The Unfolded Protein Response in Homeostasis and Modulation of Mammalian Immune Cells

REFERENCES

• Braakman I, Bulleid NJ. Protein folding and modification in the Mammalian endoplasmic reticulum. Annu Rev Biochem. 2011;80:71–99.
   PubMed Web of Science ®Google Scholar
• Schröder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem. 2005;74:739–789.
   PubMed Web of Science ®Google Scholar
• Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13:89–102.
   PubMed Web of Science ®Google Scholar
• Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334:1081–1086.
   PubMed Web of Science ®Google Scholar
• Wang S, Kaufman RJ. The impact of the unfolded protein response on human disease. J Cell Biol. 2012;197:857–867.
   PubMed Web of Science ®Google Scholar
• Hetz C, Chevet E, Harding HP. Targeting the unfolded protein response in disease. Nat Rev Drug Discov. 2013;12:703–19.
   PubMed Web of Science ®Google Scholar
• Rutkowski DT, Hegde RS. Regulation of basal cellular physiology by the homeostatic unfolded protein response. J Cell Biol. 2010;189:783–794.
   PubMed Web of Science ®Google Scholar
• Janssens S, Pulendran B, Lambrecht BN. Emerging functions of the unfolded protein response in immunity. Nat Immunol. 2014;15:910–919.
   PubMed Web of Science ®Google Scholar
• Cox JS, Walter P. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell. 1996;87:391–404.
   PubMed Web of Science ®Google Scholar
• Patil C, Walter P. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol. 2001;13:349–355.
   PubMed Web of Science ®Google Scholar
• Kimata Y, Kohno K. Endoplasmic reticulum stress-sensing mechanisms in yeast and mammalian cells. Curr Opin Cell Biol. 2011;23:135–142.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol. 2000;2:326–332.
   PubMed Web of Science ®Google Scholar
• Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007;8:519–529.
   PubMed Web of Science ®Google Scholar
• Tirasophon W, Lee K, Callaghan B, Welihinda A, Kaufman RJ. The endoribonuclease activity of mammalian IRE1 autoregulates its mRNA and is required for the unfolded protein response. Genes Dev. 2000;14:2725–2736.
   PubMed Web of Science ®Google Scholar
• Wang XZ, Harding HP, Zhang Y, Jolicoeur EM, Kuroda M, Ron D. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J. 1998;17:5708–5717.
   PubMed Web of Science ®Google Scholar
• Reimold AM, Etkin A, Clauss I, An essential role in liver development for transcription factor XBP-1. Genes Dev. 2000;14:152–157.
   PubMed Web of Science ®Google Scholar
• Martino MB, Jones L, Brighton B, The ER stress transducer IRE1β is required for airway epithelial mucin production. Mucosal Immunol. 2012;00:1–16.
   Google Scholar
• Tsuru A, Fujimoto N, Takahashi S, Negative feedback by IRE1β optimizes mucin production in goblet cells. Proc Natl Acad Sci U S A. 2013;110:2864–2869.
   PubMed Web of Science ®Google Scholar
• Shamu CE, Walter P. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J. 1996;15:3028–3039.
   PubMed Web of Science ®Google Scholar
• Calfon M, Zeng H, Urano F, IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature. 2002;415:92–96.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Shoulders MD, Ryno LM, Genereux JC, Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep. 2013;3:1279–1292.
   PubMed Web of Science ®Google Scholar
• Sriburi R, Jackowski S, Mori K, Brewer JW. XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J Cell Biol. 2004;167:35–41.
   PubMed Web of Science ®Google Scholar
• Lee A-H, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol. 2003;23:7448–7459.
   PubMed Web of Science ®Google Scholar
• Hollien J, Weissman JS. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science. 2006;313:104–107.
   PubMed Web of Science ®Google Scholar
• Oikawa D, Tokuda M, Hosoda A, Iwawaki T. Identification of a consensus element recognized and cleaved by IRE1α. Nucleic Acids Res. 2010;38:6265–6273.
   PubMed Web of Science ®Google Scholar
• Coelho DS, Domingos PM. Physiological roles of regulated Ire1 dependent decay. Front Genet. 2014;5:1–6.
   PubMedGoogle Scholar
• Upton J-P, Wang L, Han D, IRE1α cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science. 2012;(80-):818–822.
   PubMed Web of Science ®Google Scholar
• Urano F, Wang X, Bertolotti a, Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. 2000;287:664–666.
