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Article title

Protein Disulfide Isomerase Superfamily in Disease and the Regulation of Apoptosis

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Abstracts

EN
Cellular homeostasis requires the balance of a multitude of signaling cascades that are contingent upon the essential proteins being properly synthesized, folded and delivered to appropriate subcellular locations. In eukaryotic cells the endoplasmic reticulum (ER) is a specialized organelle that is the central site of synthesis and folding of secretory, membrane and a number of organelletargeted proteins. The integrity of protein folding is enabled by the presence of ATP, Ca++, molecular chaperones, as well as an oxidizing redox environment. The imbalance between the load and capacity of protein folding results in a cellular condition known as ER stress. Failure of these pathways to restore ER homeostasis results in the activation of apoptotic pathways. Protein disulfide isomerases (PDI) compose a superfamily of oxidoreductases that have diverse sequences and are localized in the ER, nucleus, cytosol, mitochondria and cell membrane. The PDI superfamily has multiple functions including, acting as molecular chaperones, protein-binding partners, and hormone reservoirs. Recently , PDI family members have been implicated in the regulation of apoptotic signaling events. The complexities underlying the molecular mechanisms that define the switch from pro-survival to pro-death response are evidenced by recent studies that reveal the roles of specific chaperone proteins as integration points in signaling pathways that determine cell fate. The following review discusses the dual role of PDI in cell death and survival during ER stress.

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Year

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1

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1

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Dates

published
1 - 1 - 2014
received
2 - 2 - 2013
online
25 - 4 - 2013
accepted
27 - 2 - 2013

Contributors

author
  • Department of Cell and Molecular Pharmacology and Experimental Therapeutics
author
  • Drug Discovery and Biomedical Sciences, Medical University of South Carolina, Charleston, SC 29425

References

  • [1] Gaut JR, Hendershot LM. The modification and assembly of proteins in the endoplasmic reticulum. Curr Opin Cell Biol 1993; 5: 589-95.[Crossref]
  • [2] Ellgaard L, Helenius A. Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 2003; 4: 181-91.[Crossref]
  • [3] Meusser B, Hirsch C, Jarosch E, Sommer T. ERAD: the long road to destruction. Nat Cell Biol 2005; 7: 766-72.[Crossref]
  • [4] Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000; 404: 770-4.
  • [5] Wu J, Kaufman RJ. From acute ER stress to physiological roles of the Unfolded Protein Response. Cell Death Differ 2006; 13: 374-84.[Crossref]
  • [6] Verfaillie T, Garg AD, Agostinis P. Targeting ER stress induced apoptosis and inflammation in cancer. Cancer Lett 2010.
  • [7] Wang SB, Shi Q, Xu Y, Xie WL, Zhang J, Tian C, et al. Protein disulfide isomerase regulates endoplasmic reticulum stress and the apoptotic process during prion infection and PrP mutant-induced cytotoxicity. PLoS One 2012; 7: e38221.[Crossref]
  • [8] Townsend DM, Manevich Y, He L, Xiong Y, Bowers RR, Jr., Hutchens S, et al. Nitrosative stress-induced s-glutathionylation of protein disulfide isomerase leads to activation of the unfolded protein response. Cancer Res 2009; 69: 7626-34.[Crossref]
  • [9] Hoffstrom BG, Kaplan A, Letso R, Schmid RS, Turmel GJ, Lo DC, et al. Inhibitors of protein disulfide isomerase suppress apoptosis induced by misfolded proteins. Nat Chem Biol 2010; 6: 900-6.[Crossref]
  • [10] Anathy V, Roberson E, Cunniff B, Nolin JD, Hoffman S, Spiess P, et al. Oxidative processing of latent Fas in the endoplasmic reticulum controls the strength of apoptosis. Mol Cell Biol 2012; 32: 3464-78.[Crossref]
  • [11] Guerin R, Arseneault G, Dumont S, Rokeach LA. Calnexin is involved in apoptosis induced by endoplasmic reticulum stress in the fission yeast. Mol Biol Cell 2008; 19: 4404-20.[Crossref]
  • [12] Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J Biol Chem 2003; 278: 20915-24.
