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http://dx.doi.org/10.14348/molcells.2018.0241

Roles of Endoplasmic Reticulum Stress in Immune Responses  

So, Jae-Seon (Department of Medical Biotechnology, Dongguk University Gyeongju)
Publication Information
Molecules and Cells / v.41, no.8, 2018 , pp. 705-716 More about this Journal
Abstract
The endoplasmic reticulum (ER) is a critical organelle for protein synthesis, folding and modification, and lipid synthesis and calcium storage. Dysregulation of ER functions leads to the accumulation of misfolded- or unfolded-protein in the ER lumen, and this triggers the unfolded protein response (UPR), which restores ER homeostasis. The UPR is characterized by three distinct downstream signaling pathways that promote cell survival or apoptosis depending on the stressor, the intensity and duration of ER stress, and the cell type. Mammalian cells express the UPR transducers IRE1, PERK, and ATF6, which control transcriptional and translational responses to ER stress. Direct links between ER stress and immune responses are also evident, but the mechanisms by which UPR signaling cascades are coordinated with immunity remain unclear. This review discusses recent investigations of the roles of ER stress in immune responses that lead to differentiation, maturation, and cytokine expression in immune cells. Further understanding of how ER stress contributes to the pathogenesis of immune disorders will facilitate the development of novel therapies that target UPR pathways.
Keywords
ER stress; immune response; inositol requiring enzyme 1 (IRE1); unfolded protein response (UPR); X-box binding protein 1 (XBP1);
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1 Yoshida, H., Matsui, T., Yamamoto, A., Okada, T., and Mori, K. (2001). XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891.   DOI
2 Zhang, K., and Kaufman, R.J. (2008). From endoplasmic-reticulum stress to the inflammatory response. Nature 454, 455-462.   DOI
3 Zhang, K., Shen, X., Wu, J., Sakaki, K., Saunders, T., Rutkowski, D.T., Back, S.H., and Kaufman, R.J. (2006). Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124, 587-599.   DOI
4 Zinszner, H., Kuroda, M., Wang, X., Batchvarova, N., Lightfoot, R.T., Remotti, H., Stevens, J.L., and Ron, D. (1998). CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12, 982-995.   DOI
5 Deng, J., Lu, P.D., Zhang, Y., Scheuner, D., Kaufman, R.J., Sonenberg, N., Harding, H.P., and Ron, D. (2004). Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol. Cell. Biol. 24, 10161-10168.   DOI
6 Endo, M., Oyadomari, S., Suga, M., Mori, M., and Gotoh, T. (2005). The ER stress pathway involving CHOP is activated in the lungs of LPS-treated mice. J. Biochem. 138, 501-507.   DOI
7 Fanlei, H., Xiaofei, Y., Hongxia, W., Daming, Z., Chunqing, G., Huanfa, Y., Boaz, T., R., S.J., Xiaoyan, Q., and Xiang-Yang, W. (2011). ER stress and its regulator X-box-binding protein-1 enhance polyICinduced innate immune response in dendritic cells. Eur. J. Immunol. 41, 1086-1097.   DOI
8 Fawcett, T.W., Martindale, J.L., Guyton, K.Z., Hai, T., and Holbrook, N.J. (1999). Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem. J. 339, 135-141.