   PubMed Web of Science ®Google Scholar
• Kaneko M, Niinuma Y, Nomura Y. Activation signal of nuclear factor-kappa B in response to endoplasmic reticulum stress is transduced via IRE1 and tumor necrosis factor receptor-associated factor 2. Biol Pharm Bull. 2003;26:931–935.
   PubMed Web of Science ®Google Scholar
• Gardner BM, Walter P. Unfolded proteins are ire1-activating ligands that directly induce the unfolded protein response. Science. 2011;333(80-):1891–1894.
   PubMed Web of Science ®Google Scholar
• Wiseman RL, Zhang Y, Lee KPK, Flavonol activation defines an unanticipated ligand-binding site in the kinase-RNase domain of IRE1. Mol Cell. 2010;38:291–304.
   PubMed Web of Science ®Google Scholar
• Volmer R, van der Ploeg K, Ron D. Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc Natl Acad Sci U S A. 2013;110:4628–4633.
   PubMed Web of Science ®Google Scholar
• Shi Y, Vattem KM, Sood R, Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol. 1998;18:7499–7509.
   PubMed Web of Science ®Google Scholar
• Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature. 1999;397:271–274.
   PubMed Web of Science ®Google Scholar
• Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell. 2000;5:897–904.
   PubMed Web of Science ®Google Scholar
• Harding HP, Zhang Y, Zeng H, An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell. 2003;11:619–633.
   PubMed Web of Science ®Google Scholar
• Yang X, Matsuda K, Bialek P, ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology: Implication for Coffin–Lowry syndrome. Cell. 2004;117:387–398.
   PubMed Web of Science ®Google Scholar
• Roybal CN, Yang S, Sun C-W, Homocysteine increases the expression of vascular endothelial growth factor by a mechanism involving endoplasmic reticulum stress and transcription factor ATF4. J Biol Chem. 2004;279:14844–14852.
   PubMed Web of Science ®Google Scholar
• B’Chir W, Maurin AC, Carraro V, The eIF2α/ATF4 pathway is essential for stress-induced autophagy gene expression. Nucleic Acids Res. 2013;41(16):7683–7699.
   PubMed Web of Science ®Google Scholar
• Jiang H, Wek S a, Mcgrath BC, Phosphorylation of the α subunit of eukaryotic initiation factor 2 is required for activation of NF-κB in response to diverse cellular stresses. Mol Cell Biol. 2003;23:5651–5663.
   PubMed Web of Science ®Google Scholar
• Deng J, Lu P, Zhang Y. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. … Cell Biol. 2004;24:10161–10168.
   Web of Science ®Google Scholar
• Cullinan SB, Zhang D, Hannink M, Arvisais E, Kaufman RJ, Diehl JA. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol. 2003;23:7198–7209.
   PubMed Web of Science ®Google Scholar
• Cullinan SB, Diehl JA. PERK-dependent Activation of Nrf2 Contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. J Biol Chem. 2004;279:20108–20117.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Thuerauf DJ, Marcinko M, Belmont PJ, Glembotski CC. Effects of the isoform-specific characteristics of ATF6 alpha and ATF6 beta on endoplasmic reticulum stress response gene expression and cell viability. J Biol Chem. 2007;282:22865–22878.
   PubMed Web of Science ®Google Scholar
• Yamazaki H, Hiramatsu N, Hayakawa K, Activation of the Akt–NF-kappaB pathway by subtilase cytotoxin through the ATF6 branch of the unfolded protein response. J Immunol. 2009;183:1480–1487.
   PubMed Web of Science ®Google Scholar
• Liu Y-P, Zeng L, Tian a., Endoplasmic reticulum stress regulates the innate immunity critical transcription factor IRF3. J Immunol. 2012;189:4630–4639.
   PubMed Web of Science ®Google Scholar
• Reimold AM, Iwakoshi NN, Manis J, Plasma cell differentiation requires the transcription factor XBP-1. Nature. 2001;412:300–307.
   PubMed Web of Science ®Google Scholar
• Iwakoshi NN, Lee A-H, Vallabhajosyula P, Otipoby KL, Rajewsky K, Glimcher LH. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol. 2003;4:321–329.
   PubMed Web of Science ®Google Scholar
• Brunsing R, Omori SA, Weber F, B- and T-cell development both involve activity of the unfolded protein response pathway. J Biol Chem. 2008;283:17954–61.
   PubMed Web of Science ®Google Scholar
• Iwakoshi NN, Pypaert M, Glimcher LH. The transcription factor XBP-1 is essential for the development and survival of dendritic cells. J Exp Med. 2007;204:2267–2275.