  • [13] Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 2003; 11: 619-33.[Crossref]
  • [14] Cullinan SB, Diehl JA. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol 2006; 38: 317-32.[Crossref]
  • [15] Liu Y, Adachi M, Zhao S, Hareyama M, Koong AC, Luo D, et al. Preventing oxidative stress: a new role for XBP1. Cell Death Differ 2009; 16: 847-57.[Crossref]
  • [16] Yan W, Frank CL, Korth MJ, Sopher BL, Novoa I, Ron D, et al. Control of PERK eIF2alpha kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc Natl Acad Sci U S A 2002; 99: 15920-5.[Crossref]
  • [17] Iwawaki T, Hosoda A, Okuda T, Kamigori Y, Nomura- Furuwatari C, Kimata Y, et al. Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat Cell Biol 2001; 3: 158-64.
  • [18] Hetz C, Bernasconi P, Fisher J, Lee AH, Bassik MC, Antonsson B, et al. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 2006; 312: 572-6.
  • [19] Nadanaka S, Okada T, Yoshida H, Mori K. Role of disulfide bridges formed in the luminal domain of ATF6 in sensing endoplasmic reticulum stress. Mol Cell Biol 2007; 27: 1027-43.[Crossref]
  • [20] Bommiasamy H, Back SH, Fagone P, Lee K, Meshinchi S, Vink E, et al. ATF6alpha induces XBP1-independent expansion of the endoplasmic reticulum. J Cell Sci 2009; 122: 1626-36.
  • [21] Wang Y, Shen J, Arenzana N, Tirasophon W, Kaufman RJ, Prywes R. Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J Biol Chem 2000; 275: 27013-20.
  • [22] Rutkowski DT, Arnold SM, Miller CN, Wu J, Li J, Gunnison KM, et al. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol 2006; 4: e374.[Crossref]
  • [23] Morishima N, Nakanishi K, Nakano A. Activating transcription factor-6 (ATF6) mediates apoptosis with reduction of myeloid cell leukemia sequence 1 (Mcl-1) protein via induction of WW domain binding protein 1. J Biol Chem 2011; 286: 35227-35.
  • [24] 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: 1345-55.[Crossref]
  • [25] Hatai T, Matsuzawa A, Inoshita S, Mochida Y, Kuroda T, Sakamaki K, et al. Execution of apoptosis signal-regulating kinase 1 (ASK1)- induced apoptosis by the mitochondria-dependent caspase activation. J Biol Chem 2000; 275: 26576-81.
  • [26] Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 2000; 103: 239-52.[Crossref]
  • [27] Oono K, Yoneda T, Manabe T, Yamagishi S, Matsuda S, Hitomi J, et al. JAB1 participates in unfolded protein responses by association and dissociation with IRE1. Neurochem Int 2004; 45: 765-72.[Crossref]
  • [28] Li J, Lee B, Lee AS. Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-upregulated modulator of apoptosis (PUMA) and NOXA by p53. J Biol Chem 2006; 281: 7260-70.
  • [29] Gorman AM, Healy SJ, Jager R, Samali A. Stress management at the ER: regulators of ER stress-induced apoptosis. Pharmacol Ther 2012; 134: 306-16.[Crossref]
  • [30] Gorlach A, Klappa P, Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal 2006; 8: 1391-418.
  • [31] Benham AM. The protein disulfide isomerase family: key players in health and disease. Antioxid Redox Signal 2012; 16: 781-9.
  • [32] Imaoka S. Chemical stress on protein disulfide isomerases and inhibition of their functions. Int Rev Cell Mol Biol 2011; 290: 121-66.
  • [33] Zhou M, Jacob A, Ho N, Miksa M, Wu R, Maitra SR, et al. Downregulation of protein disulfide isomerase in sepsis and its role in tumor necrosis factor-alpha release. Crit Care 2008; 12: R100.[Crossref]
  • [34] Rigobello MP, Donella-Deana A, Cesaro L, Bindoli A. Distribution of protein disulphide isomerase in rat liver mitochondria. Biochem J 2001; 356: 567-70.