9 Marisa, R., Andreia, M., J., A.R., Evelina, G., and Philippe, P. (2018). At the crossway of ER-stress and proinflammatory responses. FEBS J. doi:10.1111/febs.14391. [Epub ahead of print].   DOI
10 Marciniak, S.J., and Ron, D. (2006). Endoplasmic reticulum stress signaling in disease. Physiol. Rev. 86, 1133-1149.   DOI
11 Moore, K., and Hollien, J. (2015). Ire1-mediated decay in mammalian cells relies on mRNA sequence, structure, and translational status. Mol. Biol. Cell 26, 2873-2884.   DOI
12 Smith, J.A. (2018). Regulation of cytokine production by the unfolded protein response; implications for infection and autoimmunity. Front. Immunol. 9, 422.   DOI
13 Smith, J.A., Turner, M.J., DeLay, M.L., Klenk, E.I., Sowders, D.P., and Colbert, R.A. (2008). Endoplasmic reticulum stress and the unfolded protein response are linked to synergistic IFN-${\beta}$ induction via X-box binding protein 1. Eur. J. Immunol. 38, 1194-1203.   DOI
14 Franco, A., Almanza, G., Burns, J.C., Wheeler, M., and Zanetti, M. (2010). Endoplasmic reticulum stress drives a regulatory phenotype in human T-cell clones. Cell. Immunol. 266, 1-6.   DOI
15 Garg, A.D., Kaczmarek, A., Krysko, O., Vandenabeele, P., Krysko, D. V, and Agostinis, P. (2012). ER stress-induced inflammation: does it aid or impede disease progression? Trends Mol. Med. 18, 589-598.   DOI
16 Gass, J.N., Gifford, N.M., and Brewer, J.W. (2002). Activation of an unfolded protein response during differentiation of antibodysecreting B cells. J. Biol. Chem. 277, 49047-49054.   DOI
17 Martinon, F., Chen, X., Lee, A.-H., and Glimcher, L.H. (2010). TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 11, 411-418.   DOI
18 Martins, A.S., Alves, I., Helguero, L., Domingues, M.R., and Neves, B.M. (2016). The unfolded protein response in homeostasis and modulation of mammalian immune cells. Int. Rev. Immunol. 35, 457-476.   DOI
19 Novoa, I., Zhang, Y., Zeng, H., Jungreis, R., Harding, H.P., and Ron, D. (2003). Stress-induced gene expression requires programmed recovery from translational repression. EMBO J. 22, 1180-1187.   DOI
20 Oikawa, D., Kimata, Y., Kohno, K., and Iwawaki, T. (2009). Activation of mammalian IRE1${\alpha}$ upon ER stress depends on dissociation of BiP rather than on direct interaction with unfolded proteins. Exp. Cell Res. 315, 2496-2504.   DOI
21 Oikawa, D., Tokuda, M., Hosoda, A., and Iwawaki, T. (2010). Identification of a consensus element recognized and cleaved by IRE1${\alpha}$. Nucleic Acids Res. 38, 6265-6273.   DOI
22 Oslowski, C.M., and Urano, F. (2011). Measuring ER stress and the unfolded protein response using mammalian tissue culture system. Methods Enzymol. 490, 71-92.
23 Tang, C.-H.A., Chang, S., Paton, A.W., Paton, J.C., Gabrilovich, D.I., Ploegh, H.L., Del Valle, J.R., and Hu, C.-C.A. (2018). Phosphorylation of IRE1 at S729 regulates RIDD in B cells and antibody production after immunization. J. Cell Biol. 217, 1739-1755.   DOI
24 So, J.-S., Hur, K.Y., Tarrio, M., Ruda, V., Frank-Kamenetsky, M., Fitzgerald, K., Koteliansky, V., Lichtman, A.H., Iwawaki, T., Glimcher, L.H., et al. (2012). Silencing of lipid metabolism genes through IRE1${\alpha}$-mediated mRNA decay lowers plasma lipids in mice. Cell Metab. 16, 487-499.   DOI
25 So, J.-S., Cho, S., Min, S.-H., Kimball, S.R., and Lee, A.-H. (2015). IRE1${\alpha}$-dependent decay of CReP/Ppp1r15b mRNA increases eukaryotic initiation factor 2${\alpha}$ phosphorylation and suppresses protein synthesis. Mol. Cell. Biol. 35, 2761-2770.   DOI
26 Stadhouders, R., Lubberts, E., and Hendriks, R.W. (2018). A cellular and molecular view of T helper 17 cell plasticity in autoimmunity. J. Autoimmun. 87, 1-15.   DOI
27 Taubenheim, N., Tarlinton, D.M., Crawford, S., Corcoran, L.M., Hodgkin, P.D., and Nutt, S.L. (2012). High rate of antibody secretion is not integral to plasma cell differentiation as revealed by XBP-1 deficiency. J. Immunol. 189, 3328-3338.   DOI
28 Harding, H.P., Zeng, H., Zhang, Y., Jungries, R., Chung, P., Plesken, H., Sabatini, D.D., and Ron, D. (2001). Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol. Cell 7, 1153-1163.   DOI
29 Goodall, J.C., Wu, C., Zhang, Y., McNeill, L., Ellis, L., Saudek, V., and Gaston, J.S.H. (2010). Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression. Proc. Natl. Acad. Sci. USA 107, 17698-17703.   DOI
30 Han, D., Lerner, A.G., Vande Walle, L., Upton, J.-P., Xu, W., Hagen, A., Backes, B.J., Oakes, S.A., and Papa, F.R. (2009). IRE1${\alpha}$ kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138, 562-575.   DOI
31 Harding, H.P., Zhang, Y., Scheuner, D., Chen, J.-J., Kaufman, R.J., and Ron, D. (2009). Ppp1r15 gene knockout reveals an essential role for translation initiation factor 2 alpha (eIF2${\alpha}$) dephosphorylation in mammalian development. Proc. Natl. Acad. Sci. USA 106, 1832-1837.   DOI
32 Hollien, J., Lin, J.H., Li, H., Stevens, N., Walter, P., and Weissman, J.S. (2009). Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 186, 323-331.   DOI
33 Heazlewood, C.K., Cook, M.C., Eri, R., Price, G.R., Tauro, S.B., Taupin, D., Thornton, D.J., Png, C.W., Crockford, T.L., Cornall, R.J., et al. (2008). Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLOS Med. 5, e54.   DOI
34 Hetz, C. (2012). The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13, 89-102.   DOI
35 Hetz, C., Chevet, E., and Harding, H.P. (2013). Targeting the unfolded protein response in disease. Nat. Rev. Drug Discov. 12, 703-719.   DOI
36 Hirayama, D., Iida, T., and Nakase, H. (2018). The phagocytic function of macrophage-enforcing innate immunity and tissue homeostasis. Int. J. Mol. Sci. 19, 92.