   PubMed Web of Science ®Google Scholar
• Todd DJ, Lee A-H, Glimcher LH. The endoplasmic reticulum stress response in immunity and autoimmunity. Nat Rev Immunol. 2008;8:663–674.
   PubMed Web of Science ®Google Scholar
• Hasnain SZ, Lourie R, Das I, Chen AC-H, McGuckin MA. The interplay between endoplasmic reticulum stress and inflammation. Immunol Cell Biol. 2012;90:260–270.
   PubMed Web of Science ®Google Scholar
• Hosoi T, Ozawa K. Endoplasmic reticulum stress in disease: mechanisms and therapeutic opportunities. Clin Sci (Lond). 2010;118:19–29.
   Web of Science ®Google Scholar
• Garg AD, Kaczmarek A, Krysko O, Vandenabeele P, Krysko D V., Agostinis P. ER stress-induced inflammation: Does it aid or impede disease progression? Trends Mol Med. 2012;18:589–598.
   PubMed Web of Science ®Google Scholar
• Tersey SA, Nishiki Y, Templin AT, Islet β-cell endoplasmic reticulum stress precedes the onset of type 1 diabetes in the nonobese diabetic mouse model. Diabetes. 2012;61:818–827.
   PubMed Web of Science ®Google Scholar
• Engin F, Yermalovich A, Nguyen T, Restoration of the unfolded protein response in pancreatic β cells protects mice against type 1 diabetes. Sci Transl Med. 2013;5:211ra156.
   PubMed Web of Science ®Google Scholar
• Gora S, Maouche S, Atout R, Phospholipolyzed LDL induces an inflammatory response in endothelial cells through endoplasmic reticulum stress signaling. FASEB J. 2010;24:3284–3297.
   PubMed Web of Science ®Google Scholar
• Maguire JA, Mulugeta S, Beers MF. Endoplasmic reticulum stress induced by surfactant protein C BRICHOS mutants promotes proinflammatory signaling by epithelial cells. Am J Respir Cell Mol Biol. 2011;44:404–414.
   PubMed Web of Science ®Google Scholar
• Clavarino G, Cláudio N, Couderc T, Induction of GADD34 is necessary for dsRNA-dependent interferon-β production and participates in the control of Chikungunya virus infection. PLoS Pathog. 2012;8:e1002708.
   PubMed Web of Science ®Google Scholar
• Goodall JC, Wu C, Zhang Y, Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression. Proc Natl Acad Sci U S A. 2010;107:17698–17703.
   PubMed Web of Science ®Google Scholar
• Smith JA, Turner MJ, DeLay ML, Klenk EI, Sowders DP, Colbert RA. Endoplasmic reticulum stress and the unfolded protein response are linked to synergistic IFN-beta induction via X-box binding protein 1. Eur J Immunol. 2008;38:1194–1203.
   PubMed Web of Science ®Google Scholar
• Zhang C, Bai N, Chang A, ATF4 is directly recruited by TLR4 signaling and positively regulates TLR4-trigged cytokine production in human monocytes. Cell Mol Immunol. 2013;10:84–94.
   PubMed Web of Science ®Google Scholar
• Roy CR, Salcedo SP, Gorvel J-PE. Pathogen-endoplasmic-reticulum interactions: in through the out door. Nat Rev Immunol. 2006;6:136–147.
   PubMed Web of Science ®Google Scholar
• Smith JA. A new paradigm: Innate immune sensing of viruses via the unfolded protein response. Front Microbiol. 2014;5:222.
   PubMed Web of Science ®Google Scholar
• Celli J, Tsolis RM. Bacteria, the endoplasmic reticulum and the unfolded protein response: friends or foes?. Nat Rev Microbiol. 2015;13:71–82.
   PubMed Web of Science ®Google Scholar
• Dalod M, Pierre P. Integration of ER stress and viral nucleotide sensing in DCs: mounting a response commensurate to the threat? Eur J Immunol. 2011;41:898–901.
   PubMed Web of Science ®Google Scholar
• Martinon F, Chen X, Lee A-H, Glimcher LH. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol. 2010;11:411–418.
   PubMed Web of Science ®Google Scholar
• Cho JA, Lee AH, Platzer B, The unfolded protein response element IRE1α senses bacterial proteins invading the ER to activate RIG-I and innate immune signaling. Cell Host Microbe. 2013;13:558–569.