  • [35] Turano C, Coppari S, Altieri F, Ferraro A. Proteins of the PDI family: unpredicted non-ER locations and functions. J Cell Physiol 2002; 193: 154-63.[Crossref]
  • [36] Popescu NI, Lupu C, Lupu F. Extracellular protein disulfide isomerase regulates coagulation on endothelial cells through modulation of phosphatidylserine exposure. Blood 2010; 116: 993-1001.[Crossref]
  • [37] Bi S, Hong PW, Lee B, Baum LG. Galectin-9 binding to cell surface protein disulfide isomerase regulates the redox environment to enhance T-cell migration and HIV entry. Proc Natl Acad Sci U S A 2011; 108: 10650-5.[Crossref]
  • [38] Gonzalez-Gronow M, Selim MA, Papalas J, Pizzo SV. GRP78: a multifunctional receptor on the cell surface. Antioxid Redox Signal 2009; 11: 2299-306.
  • [39] Zhang Y, Liu R, Ni M, Gill P, Lee AS. Cell surface relocalization of the endoplasmic reticulum chaperone and unfolded protein response regulator GRP78/BiP. J Biol Chem 2010; 285: 15065-75.
  • [40] Tabata Y, Takano K, Ito T, Iinuma M, Yoshimoto T, Miura H, et al. Vaticanol B, a resveratrol tetramer, regulates endoplasmic reticulum stress and inflammation. Am J Physiol Cell Physiol 2007; 293: C411-8.
  • [41] Tu BP, Ho-Schleyer SC, Travers KJ, Weissman JS. Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 2000; 290: 1571-4.
  • [42] Frand AR, Kaiser CA. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1998; 1: 161-70.[Crossref]
  • [43] Cai H, Wang CC, Tsou CL. Chaperone-like activity of protein disulfide isomerase in the refolding of a protein with no disulfide bonds. J Biol Chem 1994; 269: 24550-2.
  • [44] Delic M, Rebnegger C, Wanka F, Puxbaum V, Haberhauer- Troyer C, Hann S, et al. Oxidative protein folding and unfolded protein response elicit differing redox regulation in endoplasmic reticulum and cytosol of yeast. Free Radic Biol Med 2012; 52: 2000-12.
  • [45] Merksamer PI, Trusina A, Papa FR. Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions. Cell 2008; 135: 933-47.[Crossref]
  • [46] Tsai B, Rodighiero C, Lencer WI, Rapoport TA. Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 2001; 104: 937-48.[Crossref]
  • [47] Moore P, Bernardi KM, Tsai B. The Ero1alpha-PDI redox cycle regulates retro-translocation of cholera toxin. Mol Biol Cell 2010; 21: 1305-13.
  • [48] Gillece P, Luz JM, Lennarz WJ, de La Cruz FJ, Romisch K. Export of a cysteine-free misfolded secretory protein from the endoplasmic reticulum for degradation requires interaction with protein disulfide isomerase. J Cell Biol 1999; 147: 1443-56.
  • [49] Nardai G, Stadler K, Papp E, Korcsmaros T, Jakus J, Csermely P. Diabetic changes in the redox status of the microsomal protein folding machinery. Biochem Biophys Res Commun 2005; 334: 787-95.
  • [50] Uys JD, Xiong Y, Townsend DM. Nitrosative stress-induced S-glutathionylation of protein disulfide isomerase. Methods Enzymol 2011; 490: 321-32.
  • [51] Townsend DM. S-glutathionylation: indicator of cell stress and regulator of the unfolded protein response. Mol Interv 2007; 7: 313-24.[Crossref]
  • [52] Xiong Y, Uys JD, Tew KD, Townsend DM. S-glutathionylation: from molecular mechanisms to health outcomes. Antioxid Redox Signal 2011; 15: 233-70.
  • [53] Uehara T, Nakamura T, Yao D, Shi ZQ, Gu Z, Ma Y, et al. S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 2006; 441: 513-7.
