol Chem 2011;286(13):10939-49
   PubMed Web of Science ®Google Scholar
• Hsu LC, Park JM, Zhang K, et al. The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature 2004;428(6980):341-5
   PubMed Web of Science ®Google Scholar
• Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008;454(7203):455-62
   PubMed Web of Science ®Google Scholar
• Kaufman RJ. Orchestrating the unfolded protein response in health and disease. J Clin Invest 2002;110(10):1389-98
   PubMed Web of Science ®Google Scholar
• Fels DR, Koumenis C. The PERK/eIF2alpha/ATF4 module of the UPR in hypoxia resistance and tumor growth. Cancer Biol Ther 2006;5(7):723-8
   PubMed Web of Science ®Google Scholar
• Ye J, Kumanova M, Hart LS, et al. The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation. EMBO J 2010;29(12):2082-96
   PubMed Web of Science ®Google Scholar
• Oyadomari S, Harding HP, Zhang Y, et al. Dephosphorylation of translation initiation factor 2alpha enhances glucose tolerance and attenuates hepatosteatosis in mice. Cell Metab 2008;7(6):520-32
   PubMedGoogle Scholar
• Zhou L, Yang D, Wu DF, et al. Inhibition of endoplasmic reticulum stress and atherosclerosis by 2-aminopurine in apolipoprotein e-deficient mice. ISRN Pharmacol 2013;2013:847310
   PubMedGoogle Scholar
• Delepine M, Nicolino M, Barrett T, et al. EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat Genet 2000;25(4):406-9
   PubMed Web of Science ®Google Scholar
• Back SH, Scheuner D, Han J, et al. Translation attenuation through eIF2alpha phosphorylation prevents oxidative stress and maintains the differentiated state in beta cells. Cell Metab 2009;10(1):13-26
   PubMedGoogle Scholar
• Harding HP, Zeng H, Zhang Y, 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(6):1153-63
   PubMed Web of Science ®Google Scholar
• Zimmermann-Belsing T, Feldt-Rasmussen U. Obesity: the new worldwide epidemic threat to general health and our complete lack of effective treatment. Endocrinology 2004;145(4):1501-2
   PubMedGoogle Scholar
• Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 2008;29(1):42-61
   PubMed Web of Science ®Google Scholar
• Eizirik DL, Cnop M. ER stress in pancreatic beta cells: the thin red line between adaptation and failure. Sci Signal 2010;3(110):pe7
   PubMed Web of Science ®Google Scholar
• Back SH, Kaufman RJ. Endoplasmic reticulum stress and type 2 diabetes. Annu Rev Biochem 2012;81:767-93
   PubMed Web of Science ®Google Scholar
• Maedler K, Oberholzer J, Bucher P, et al. Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 2003;52(3):726-33
   PubMed Web of Science ®Google Scholar
• United Kingdom Prospective Diabetes Study (UKPDS). 13: relative efficacy of randomly allocated diet, sulphonylurea, insulin, or metformin in patients with newly diagnosed non-insulin dependent diabetes followed for three years. BMJ 1995;310(6972):83-8
   PubMed Web of Science ®Google Scholar
• Zimmet P. The burden of type 2 diabetes: are we doing enough? Diabetes Metab 2003;29(4 Pt 2):6S9-18
   PubMedGoogle Scholar
• Zhang W, Feng D, Li Y, et al. PERK EIF2AK3 control of pancreatic beta cell differentiation and proliferation is required for postnatal glucose homeostasis. Cell Metab 2006;4(6):491-7
   PubMed Web of Science ®Google Scholar
• Huang G, Yao J, Zeng W, et al. ER stress disrupts Ca2+-signaling complexes and Ca2+ regulation in secretory and muscle cells from PERK-knockout mice. J Cell Sci 2006;119(Pt 1):153-61
   PubMedGoogle Scholar
• Song B, Scheuner D, Ron D, et al. Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 2008;118(10):3378-89
   PubMed Web of Science ®Google Scholar
• Brush MH, Weiser DC, Shenolikar S. 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 2003;23(4):1292-303
   PubMed Web of Science ®Google Scholar
• Powers ET, Balch WE. Diversity in the origins of proteostasis networks--a driver for protein function in evolution. Nat Rev Mol Cell Biol 2013;14(4):237-48
   PubMedGoogle Scholar
• Cheng SH, Gregory RJ, Marshall J, et al. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 1990;63(4):827-34
   PubMed Web of Science ®Google Scholar
• Qu BH, Thomas PJ. Alteration of the cystic fibrosis transmembrane conductance regulator folding pathway. J Biol Chem 1996;271(13):7261-4
   PubMedGoogle Scholar
• Lukacs GL, Chang XB, Bear C, et al. The delta F508 mutation decreases the stability of cystic fibrosis transmembrane conductance regulator in the plasma membrane. Determination of functional half-lives on transfected cells. J Biol Chem 1993;268(29):21592-8
   PubMed Web of Science ®Google Scholar
• Maegawa GH, Tropak M, Buttner J, et al. Pyrimethamine as a potential pharmacological chaperone for late-onset forms of GM2 gangliosidosis. J Biol Chem 2007;282(12):9150-61
   PubMed Web of Science ®Google Scholar
• DiFiglia M, Sapp E, Chase KO, et al. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997;277(5334):1990-3
   PubMed Web of Science ®Google Scholar
• Wang J, Slunt H, Gonzales V, et al. Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature. Hum Mol Genet 2003;12(21):2753-64