   PubMed Web of Science ®Google Scholar
• Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signaling. Nature. 2008;455:674–678.
   PubMed Web of Science ®Google Scholar
• Pahl HL, Baeuerle PA. A novel signal transduction pathway from the endoplasmic reticulum to the nucleus is mediated by transcription factor NF-kappa B. EMBO J. 1995;14:2580–2588.
   PubMed Web of Science ®Google Scholar
• Menu P, Mayor a, Zhou R, ER stress activates the NLRP3 inflammasome via an UPR-independent pathway. Cell Death Dis. 2012;3:e261.
   PubMed Web of Science ®Google Scholar
• Pahl HL, Baeuerle PA. Activation of NF-kappa B by ER stress requires both Ca2 +and reactive oxygen intermediates as messengers. FEBS Lett. 1996;392:129–136.
   PubMed Web of Science ®Google Scholar
• Deniaud A, Sharaf el dein O, Maillier E, Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene. 2008;27:285–299.
   PubMed Web of Science ®Google Scholar
• Shkoda A, Ruiz PA, Daniel H, Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology. 2007;132:190–207.
   PubMed Web of Science ®Google Scholar
• Zhang K, Shen X, Wu J, Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell. 2006;124:587–599.
   PubMed Web of Science ®Google Scholar
• Nakajima S, Saito Y, Takahashi S, Anti-inflammatory subtilase cytotoxin up-regulates A20 through the unfolded protein response. Biochem Biophys Res Commun. 2010;397:176–180.
   PubMed Web of Science ®Google Scholar
• Hayakawa K, Nakajima S, Hiramatsu N, ER stress depresses NF-kappaB activation in mesangial cells through preferential induction of C/EBP beta. J Am Soc Nephrol. 2010;21:73–81.
   PubMed Web of Science ®Google Scholar
• Nakajima S, Hiramatsu N, Hayakawa K, Selective abrogation of BiP/GRP78 blunts activation of NF-κB through the ATF6 branch of the UPR: involvement of C/EBPβ and mTOR-dependent dephosphorylation of Akt. Mol Cell Biol. 2011;31:1710–1718.
   PubMed Web of Science ®Google Scholar
• Luís A, Martins JD, Silva A, Ferreira I, Cruz MT, Neves BM. Oxidative stress-dependent activation of the eIF2α–ATFr unfolded protein response branch by skin sensitizer 1-fluoro-2,4-dinitrobenzene modulates dendritic-like cell maturation and inflammatory status in a biphasic manner. Free Radic Biol Med. 2014;77:217–229.
   PubMed Web of Science ®Google Scholar
• Inagi R, Kumagai T, Nishi H, Preconditioning with endoplasmic reticulum stress ameliorates mesangioproliferative glomerulonephritis. J Am Soc Nephrol. 2008;19:915–922.
   PubMed Web of Science ®Google Scholar
• Li J, Wang JJ, Zhang SX. Preconditioning with endoplasmic reticulum stress mitigates retinal endothelial inflammation via activation of X-box binding protein 1. J Biol Chem. 2011;286:4912–4921.
   PubMed Web of Science ®Google Scholar
• Lin W, Bailey SL, Ho H, The integrated stress response prevents demyelination by protecting oligodendrocytes against immune-mediated damage. J Clin Invest. 2007;117:448–456.
   PubMed Web of Science ®Google Scholar
• Ulianich L, Terrazzano G, Annunziatella M, Ruggiero G, Beguinot F, Di Jeso B. ER stress impairs MHC Class I surface expression and increases susceptibility of thyroid cells to NK-mediated cytotoxicity. Biochim Biophys Acta. 2011;1812:431–438.
   PubMed Web of Science ®Google Scholar
• Granados DP, Tanguay P-L, Hardy M-P, ER stress affects processing of MHC class I-associated peptides. BMC Immunol. 2009;10:10.
   PubMed Web of Science ®Google Scholar
• Bläß S, Union A, Raymackers J, The stress protein BiP is overexpressed and is a major B and T cell target in rheumatoid arthritis. Arthritis Rheum. 2001;44:761–771.
   PubMed Web of Science ®Google Scholar
• O’Sullivan-Murphy B, Urano F. ER stress as a trigger for β-cell dysfunction and autoimmunity in type 1 Diabetes. Diabetes. 2012;61:780–781.
   PubMed Web of Science ®Google Scholar
• Wiest DL, Burkhardt JK, Hester S, Hortsch M, Meyer DI, Argon Y. Membrane biogenesis during B cell differentiation: most endoplasmic reticulum proteins are expressed coordinately. J Cell Biol. 1990;110:1501–1511.