  • [54] Xiong Y, Manevich Y, Tew KD, Townsend DM. S-Glutathionylation of Protein Disulfide Isomerase Regulates Estrogen Receptor alpha Stability and Function. Int J Cell Biol 2012; 2012: 273549.
  • [55] Townsend DM, Findlay VJ, Fazilev F, Ogle M, Fraser J, Saavedra JE, et al. A glutathione S-transferase pi-activated prodrug causes kinase activation concurrent with S-glutathionylation of proteins. Mol Pharmacol 2006; 69: 501-8.
  • [56] Yoshida H. ER stress and diseases. FEBS J 2007; 274: 630-58.
  • [57] Forman MS, Lee VM, Trojanowski JQ. ‘Unfolding’ pathways in neurodegenerative disease. Trends Neurosci 2003; 26: 407-10.[Crossref]
  • [58] Torres M, Castillo K, Armisen R, Stutzin A, Soto C, Hetz C. Prion protein misfolding affects calcium homeostasis and sensitizes cells to endoplasmic reticulum stress. PLoS One 2010; 5: e15658.[Crossref]
  • [59] Yankner BA, Duffy LK, Kirschner DA. Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. Science 1990; 250: 279-82.
  • [60] Xu J, Kao SY, Lee FJ, Song W, Jin LW, Yankner BA. Dopamine-dependent neurotoxicity of alpha-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. Nat Med 2002; 8: 600-6.[Crossref]
  • [61] Cheng H, Wang L, Wang CC. Domain a’ of protein disulfide isomerase plays key role in inhibiting alpha-synuclein fibril formation. Cell Stress Chaperones 2010; 15: 415-21.[Crossref]
  • [62] Atkin JD, Farg MA, Walker AK, McLean C, Tomas D, Horne MK. Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol Dis 2008; 30: 400-7.[Crossref]
  • [63] Shashidharan P, Sandu D, Potla U, Armata IA, Walker RH, McNaught KS, et al. Transgenic mouse model of early-onset DYT1 dystonia. Hum Mol Genet 2005; 14: 125-33.
  • [64] Honjo Y, Ito H, Horibe T, Takahashi R, Kawakami K. Protein disulfide isomerase-immunopositive inclusions in patients with Alzheimer disease. Brain Res 2010; 1349: 90-6.
  • [65] Conn KJ, Gao W, McKee A, Lan MS, Ullman MD, Eisenhauer PB, et al. Identification of the protein disulfide isomerase family member PDIp in experimental Parkinson’s disease and Lewy body pathology. Brain Res 2004; 1022: 164-72.
  • [66] Tanaka S, Uehara T, Nomura Y. Up-regulation of proteindisulfide isomerase in response to hypoxia/brain ischemia and its protective effect against apoptotic cell death. J Biol Chem 2000; 275: 10388-93.
  • [67] Hetz C, Russelakis-Carneiro M, Walchli S, Carboni S, Vial- Knecht E, Maundrell K, et al. The disulfide isomerase Grp58 is a protective factor against prion neurotoxicity. J Neurosci 2005; 25: 2793-802.[Crossref]
  • [68] Walker AK, Farg MA, Bye CR, McLean CA, Horne MK, Atkin JD. Protein disulphide isomerase protects against protein aggregation and is S-nitrosylated in amyotrophic lateral sclerosis. Brain 2010; 133: 105-16.[Crossref]
  • [69] Papp E, Szaraz P, Korcsmaros T, Csermely P. Changes of endoplasmic reticulum chaperone complexes, redox state, and impaired protein disulfide reductase activity in misfolding alpha1-antitrypsin transgenic mice. FASEB J 2006; 20: 1018-20.[Crossref]
  • [70] Yang YS, Harel NY, Strittmatter SM. Reticulon-4A (Nogo-A) redistributes protein disulfide isomerase to protect mice from SOD1-dependent amyotrophic lateral sclerosis. J Neurosci 2009; 29: 13850-9.[Crossref]
  • [71] Ko HS, Uehara T, Nomura Y. Role of ubiquilin associated with protein-disulfide isomerase in the endoplasmic reticulum in stress-induced apoptotic cell death. J Biol Chem 2002; 277: 35386-92.