37 Hollien, J., and Weissman, J.S. (2006). Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313, 104-107.   DOI
38 Hotamisligil, G.S. (2010). Endoplasmic reticulum stress and atherosclerosis. Nat. Med. 16, 396-399.   DOI
39 Hu, P., Han, Z., Couvillon, A.D., Kaufman, R.J., and Exton, J.H. (2006). Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1${\alpha}$-mediated NF-${\kappa}$B activation and down-regulation of TRAF2 expression. Mol. Cell. Biol. 26, 3071-3084.   DOI
40 Hur, K.Y., So, J.-S., Ruda, V., Frank-Kamenetsky, M., Fitzgerald, K., Koteliansky, V., Iwawaki, T., Glimcher, L.H., and Lee, A.-H. (2012). IRE1${\alpha}$ activation protects mice against acetaminophen-induced hepatotoxicity. J. Exp. Med. 209, 307-318.   DOI
41 Puthalakath, H., O'Reilly, L.A., Gunn, P., Lee, L., Kelly, P.N., Huntington, N.D., Hughes, P.D., Michalak, E.M., McKimm-Breschkin, J., Motoyama, N., et al. (2007). ER Stress Triggers Apoptosis by Activating BH3-Only Protein Bim. Cell 129, 1337-1349.   DOI
42 Osorio, F., Tavernier, S.J., Hoffmann, E., Saeys, Y., Martens, L., Vetters, J., Delrue, I., De Rycke, R., Parthoens, E., Pouliot, P., et al. (2014). The unfolded-protein-response sensor IRE-1${\alpha}$ regulates the function of CD8${\alpha}+$ dendritic cells. Nat. Immunol. 15, 248-257.   DOI
43 Oyadomari, S., Harding, H.P., Zhang, Y., Oyadomari, M., and Ron, D. (2008). Dephosphorylation of translation initiation factor 2${\alpha}$ enhances glucose tolerance and attenuates hepatosteatosis in mice. Cell Metab. 7, 520-532.   DOI
44 Ozcan, U., Cao, Q., Yilmaz, E., Lee, A.-H., Iwakoshi, N.N., Ozdelen, E., Tuncman, G., GOrgun, C., Glimcher, L.H., and Hotamisligil, G.S. (2004). Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306, 457-461.   DOI
45 Raffaella, I., and Cristina, M. (2015). Cell death induced by endoplasmic reticulum stress. FEBS J. 283, 2640-2652.
46 Rao, J., Yue, S., Fu, Y., Zhu, J., Wang, X., Busuttil, R.W., Kupiec-Weglinski, J.W., Lu, L., and Zhai, Y. (2014). ATF6 mediates a proinflammatory synergy between ER stress and TLR activation in the pathogenesis of liver ischemia reperfusion injury. Am. J. Transplant 14, 1552-1561.   DOI
47 Reimold, A.M., Etkin, A., Clauss, I., Perkins, A., Friend, D.S., Zhang, J., Horton, H.F., Scott, A., Orkin, S.H., Byrne, M.C., et al. (2000). An essential role in liver development for transcription factor XBP-1. Genes Dev. 14, 152-157.