   PubMed Web of Science ®Google Scholar
• Shapiro-Shelef M, Lin KI, McHeyzer-Williams LJ, Liao J, McHeyzer-Williams MG, Calame K. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity. 2003;19:607–620.
   PubMed Web of Science ®Google Scholar
• Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity. 2004;21:81–93.
   PubMed Web of Science ®Google Scholar
• Klein U, Casola S, Cattoretti G, Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat Immunol. 2006;7:773–782.
   PubMed Web of Science ®Google Scholar
• Shimizu Y, Meunier L, Hendershot LM. pERp1 is significantly up-regulated during plasma cell differentiation and contributes to the oxidative folding of immunoglobulin. Proc Natl Acad Sci U S A. 2009;106:17013–17018.
   PubMed Web of Science ®Google Scholar
• Tirosh B, Iwakoshi NN, Glimcher LH, Ploegh HL. XBP-1 specifically promotes IgM synthesis and secretion, but is dispensable for degradation of glycoproteins in primary B cells. J Exp Med. 2005;202:505–516.
   PubMed Web of Science ®Google Scholar
• Benhamron S, Hadar R, Iwawaky T, So JS, Lee AH, Tirosh B. Regulated IRE1-dependent decay participates in curtailing immunoglobulin secretion from plasma cells. Eur J Immunol. 2014;44:867–876.
   PubMed Web of Science ®Google Scholar
• Zhang K, Wong HN, Song B, Miller CN, Scheuner D, Kaufman RJ. The unfolded protein response sensor IRE1α is required at 2 distinct steps in B cell lymphopoiesis. J Clin Invest. 2005;115:268–281.
   PubMed Web of Science ®Google Scholar
• Brewer JW, Jackowski S. UPR-mediated membrane biogenesis in B cells. Biochem Res Int. 2012;7:1–7.
   Google Scholar
• Gass JN, Jiang H-Y, Wek RC, Brewer JW. The unfolded protein response of B-lymphocytes: PERK-independent development of antibody-secreting cells. Mol Immunol. 2008;45:1035–1043.
   PubMed Web of Science ®Google Scholar
• Masciarelli S, Fra AM, Pengo N, Bertolotti M, CHOP-independent apoptosis and pathway-selective induction of the UPR in developing plasma cells. Mol Immunol. 2010;47:1356–1365.
   PubMed Web of Science ®Google Scholar
• Ma Y, Shimizu Y, Mann MJ, Jin Y, Hendershot LM. Plasma cell differentiation initiates a limited ER stress response by specifically suppressing the PERK-dependent branch of the unfolded protein response. Cell Stress Chaperones. 2010;15:281–293.
   PubMed Web of Science ®Google Scholar
• Gunn KE, Gifford NM, Mori K, Brewer JW. A role for the unfolded protein response in optimizing antibody secretion. Mol Immunol. 2004;41:919–27.
   PubMed Web of Science ®Google Scholar
• Aragon I V, Barrington RA, Jackowski S, Mori K, Brewer JW. The specialized unfolded protein response of B lymphocytes: ATF6α-independent development of antibody-secreting B cells. Mol Immunol. 2012;51:347–55.
   PubMed Web of Science ®Google Scholar
• Carrasco DR, Sukhdeo K, Protopopova M, The differentiation and stress response factor XBP-1 drives multiple myeloma pathogenesis. Cancer Cell. 2007;11:349–360.
   PubMed Web of Science ®Google Scholar
• Bagratuni T, Wu P, Gonzalez de Castro D, XBP1s levels are implicated in the biology and outcome of myeloma mediating different clinical outcomes to thalidomide-based treatments. Blood. 2010;116:250–3.
   PubMed Web of Science ®Google Scholar
• Vincenz L, Jäger R, O’Dwyer M, Samali A. Endoplasmic reticulum stress and the unfolded protein response: targeting the Achilles heel of multiple myeloma. Mol Cancer Ther. 2013;12:831–843.
   PubMed Web of Science ®Google Scholar
• Ri M, Tashiro E, Oikawa D, Identification of Toyocamycin, an agent cytotoxic for multiple myeloma cells, as a potent inhibitor of ER stress-induced XBP1 mRNA splicing. Blood Cancer J. 2012;2:e79.