  • [72] Zhang P, McGrath B, Li S, Frank A, Zambito F, Reinert J, et al. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol Cell Biol 2002; 22: 3864-74.[Crossref]
  • [73] Scheuner D, Vander Mierde D, Song B, Flamez D, Creemers JW, Tsukamoto K, et al. Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis. Nat Med 2005; 11: 757-64.[Crossref]
  • [74] Oyadomari S, Koizumi A, Takeda K, Gotoh T, Akira S, Araki E, et al. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 2002; 109: 525-32.[Crossref]
  • [75] Ladiges WC, Knoblaugh SE, Morton JF, Korth MJ, Sopher BL, Baskin CR, et al. Pancreatic beta-cell failure and diabetes in mice with a deletion mutation of the endoplasmic reticulum molecular chaperone gene P58IPK. Diabetes 2005; 54: 1074-81.[Crossref]
  • [76] Nakatani Y, Kaneto H, Kawamori D, Yoshiuchi K, Hatazaki M, Matsuoka TA, et al. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J Biol Chem 2005; 280: 847-51.[Crossref]
  • [77] Zhang L, Lai E, Teodoro T, Volchuk A. GRP78, but Not Proteindisulfide Isomerase, Partially Reverses Hyperglycemiainduced Inhibition of Insulin Synthesis and Secretion in Pancreatic {beta}-Cells. J Biol Chem 2009; 284: 5289-98.
  • [78] Tabas I. The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ Res 2010; 107: 839-50.[Crossref]
  • [79] Zhou J, Werstuck GH, Lhotak S, de Koning AB, Sood SK, Hossain GS, et al. Association of multiple cellular stress pathways with accelerated atherosclerosis in hyperhomocysteinemic apolipoprotein E-deficient mice. Circulation 2004; 110: 207-13. [Crossref]
  • [80] Devries-Seimon T, Li Y, Yao PM, Stone E, Wang Y, Davis RJ, et al. Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor. J Cell Biol 2005; 171: 61-73.[Crossref]
  • [81] Sanson M, Auge N, Vindis C, Muller C, Bando Y, Thiers JC, et al. Oxidized low-density lipoproteins trigger endoplasmic reticulum stress in vascular cells: prevention by oxygenregulated protein 150 expression. Circ Res 2009; 104: 328-36.
  • [82] Thorp E, Li G, Seimon TA, Kuriakose G, Ron D, Tabas I. Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe-/- and Ldlr-/- mice lacking CHOP. Cell Metab 2009; 9: 474-81.[Crossref]
  • [83] Muller C, Bandemer J, Vindis C, Camare C, Mucher E, Gueraud F, et al. Protein Disulfide Isomerase Modification and Inhibition potentiates ER stress and apoptosis induced by oxidized low density lipoproteins. Antioxid Redox Signal 2012.
  • [84] Tian F, Zhou X, Wikstrom J, Karlsson H, Sjoland H, Gan LM, et al. Protein disulfide isomerase increases in myocardial endothelial cells in mice exposed to chronic hypoxia: a stimulatory role in angiogenesis. Am J Physiol Heart Circ Physiol 2009; 297: H1078-86.
  • [85] Severino A, Campioni M, Straino S, Salloum FN, Schmidt N, Herbrand U, et al. Identification of protein disulfide isomerase as a cardiomyocyte survival factor in ischemic cardiomyopathy. J Am Coll Cardiol 2007; 50: 1029-37.[Crossref]
  • [86] Swiatkowska M, Szymanski J, Padula G, Cierniewski CS. Interaction and functional association of protein disulfide isomerase with alphaVbeta3 integrin on endothelial cells. FEBS J 2008; 275: 1813-23.
  • [87] Toldo S, Boccellino M, Rinaldi B, Seropian IM, Mezzaroma E, Severino A, et al. Altered oxido-reductive state in the diabetic heart: loss of cardioprotection due to protein disulfide isomerase. Mol Med 2011; 17: 1012-21.