48 Thaxton, J.E., Wallace, C., Riesenberg, B., Zhang, Y., Paulos, C.M., Beeson, C.C., Liu, B., and Li, Z. (2017). Modulation of endoplasmic reticulum stress controls CD4+ T-cell activation and antitumor function. Cancer Immunol. Res. 5, 666-675.   DOI
49 Tavernier, S.J., Osorio, F., Vandersarren, L., Vetters, J., Vanlangenakker, N., Van Isterdael, G., Vergote, K., De Rycke, R., Parthoens, E., van de Laar, L., et al. (2017). Regulated IRE1-dependent mRNA decay sets the threshold for dendritic cell survival. Nat. Cell Biol. 19, 698-710.   DOI
50 Tellier, J., Shi, W., Minnich, M., Liao, Y., Crawford, S., Smyth, G.K., Kallies, A., Busslinger, M., and Nutt, S.L. (2016). Blimp-1 controls plasma cell function through the regulation of immunoglobulin secretion and the unfolded protein response. Nat. Immunol. 17, 323-330.   DOI
51 Todd, D.J., McHeyzer-Williams, L.J., Kowal, C., Lee, A.-H., Volpe, B.T., Diamond, B., McHeyzer-Williams, M.G., and Glimcher, L.H. (2009). XBP1 governs late events in plasma cell differentiation and is not required for antigen-specific memory B cell development. J. Exp. Med. 206, 2151-2159.   DOI
52 Tsuru, A., Fujimoto, N., Takahashi, S., Saito, M., Nakamura, D., Iwano, M., Iwawaki, T., Kadokura, H., Ron, D., and Kohno, K. (2013). Negative feedback by IRE1${\beta}$ optimizes mucin production in goblet cells. Proc. Natl. Acad. Sci. USA 110, 2864 LP-2869.
53 Upton, J.-P., Wang, L., Han, D., Wang, E.S., Huskey, N.E., Lim, L., Truitt, M., McManus, M.T., Ruggero, D., Goga, A., et al. (2012). IRE1${\alpha}$ cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science 338, 818-822.   DOI
54 Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., Harding, H.P., and Ron, D. (2000). Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666.   DOI
55 Kamimura, D., and Bevan, M.J. (2008). Endoplasmic reticulum stress regulator XBP-1 contributes to effector CD8+ T cell differentiation during acute infection. J. Immunol. 181, 5433-5441.   DOI
56 Iqbal, J., Dai, K., Seimon, T., Jungreis, R., Oyadomari, M., Kuriakose, G., Ron, D., Tabas, I., and Hussain, M.M. (2008). IRE1${\beta}$ inhibits chylomicron production by selectively degrading MTP mRNA. Cell Metab. 7, 445-455.   DOI
57 Iwakoshi, N.N., Pypaert, M., and Glimcher, L.H. (2007). The transcription factor XBP-1 is essential for the development and survival of dendritic cells. J. Exp. Med. 204, 2267-2275.   DOI
58 Janssens, S., Pulendran, B., and Lambrecht, B.N. (2014). Emerging functions of the unfolded protein response in immunity. Nat. Immunol. 15, 910-919.   DOI
59 Kaser, A., Lee, A.-H., Franke, A., Glickman, J.N., Zeissig, S., Tilg, H., Nieuwenhuis, E.E.S., Higgins, D.E., Schreiber, S., Glimcher, L.H., et al. (2008). XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134, 743-756.   DOI
60 Kaufman, R.J., Scheuner, D., SchrOder, M., Shen, X., Lee, K., Liu, C.Y., and Arnold, S.M. (2002). The unfolded protein response in nutrient sensing and differentiation. Nat. Rev. Mol. Cell Biol. 3, 411-421.