   PubMed Web of Science ®Google Scholar
• Bae J, Smith R, Daley J, Myeloma-specific multiple peptides able to generate cytotoxic T lymphocytes: a potential therapeutic application in multiple myeloma and other plasma cell disorders. Clin Cancer Res. 2012;18:4850–60.
   PubMed Web of Science ®Google Scholar
• Bae J, Prabhala R, Voskertchian a, A multiepitope of XBP1, CD138 and CS1 peptides induces myeloma-specific cytotoxic T lymphocytes in T cells of smoldering myeloma patients. Leukemia. 2014;1:1–12.
   Google Scholar
• Michallet AS, Mondiere P, Taillardet M, Leverrier Y, Genestier L, Defrance T. Compromising the unfolded protein response induces autophagy-mediated cell death in multiple myeloma cells. PLoS One. 2011;6:e25820.
   PubMed Web of Science ®Google Scholar
• Kamimura D, Bevan MJ. Endoplasmic reticulum stress regulator XBP-1 contributes to effector CD8+ T cell differentiation during acute infection. J Immunol. 2008;181:5433–41.
   PubMed Web of Science ®Google Scholar
• García-Navas R, Munder M, Mollinedo F. Depletion of l-arginine induces autophagy as a cytoprotective response to endoplasmic reticulum stress in human T lymphocytes. Autophagy. 2012;8:1557–1576.
   PubMed Web of Science ®Google Scholar
• Scheu S, Stetson DB, Reinhardt RL, Leber JH, Mohrs M, Locksley RM. Activation of the integrated stress response during T helper cell differentiation. Nat Immunol. 2006;7:644–651.
   PubMed Web of Science ®Google Scholar
• Franco A, Almanza G, Burns JC, Wheeler M, Zanetti M. Endoplasmic reticulum stress drives a regulatory phenotype in human T-cell clones. Cell Immunol. 2010;266:1–6.
   PubMed Web of Science ®Google Scholar
• Lee W-S, Sung M-S, Lee E-G, A pathogenic role for ER stress-induced autophagy and ER chaperone GRP78/BiP in T lymphocyte systemic lupus erythematosus. J Leukoc Biol. 2014;97:425–433.
   PubMed Web of Science ®Google Scholar
• Chang J-S, Ocvirk S, Berger E, Endoplasmic reticulum stress response promotes cytotoxic phenotype of CD8αβ +intraepithelial lymphocytes in a mouse model for Crohn's disease-like ileitis. J Immunol. 2012;189:1510–20.
   PubMed Web of Science ®Google Scholar
• Doody GM, Stephenson S, Tooze RM. BLIMP-1 is a target of cellular stress and downstream of the unfolded protein response. Eur J Immunol. 2006;36:1572–82.
   PubMed Web of Science ®Google Scholar
• Chang DH, Angelin-Duclos C, Calame K. BLIMP-1: trigger for differentiation of myeloid lineage. Nat Immunol. 2000;1:169–176.
   PubMed Web of Science ®Google Scholar
• Dickhout JG, Lhoták Š, Hilditch BA, Induction of the unfolded protein response after monocyte to macrophage differentiation augments cell survival in early atherosclerotic lesions. FASEB J. 2011;25:576–589.
   PubMed Web of Science ®Google Scholar
• Komura T, Sakai Y, Honda M, Takamura T, Wada T, Kaneko S. ER stress induced impaired TLR signaling and macrophage differentiation of human monocytes. Cell Immunol. 2013;282:44–52.
   PubMed Web of Science ®Google Scholar
• Yang C, Zhou J-Y, Zhong H-J, Exogenous norepinephrine correlates with macrophage endoplasmic reticulum stress response in association with XBP-1. J Surg Res. 2011;168:262–271.
   PubMed Web of Science ®Google Scholar
• Kim S, Joe Y, Kim HJ, Endoplasmic reticulum stress-induced IRE1 activation mediates cross-talk of GSK-3 and XBP-1 to regulate inflammatory cytokine production. J Immunol. 2015;194(9):4498–4506.
   Web of Science ®Google Scholar
• Feng B, Yao PM, Li Y, The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat Cell Biol. 2003;5:781–92.
   PubMed Web of Science ®Google Scholar
• Zhou J, Lhoták 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;111:1814–1821.
   PubMed Web of Science ®Google Scholar
• Myoishi M, Hao H, Minamino T, Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome. Circulation. 2007;116:1226–1233.
   PubMed Web of Science ®Google Scholar
• Tabas I. The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ Res. 2010;107:839–850.
   PubMed Web of Science ®Google Scholar
• Tabas I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol. 2010;10:36–46.