  • [88] Xu D, Perez RE, Rezaiekhaligh MH, Bourdi M, Truog WE. Knockdown of ERp57 increases BiP/GRP78 induction and protects against hyperoxia and tunicamycin-induced apoptosis. Am J Physiol Lung Cell Mol Physiol 2009; 297: L44-51.
  • [89] Lee E, Nichols P, Spicer D, Groshen S, Yu MC, Lee AS. GRP78 as a novel predictor of responsiveness to chemotherapy in breast cancer. Cancer Res 2006; 66: 7849-53.[Crossref]
  • [90] Zheng HC, Takahashi H, Li XH, Hara T, Masuda S, Guan YF, et al. Overexpression of GRP78 and GRP94 are markers for aggressive behavior and poor prognosis in gastric carcinomas. Hum Pathol 2008; 39: 1042-9.[Crossref]
  • [91] Ozawa K, Tsukamoto Y, Hori O, Kitao Y, Yanagi H, Stern DM, et al. Regulation of tumor angiogenesis by oxygen-regulated protein 150, an inducible endoplasmic reticulum chaperone. Cancer Res 2001; 61: 4206-13.
  • [92] Lovat PE, Corazzari M, Armstrong JL, Martin S, Pagliarini V, Hill D, et al. Increasing melanoma cell death using inhibitors of protein disulfide isomerases to abrogate survival responses to endoplasmic reticulum stress. Cancer Res 2008; 68: 5363-9. [Crossref]
  • [93] Haefliger S, Klebig C, Schaubitzer K, Schardt J, Timchenko N, Mueller BU, et al. Protein disulfide isomerase blocks CEBPA translation and is up-regulated during the unfolded protein response in AML. Blood 2011; 117: 5931-40.[Crossref]
  • [94] Xu S, Butkevich AN, Yamada R, Zhou Y, Debnath B, Duncan R, et al. Discovery of an orally active small-molecule irreversible inhibitor of protein disulfide isomerase for ovarian cancer treatment. Proc Natl Acad Sci U S A 2012; 109: 16348-53.[Crossref]
  • [95] Welsh JB, Sapinoso LM, Su AI, Kern SG, Wang-Rodriguez J, Moskaluk CA, et al. Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Res 2001; 61: 5974-8.
  • [96] Beer DG, Kardia SL, Huang CC, Giordano TJ, Levin AM, Misek DE, et al. Gene-expression profiles predict survival of patients with lung adenocarcinoma. Nat Med 2002; 8: 816-24.
  • [97] Goplen D, Wang J, Enger PO, Tysnes BB, Terzis AJ, Laerum OD, et al. Protein disulfide isomerase expression is related to the invasive properties of malignant glioma. Cancer Res 2006; 66: 9895-902.[Crossref]
  • [98] Kurtoglu M, Philips K, Liu H, Boise LH, Lampidis TJ. High endoplasmic reticulum activity renders multiple myeloma cells hypersensitive to mitochondrial inhibitors. Cancer Chemother Pharmacol 2010; 66: 129-40.[Crossref]
  • [99] Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, Murphy-Ullrich JE, et al. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 2005; 123: 321-34.[Crossref]
  • [100] Obeid M, Panaretakis T, Joza N, Tufi R, Tesniere A, van Endert P, et al. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ 2007; 14: 1848-50.[Crossref]
  • [101] Burikhanov R, Zhao Y, Goswami A, Qiu S, Schwarze SR, Rangnekar VM. The tumor suppressor Par-4 activates an extrinsic pathway for apoptosis. Cell 2009; 138: 377-88.[Crossref]
  • [102] Wang X, Olberding KE, White C, Li C. Bcl-2 proteins regulate ER membrane permeability to luminal proteins during ER stress-induced apoptosis. Cell Death Differ 2011; 18: 38-47.[Crossref]
  • [103] Na KS, Park BC, Jang M, Cho S, Lee do H, Kang S, et al. Protein disulfide isomerase is cleaved by caspase-3 and -7 during apoptosis. Mol Cells 2007; 24: 261-7.