61 Wang, S., and Kaufman, R.J. (2012). The impact of the unfolded protein response on human disease. J. Cell Biol. 197, 857-867.   DOI
62 Acosta-Alvear, D., Zhou, Y., Blais, A., Tsikitis, M., Lents, N.H., Arias, C., Lennon, C.J., Kluger, Y., and Dynlacht, B.D. (2007). XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol. Cell 27, 53-66.   DOI
63 Ko, J.S., Koh, J.M., So, J.-S., Jeon, Y.K., Kim, H.Y., and Chung, D.H. (2017). Palmitate inhibits arthritis by inducing t-bet and gata-3 mRNA degradation in iNKT cells via IRE1${\alpha}$-dependent decay. Sci. Rep. 7, 14940.   DOI
64 Lee, A.-H., Iwakoshi, N.N., and Glimcher, L.H. (2003). XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23, 7448-7459.   DOI
65 Urra, H., Dufey, E., Lisbona, F., Rojas-Rivera, D., and Hetz, C. (2013). When ER stress reaches a dead end. Biochim. Biophys. Acta. Mol. Cell Res. 1833, 3507-3517.   DOI
66 Vattemi, G., Engel, W.K., McFerrin, J., and Askanas, V. (2004). Endoplasmic reticulum stress and unfolded protein response in inclusion body myositis muscle. Am. J. Pathol. 164, 1-7.   DOI
67 Volmer, R., and Ron, D. (2015). Lipid-dependent regulation of the unfolded protein response. Curr. Opin. Cell Biol. 33, 67-73.   DOI
68 Walter, P., and Ron, D. (2011). The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086.   DOI
69 Wheeler, M.C., Rizzi, M., Sasik, R., Almanza, G., Hardiman, G., and Zanetti, M. (2008). KDEL-retained antigen in B lymphocytes induces a proinflammatory response: a possible role for endoplasmic reticulum stress in adaptive T cell immunity. J. Immunol. 181, 256-264.   DOI
70 Xue, X., Piao, J.-H., Nakajima, A., Sakon-Komazawa, S., Kojima, Y., Mori, K., Yagita, H., Okumura, K., Harding, H., and Nakano, H. (2005). Tumor necrosis factor ${\alpha}$ (TNF${\alpha}$) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNF${\alpha}$. J. Biol. Chem. 280, 33917-33925.   DOI
71 Yamaguchi, H., and Wang, H.-G. (2004). CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J. Biol. Chem. 279, 45495-45502.   DOI
72 Bettigole, S.E., and Glimcher, L.H. (2015). Endoplasmic reticulum stress in immunity. Annu. Rev. Immunol. 33, 107-138.   DOI
73 Adachi, Y., Yamamoto, K., Okada, T., Yoshida, H., Harada, A., and Mori, K. (2008). ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum. Cell Struct. Funct. 33, 75-89.   DOI
74 Ansa-Addo, E.A., Thaxton, J., Hong, F., Wu, B.X., Zhang, Y., Fugle, C.W., Metelli, A., Riesenberg, B., Williams, K., Gewirth, D.T., et al. (2016). Clients and oncogenic roles of molecular chaperone gp96/grp94. Curr. Top. Med. Chem. 16, 2765-2778.   DOI
75 Bertolotti, A., Zhang, Y., Hendershot, L.M., Harding, H.P., and Ron, D. (2000). Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2, 326-332.   DOI
76 Bettigole, S.E., Lis, R., Adoro, S., Lee, A.-H., Spencer, L.A., Weller, P.F., and Glimcher, L.H. (2015). The transcription factor XBP1 is selectively required for eosinophil differentiation. Nat. Immunol. 16, 829-837.   DOI
77 Braakman, I., and Bulleid, N.J. (2011). Protein folding and modification in the mammalian endoplasmic reticulum. Annu. Rev. Biochem. 80, 71-99.   DOI
78 Calfon, M., Zeng, H., Urano, F., Till, J.H., Hubbard, S.R., Harding, H.P., Clark, S.G., and Ron, D. (2002). IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96.   DOI
79 Brucklacher-Waldert, V., Ferreira, C., Stebegg, M., Fesneau, O., Innocentin, S., Marie, J.C., and Veldhoen, M. (2017). Cellular stress in the context of an inflammatory environment supports TGF-${\beta}$-independent T helper-17 differentiation. Cell Rep. 19, 2357-2370.   DOI
80 Byrd, A.E., and Brewer, J.W. (2012). Intricately regulated: a cellular toolbox for fine-tuning XBP1 expression and activity. Cells 1, 738-753.   DOI
81 Lipson, K.L., Fonseca, S.G., Ishigaki, S., Nguyen, L.X., Foss, E., Bortell, R., Rossini, A.A., and Urano, F. (2006). Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulumresident protein kinase IRE1. Cell Metab. 4, 245-254.   DOI