   PubMed Web of Science ®Google Scholar
• Ozcan U, Ozcan L, Yilmaz E, et al. Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol Cell 2008;29(5):541-51
   PubMedGoogle Scholar
• Kars M, Yang L, Gregor MF, et al. Tauroursodeoxycholic Acid may improve liver and muscle but not adipose tissue insulin sensitivity in obese men and women. Diabetes 2010;59(8):1899-905
   PubMed Web of Science ®Google Scholar
• Xiao C, Giacca A, Lewis GF. Sodium phenylbutyrate, a drug with known capacity to reduce endoplasmic reticulum stress, partially alleviates lipid-induced insulin resistance and beta-cell dysfunction in humans. Diabetes 2011;60(3):918-24
   PubMed Web of Science ®Google Scholar
• Cao SS, Zimmermann EM, Chuang BM, et al. The unfolded protein response and chemical chaperones reduce protein misfolding and colitis in mice. Gastroenterology 2013;144(5):989-1000; e6
   PubMedGoogle Scholar
• Lawless MW, Greene CM, Mulgrew A, et al. Activation of endoplasmic reticulum-specific stress responses associated with the conformational disease Z alpha 1-antitrypsin deficiency. J Immunol 2004;172(9):5722-6
   PubMed Web of Science ®Google Scholar
• Hidvegi T, Ewing M, Hale P, et al. An autophagy-enhancing drug promotes degradation of mutant alpha1-antitrypsin Z and reduces hepatic fibrosis. Science 2010;329(5988):229-32
   PubMed Web of Science ®Google Scholar
• Shin Y, Klucken J, Patterson C, et al. The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways. J Biol Chem 2005;280(25):23727-34
   PubMed Web of Science ®Google Scholar
• Axten JM, Medina JR, Feng Y, et al. Discovery of 7-methyl-5-(1-{[3-(trifluoromethyl)phenyl]acetyl}-2,3-dihydro-1H-indol-5-yl)-7H-pyrrolo[2,3-d]pyrimidin-4-amine (GSK2606414), a potent and selective first-in-class inhibitor of protein kinase R (PKR)-like endoplasmic reticulum kinase (PERK). J Med Chem 2012;55(16):7193-207
   PubMed Web of Science ®Google Scholar
• Harding HP, Zyryanova AF, Ron D. Uncoupling proteostasis and development in vitro with a small molecule inhibitor of the pancreatic endoplasmic reticulum kinase, PERK. J Biol Chem 2012;287(53):44338-44
   PubMed Web of Science ®Google Scholar
• Atkins C, Liu Q, Minthorn E, et al. Characterization of a novel PERK kinase inhibitor with antitumor and antiangiogenic activity. Cancer Res 2013;73(6):1993-2002
   PubMed Web of Science ®Google Scholar
• Boyce M, Bryant KF, Jousse C, et al. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 2005;307(5711):935-9
   PubMed Web of Science ®Google Scholar
• Pennuto M, Tinelli E, Malaguti M, et al. Ablation of the UPR-mediator CHOP restores motor function and reduces demyelination in Charcot-Marie-Tooth 1B mice. Neuron 2008;57(3):393-405
   PubMed Web of Science ®Google Scholar
• D’Antonio M, Musner N, Scapin C, et al. Resetting translational homeostasis restores myelination in Charcot-Marie-Tooth disease type 1B mice. J Exp Med 2013;210(4):821-38
   PubMedGoogle Scholar
• Moreno JA, Radford H, Peretti D, et al. Sustained translational repression by eIF2alpha-P mediates prion neurodegeneration. Nature 2012;485(7399):507-11
   PubMed Web of Science ®Google Scholar
• Cnop M, Ladriere L, Hekerman P, et al. Selective inhibition of eukaryotic translation initiation factor 2 alpha dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic beta-cell dysfunction and apoptosis. J Biol Chem 2007;282(6):3989-97
   PubMed Web of Science ®Google Scholar
• Bonham AC, Trapani AJ, Portis LR, Brody MJ. Studies on the mechanism of the central antihypertensive effect of guanabenz and clonidine. J Hypertens Suppl 1984;2(3):S543-6
   Google Scholar
• Tsaytler P, Harding HP, Ron D, Bertolotti A. Selective inhibition of a regulatory subunit of protein phosphatase 1 restores proteostasis. Science 2011;332(6025):91-4
   PubMed Web of Science ®Google Scholar
• Sidrauski C, Acosta-Alvear D, Khoutorsky A, et al. Pharmacological brake-release of mRNA translation enhances cognitive memory. Elife 2013;2:e00498
   PubMed Web of Science ®Google Scholar
• Prisco GV, Huang W, Buffington SA, et al. A new mechanism of translational control of hippocampal mGluR-dependent long-term depression and object-place learning. Nature, in press
   Google Scholar
• Liu Y, Wang J, Qi SY, et al. Reduced endoplasmic reticulum stress might alter the course of heart failure Via caspase-12 and JNK pathways. Can J Cardiol 2014;30(3):368-75
   PubMed Web of Science ®Google Scholar
• Ma T, Trinh MA, Wexler AJ, et al. Suppression of eIF2alpha kinases alleviates Alzheimer’s disease-related plasticity and memory deficits. Nat Neurosci 2013;16(9):1299-305
   PubMed Web of Science ®Google Scholar
• Muaddi H, Majumder M, Peidis P, et al. Phosphorylation of eIF2alpha at serine 51 is an important determinant of cell survival and adaptation to glucose deficiency. Mol Biol Cell 2010;21(18):3220-31
   PubMedGoogle Scholar
• Ozasa R, Okada T, Nadanaka S, et al. The antipsychotic olanzapine induces apoptosis in insulin-secreting pancreatic beta cells by blocking PERK-mediated translational attenuation. Cell Struct Funct 2013;38(2):183-95
   PubMedGoogle Scholar