  • [104] Sliskovic I, Mutus B. Reversible inhibition of caspase-3 activity by iron(III): potential role in physiological control of apoptosis. FEBS Lett 2006; 580: 2233-7.
  • [105] Fenouillet E, Barbouche R, Courageot J, Miquelis R. The catalytic activity of protein disulfide isomerase is involved in human immunodeficiency virus envelope-mediated membrane fusion after CD4 cell binding. J Infect Dis 2001; 183: 744-52.
  • [106] Jain S, McGinnes LW, Morrison TG. Thiol/disulfide exchange is required for membrane fusion directed by the Newcastle disease virus fusion protein. J Virol 2007; 81: 2328-39.[Crossref]
  • [107] Townsend DM, He L, Hutchens S, Garrett TE, Pazoles CJ, Tew KD. NOV-002, a glutathione disulfide mimetic, as a modulator of cellular redox balance. Cancer Res 2008; 68: 2870-7.[Crossref]
  • [108] Hashida T, Kotake Y, Ohta S. Protein disulfide isomerase knockdown-induced cell death is cell-line-dependent and involves apoptosis in MCF-7 cells. J Toxicol Sci 2011; 36: 1-7.[Crossref]
  • [109] Kraus M, Malenke E, Gogel J, Muller H, Ruckrich T, Overkleeft H, et al. Ritonavir induces endoplasmic reticulum stress and sensitizes sarcoma cells toward bortezomib-induced apoptosis. Mol Cancer Ther 2008; 7: 1940-8.[Crossref]
  • [110] Findlay VJ, Townsend DM, Saavedra JE, Buzard GS, Citro ML, Keefer LK, et al. Tumor cell responses to a novel glutathione S-transferase-activated nitric oxide-releasing prodrug. Mol Pharmacol 2004; 65: 1070-9.[Crossref]
  • [111] Kiziltepe T, Hideshima T, Ishitsuka K, Ocio EM, Raje N, Catley L, et al. JS-K, a GST-activated nitric oxide generator, induces DNA double-strand breaks, activates DNA damage response pathways, and induces apoptosis in vitro and in vivo in human multiple myeloma cells. Blood 2007; 110: 709-18.[Crossref]
  • [112] Hutchens S, Manevich Y, He L, Tew KD, Townsend DM. Cellular resistance to a nitric oxide releasing glutathione S-transferase P-activated prodrug, PABA/NO. Invest New Drugs 2011; 29: 719-29.[Crossref]
  • [113] Ma Y, Hendershot LM. The role of the unfolded protein response in tumour development: friend or foe? Nat Rev Cancer 2004; 4: 966-77.[Crossref]
  • [114] Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, Hu N, et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J 2005; 24: 3470-81.[Crossref]
  • [115] Herr I, Debatin KM. Cellular stress response and apoptosis in cancer therapy. Blood 2001; 98: 2603-14.[Crossref]
  • [116] Sato N, Urano F, Yoon Leem J, Kim SH, Li M, Donoviel D, et al. Upregulation of BiP and CHOP by the unfolded-protein response is independent of presenilin expression. Nat Cell Biol 2000; 2: 863-70.
  • [117] Terro F, Czech C, Esclaire F, Elyaman W, Yardin C, Baclet MC, et al. Neurons overexpressing mutant presenilin-1 are more sensitive to apoptosis induced by endoplasmic reticulum- Golgi stress. J Neurosci Res 2002; 69: 530-9.[Crossref]
  • [118] Lindholm D, Wootz H, Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ 2006; 13: 385-92.[Crossref]
  • [119] Imai Y, Soda M, Takahashi R. Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitinprotein ligase activity. J Biol Chem 2000; 275: 35661-4.
  • [120] Ryu EJ, Harding HP, Angelastro JM, Vitolo OV, Ron D, Greene LA. Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson’s disease. J Neurosci 2002; 22: 10690-8.