   PubMed Web of Science ®Google Scholar
• Oh J, Riek AE, Weng S, Endoplasmic reticulum stress controls M2 macrophage differentiation and foam cell formation. J Biol Chem. 2012;287:11629–11641.
   PubMed Web of Science ®Google Scholar
• Yao S, Miao C, Tian H, Endoplasmic reticulum stress promotes macrophage-derived foam cell formation by up-regulating cluster of differentiation 36 (CD36) expression. J Biol Chem. 2014;289:4032–4042.
   PubMed Web of Science ®Google Scholar
• Yao S, Yang N, Song G, Minimally modified low-density lipoprotein induces macrophage endoplasmic reticulum stress via toll-like receptor 4. Biochim Biophys Acta. 2012;1821:954–963.
   PubMed Web of Science ®Google Scholar
• Ishiyama J, Taguchi R, Akasaka Y, Unsaturated FAs prevent palmitate-induced LOX-1 induction via inhibition of ER stress in macrophages. J Lipid Res. 2011;52:299–307.
   PubMed Web of Science ®Google Scholar
• Dai M-X, Zheng X-H, Yu J, The impact of intermittent and repetitive cold stress exposure on endoplasmic reticulum stress and instability of atherosclerotic plaques. Cell Physiol Biochem. 2014;34:393–404.
   PubMed Web of Science ®Google Scholar
• DeVries-Seimon T, Li Y, Pin MY, Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor. J Cell Biol. 2005;171:61–73.
   PubMed Web of Science ®Google Scholar
• Thorp E, Iwawaki T, Miura M, Tabas I. A reporter for tracking the UPR in vivo reveals patterns of temporal and cellular stress during atherosclerotic progression. J Lipid Res. 2011;52:1033–1038.
   PubMed Web of Science ®Google Scholar
• 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;9:474–481.
   PubMed Web of Science ®Google Scholar
• Shenderov K, Riteau N, Yip R, Cutting edge: endoplasmic reticulum stress licenses macrophages to produce mature IL-1β in response to TLR4 stimulation through a caspase-8- and TRIF-dependent pathway. J Immunol. 2014;192:2029–2033.
   PubMed Web of Science ®Google Scholar
• Kim HM, Do C-H, Lee DH. Combined effects of multiple endoplasmic reticulum stresses on cytokine secretion in macrophage. Biomol Ther (Seoul). 2012;20:346–351.
   PubMed Web of Science ®Google Scholar
• Komura T, Sakai Y, Honda M, Takamura T, Matsushima K, Kaneko S. CD14+ monocytes are vulnerable and functionally impaired under endoplasmic reticulum stress in patients with type 2 diabetes. Diabetes. 2010;59:634–643.
   PubMed Web of Science ®Google Scholar
• Woo CW, Cui D, Arellano J, Adaptive suppression of the ATF4-CHOP branch of the unfolded protein response by toll-like receptor signalling. Nat Cell Biol. 2009;11:1473–1480.
   PubMed Web of Science ®Google Scholar
• Woo CW, Kutzler L, Kimball SR, Tabas I. Toll-like receptor activation suppresses ER stress factor CHOP and translation inhibition through activation of eIF2B. Nat Cell Biol. 2012;14:192–200.
   PubMed Web of Science ®Google Scholar
• De Jong MF, Starr T, Winter MG, Sensing of bacterial type IV secretion via the unfolded protein response. MBio. 2013;4:e00418–12.
   PubMed Web of Science ®Google Scholar
• Smith J a., Khan M, Magnani DD, Brucella induces an unfolded protein response via TcpB that supports intracellular replication in macrophages. PLoS Pathog. 2013;9:1–12.
   Web of Science ®Google Scholar
• Seimon T a, Kim MJ, Blumenthal A, Induction of ER stress in macrophages of tuberculosis granulomas. PLoS One. 2010;5:1–12.
   Web of Science ®Google Scholar
• Choi J, Lim Y-J, Cho S-N, Mycobacterial HBHA induces endoplasmic reticulum stress-mediated apoptosis through the generation of reactive oxygen species and cytosolic Ca2+ in murine macrophage RAW 264.7 cells. Cell Death Dis. 2013;4:e957.
   PubMed Web of Science ®Google Scholar
• Lim YJ, Choi HH, Choi JA, Mycobacterium kansasii-induced death of murine macrophages involves endoplasmic reticulum stress responses mediated by reactive oxygen species generation or calpain activation. Apoptosis. 2013;18:150–159.