82 Lee, A., Chu, G.C., Iwakoshi, N.N., and Glimcher, L.H. (2005). XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J. 24, 4368-4380.   DOI
83 Lee, A.-H., Scapa, E.F., Cohen, D.E., and Glimcher, L.H. (2008). Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320, 1492-1496.   DOI
84 Lerner, A.G., Upton, J.-P., Praveen, P.V.K., Ghosh, R., Nakagawa, Y., Igbaria, A., Shen, S., Nguyen, V., Backes, B.J., Heiman, M., et al. (2012). IRE1${\alpha}$ induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death during endoplasmic reticulum stress. Cell Metab. 16, 250-264.   DOI
85 Ma, Y., and Hendershot, L.M. (2003). Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J. Biol. Chem. 278, 34864-34873.   DOI
86 Reimold, A.M., Iwakoshi, N.N., Manis, J., Vallabhajosyula, P., Szomolanyi-Tsuda, E., Gravallese, E.M., Friend, D., Grusby, M.J., Alt, F., and Glimcher, L.H. (2001). Plasma cell differentiation requires the transcription factor XBP-1. Nature 412, 300-307.   DOI
87 Ron, D., and Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529.   DOI
88 Rutkowski, D.T., and Hegde, R.S. (2010). Regulation of basal cellular physiology by the homeostatic unfolded protein response. J. Cell Biol. 189, 783-794.   DOI
89 Lipson, K.L., Ghosh, R., and Urano, F. (2008). The role of IRE1${\alpha}$ in the degradation of insulin mRNA in pancreatic ${\beta}$-cells. PLoS One 3, e1648.   DOI
90 Lu, P.D., Harding, H.P., and Ron, D. (2004). Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol. 167, 27-33.   DOI
91 Ma, Y., Brewer, J.W., Alan Diehl, J., and Hendershot, L.M. (2002). Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318, 1351-1365.   DOI
92 Shen, J., Chen, X., Hendershot, L., and Prywes, R. (2002). ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of golgi localization signals. Dev. Cell 3, 99-111.   DOI
93 Sandrine, B., Rivka, H., Takao, I., Jae-Seon, S., Ann-Hwee, L., and Boaz, T. (2013). Regulated IRE1-dependent decay participates in curtailing immunoglobulin secretion from plasma cells. Eur. J. Immunol. 44, 867-876.
94 Scheu, S., Stetson, D.B., Reinhardt, R.L., Leber, J.H., Mohrs, M., and Locksley, R.M. (2006). Activation of the integrated stress response during T helper cell differentiation. Nat. Immunol. 7, 644-651.
95 Shaffer, A.L., Shapiro-Shelef, M., Iwakoshi, N.N., Lee, A.-H., Qian, S.-B., Zhao, H., Yu, X., Yang, L., Tan, B.K., Rosenwald, A., et al. (2004). XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21, 81-93.   DOI
96 Shkoda, A., Ruiz, P.A., Daniel, H., Kim, S.C., Rogler, G., Sartor, R.B., and Haller, D. (2007). Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology 132, 190-207.   DOI
97 Cao, S.S., Luo, K.L., and Shi, L. (2016). Endoplasmic reticulum stress interacts with inflammation in human diseases. J. Cell. Physiol. 231, 288-294.   DOI
98 Yamamoto, K., Yoshida, H., Kokame, K., Kaufman, R.J., and Mori, K. (2004). Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J. Biochem. 136, 343-350.   DOI
99 Yamamoto, K., Suzuki, N., Wada, T., Okada, T., Yoshida, H., Kaufman, R.J., and Mori, K. (2008). Human HRD1 promoter carries a functional unfolded protein response element to which XBP1 but not ATF6 directly binds. J. Biochem. 144, 477-486.   DOI
100 Ye, J., Rawson, R.B., Komuro, R., Chen, X., Davé, U.P., Prywes, R., Brown, M.S., and Goldstein, J.L. (2000). ER Stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6, 1355-1364.   DOI
101 Chen, X., Karnovsky, A., Sans, M.D., Andrews, P.C., and Williams, J.A. (2010). Molecular characterization of the endoplasmic reticulum: insights from proteomic studies. Proteomics 10, 4040-4052.   DOI
102 Coelho, D.S., and Domingos, P.M. (2014). Physiological roles of regulated Ire1 dependent decay. Front. Genet. 5, 76.
103 Cubillos-Ruiz, J.R., Silberman, P.C., Rutkowski, M.R., Chopra, S., Perales-Puchalt, A., Song, M., Zhang, S., Bettigole, S.E., Gupta, D., Holcomb, K., et al. (2015). ER stress sensor XBP1 controls anti-tumor immunity by disrupting dendritic cell homeostasis. Cell 161, 1527-1538.   DOI