  • [121] Vidal R, Caballero B, Couve A, Hetz C. Converging pathways in the occurrence of endoplasmic reticulum (ER) stress in Huntington’s disease. Curr Mol Med 2011; 11: 1-12.[Crossref]
  • [122] Matus S, Glimcher LH, Hetz C. Protein folding stress in neurodegenerative diseases: a glimpse into the ER. Curr Opin Cell Biol 2011; 23: 239-52. [Crossref]
  • [123] Nishitoh H, Kadowaki H, Nagai A, Maruyama T, Yokota T, Fukutomi H, et al. ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev 2008; 22: 1451-64.[Crossref]
  • [124] Hetz C, Russelakis-Carneiro M, Maundrell K, Castilla J, Soto C. Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J 2003; 22: 5435-45.[Crossref]
  • [125] DeGracia DJ, Montie HL. Cerebral ischemia and the unfolded protein response. J Neurochem 2004; 91: 1-8.[Crossref]
  • [126] He B. Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 2006; 13: 393-403.[Crossref]
  • [127] 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: 171-5.[Crossref]
  • [128] Shao L, Sun X, Xu L, Young LT, Wang JF. Mood stabilizing drug lithium increases expression of endoplasmic reticulum stress proteins in primary cultured rat cerebral cortical cells. Life Sci 2006; 78: 1317-23.[Crossref]
  • [129] Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004; 306: 457-61.
  • [130] Harding HP, 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: 1153-63.[Crossref]
  • [131] Jeffrey KD, Alejandro EU, Luciani DS, Kalynyak TB, Hu X, Li H, et al. Carboxypeptidase E mediates palmitate-induced beta-cell ER stress and apoptosis. Proc Natl Acad Sci U S A 2008; 105: 8452-7.[Crossref]
  • [132] Zhang K, Shen X, Wu J, Sakaki K, Saunders T, Rutkowski DT, et al. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 2006; 124: 587-99.[Crossref]
  • [133] Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008; 454: 455-62.[Crossref]
  • [134] Vasa-Nicotera M. The new kid on the block: the unfolded protein response in the pathogenesis of atherosclerosis. Cell Death Differ 2004; 11 Suppl 1: S10-1.
  • [135] Zhang C, Kawauchi J, Adachi MT, Hashimoto Y, Oshiro S, Aso T, et al. Activation of JNK and transcriptional repressor ATF3/LRF1 through the IRE1/TRAF2 pathway is implicated in human vascular endothelial cell death by homocysteine. Biochem Biophys Res Commun 2001; 289: 718-24.
  • [136] Zhou J, Lhotak S, Hilditch BA, Austin RC. Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 2005; 111: 1814-21.[Crossref]
  • [137] Todd DJ, Lee AH, Glimcher LH. The endoplasmic reticulum stress response in immunity and autoimmunity. Nat Rev Immunol 2008; 8: 663-74.[Crossref]
  • [138] Corrigall VM, Bodman-Smith MD, Fife MS, Canas B, Myers LK, Wooley P, et al. The human endoplasmic reticulum molecular chaperone BiP is an autoantigen for rheumatoid arthritis and prevents the induction of experimental arthritis. J Immunol 2001; 166: 1492-8.
  • [139] Thuerauf DJ, Marcinko M, Gude N, Rubio M, Sussman MA, Glembotski CC. Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ Res 2006; 99: 275-82.[Crossref]
  • [140] Shintani-Ishida K, Nakajima M, Uemura K, Yoshida K. Ischemic preconditioning protects cardiomyocytes against ischemic injury by inducing GRP78. Biochem Biophys Res Commun 2006; 345: 1600-5.
  • [141] Glembotski CC. The role of the unfolded protein response in the heart. J Mol Cell Cardiol 2008; 44: 453-9.[Crossref]
  • [142] Lawless MW, Greene CM, Mulgrew A, Taggart CC, O’Neill SJ, McElvaney NG. Activation of endoplasmic reticulumspecific stress responses associated with the conformational disease Z alpha 1-antitrypsin deficiency. J Immunol 2004; 172: 5722-6.

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bwmeta1.element.-psjd-doi-10_2478_ersc-2013-0001
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