   PubMed Web of Science ®Google Scholar
• Lim YJ, Choi JA, Choi HH, Endoplasmic reticulum stress pathway-mediated apoptosis in macrophages contributes to the survival of mycobacterium tuberculosis. PLoS One. 2011;6:e28531.
   PubMed Web of Science ®Google Scholar
• Wati S, Soo M-L, Zilm P, Dengue virus infection induces upregulation of GRP78, which acts to chaperone viral antigen production. J Virol. 2009;83:12871–12880.
   PubMed Web of Science ®Google Scholar
• Clarke HJ, Chambers JE, Liniker E, Marciniak SJ. Endoplasmic reticulum stress in malignancy. Cancer Cell. 2014;25:563–573.
   PubMed Web of Science ®Google Scholar
• Mahadevan NR, Rodvold J, Sepulveda H, Rossi S, Drew AF, Zanetti M. Transmission of endoplasmic reticulum stress and pro-inflammation from tumor cells to myeloid cells. Proc Natl Acad Sci U S A. 2011;108:6561–6566.
   PubMed Web of Science ®Google Scholar
• Cullen SJ, Fatemie S, Ladiges W. Breast tumor cells primed by endoplasmic reticulum stress remodel macrophage phenotype. Am J Cancer Res. 2013;3:196–210.
   PubMed Web of Science ®Google Scholar
• Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392:245–252.
   PubMed Web of Science ®Google Scholar
• Hirai M, Kadowaki N, Kitawaki T, Bortezomib suppresses function and survival of plasmacytoid dendritic cells by targeting intracellular trafficking of Toll-like receptors and endoplasmic reticulum homeostasis. Hematology. 2011;117:500–509.
   Google Scholar
• Osorio F, Tavernier SJ, Hoffmann E, The unfolded-protein-response sensor IRE-1α regulates the function of CD8α+ dendritic cells. Nat Immunol. 2014;15:248–57.
   PubMed Web of Science ®Google Scholar
• Subramanian M, Tabas I. A new RIDDle in DC-mediated cross-presentation. Nat Publ Gr. 2014;15:213–215.
   Google Scholar
• Hu F, Yu X, Wang H, ER stress and its regulator X-box-binding protein-1 enhance polyIC-induced innate immune response in dendritic cells. Eur J Immunol. 2011;41:1086–1097.
   PubMed Web of Science ®Google Scholar
• Yang D, Chen Q, Yang H, Tracey KJ, Bustin M, Oppenheim JJ. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J Leukoc Biol. 2006;81:59–66.
   PubMed Web of Science ®Google Scholar
• Dumitriu IE, Bianchi ME, Bacci M, Manfredi AA, Rovere-Querini P. The secretion of HMGB1 is required for the migration of maturing dendritic cells. J Leukoc Biol. 2007;81:84–91.
   PubMed Web of Science ®Google Scholar
• Zhu XM, Yao FH, Yao YM, Dong N, Yu Y, Sheng ZY. Endoplasmic reticulum stress and its regulator XBP-1 contributes to dendritic cell maturation and activation induced by high mobility group box-1 protein. Int J Biochem Cell Biol. 2012;44:1097–1105.
   PubMed Web of Science ®Google Scholar
• Mahadevan NR, Anufreichik V, Rodvold JJ, Chiu KT, Sepulveda H, Zanetti M. Cell-extrinsic effects of tumor ER stress imprint myeloid dendritic cells and impair CD8+ T cell priming. PLoS One. 2012;7:e51845.
   PubMed Web of Science ®Google Scholar
• Berrou J, Fougeray S, Venot M, Natural killer cell function, an important target for infection and tumor protection, is impaired in type 2 diabetes. PLoS One. 2013;8(4):e62418.
   Web of Science ®Google Scholar
• Talmadge JE, Gabrilovich DI. History of myeloid-derived suppressor cells. Nat Rev Cancer. 2013;13:739–752.
   PubMed Web of Science ®Google Scholar
• Condamine T, Kumar V, Ramachandran IR, ER stress regulates myeloid-derived suppressor cell fate through TRAIL-R–mediated apoptosis. J Clin Invest. 2014;124:2626–2639.
   PubMed Web of Science ®Google Scholar
• Lee B, Chang S, Hong E, Elevated endoplasmic reticulum stress reinforced immunosuppression in the tumor microenvironment via myeloid-derived suppressor cells. Oncotarget. 2014;5:12331–12345.
   PubMed Web of Science ®Google Scholar