Role of the unfolded protein response in organ physiology: Lessons from mouse models

IUBMB Life

Volumn 65, Issue 12, 2013, Pages 962-975

  Cornejo, Víctor Hugo ^a,b   Pihán, Philippe ^a,b   Vidal, René Luis ^c   Hetz, Claudio ^a,b,c,d  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

^c Neurounion Biomedical Foundation   (Chile)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

ER stress; mouse model; protein misfolding; secretory cells; unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; PROTEIN IRE1; PROTEIN IRE1 ALPHA; PROTEIN IRE1 BETA; SERINE; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

APOPTOSIS; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; ENDOPLASMIC RETICULUM STRESS; ENERGY EXPENDITURE; EXTRACELLULAR MATRIX; GENETIC MANIPULATION; GLYCEMIC CONTROL; IN VIVO STUDY; LIPID STORAGE; MOUSE MODEL; NONHUMAN; PHENOTYPE; PHYSIOLOGY; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REVIEW; RNA TRANSLATION; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

ER STRESS; MOUSE MODEL; PROTEIN MISFOLDING; SECRETORY CELLS; UNFOLDED PROTEIN RESPONSE;

ANIMALS; APOPTOSIS; DISEASE MODELS, ANIMAL; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; MICE; ORGAN SPECIFICITY; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE;

EID: 84891273860     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.1224     Document Type: Review

References (122)

1. Ron, D., and, Walter, P,. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529.
2. Hetz, C,. (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13, 89-102.
3. Hetz, C., Chevet, E., and, Harding, H. P,. (2013) Targeting the unfolded protein response in disease. Nat. Rev. Drug Discov. 12, 703-719.
4. Walter, P., and, Ron, D,. (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086.
5. Calfon, M., Zeng, H., Urano, F., Till, J. H., Hubbard, S. R., et al. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96.
6. Lee, K., Tirasophon, W., Shen, X., Michalak, M., Prywes, R., et al. (2002) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16, 452-466.
7. 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.
8. Acosta-Alvear, D., Zhou, Y., Blais, A., Tsikitis, M., Lents, N. H., et al. (2007) XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol. Cell 27, 53-66.
9. 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.
10. Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., et al. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666.
11. Nishitoh, H., Matsuzawa, A., Tobiume, K., Saegusa, K., Takeda, K., et al. (2002) ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 16, 1345-1355.
12. Hollien, J., Lin, J. H., Li, H., Stevens, N., Walter, P., et al. (2009) Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 186, 323-331.
13. Han, D., Lerner, A. G., Vande Walle, L., Upton, J. P., Xu, W., et al. (2009) IRE1α kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138, 562-575.
14. Hollien, J., and, Weissman, J. S,. (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313, 104-107.
15. Upton, J. P., Wang, L., Han, D., Wang, E. S., Huskey, N. E., et al. (2012) IRE1α cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science 338, 818-822.
16. Harding, H. P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., et al. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6, 1099-1108.
17. Harding, H. P., Zhang, Y., and, Ron, D,. (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274.
18. Ameri, K., and, Harris, A. L,. (2008) Activating transcription factor 4. Int. J. Biochem. Cell Biol. 40, 14-21.
19. Harding, H. P., Zhang, Y., Zeng, H., Novoa, I., Lu, P. D., et al. (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619-633.
20. Lange, P. S., Chavez, J. C., Pinto, J. T., Coppola, G., Sun, C. W., et al. (2008) ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J. Exp. Med. 205, 1227-1242.
21. Zinszner, H., Kuroda, M., Wang, X., Batchvarova, N., Lightfoot, R. T., et al. (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12, 982-995.
22. Tabas, I., and, Ron, D,. (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 13, 184-190.
23. Urra, H., Dufey, E., Lisbona, F., Rojas-Rivera, D., and, Hetz, C,. When ER stress reaches a dead end. Biochim. Biophys. Acta; doi:pii: S0167-4889(13)00311-X.10.1016/j.bbamcr.2013.07.024 (in press).
24. Yamamoto, K., Sato, T., Matsui, T., Sato, M., Okada, T., et al. (2007) Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6α and XBP1. Dev. Cell 13, 365-376.
25. Shoulders, M. D., Ryno, L. M., Genereux, J. C., Moresco, J. J., Tu, P. G., et al. (2013) Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep. 3, 1279-1292.
26. Zhang, K., Wong, H. N., Song, B., Miller, C. N., Scheuner, D., et al. (2005) The unfolded protein response sensor IRE1α is required at 2 distinct steps in B cell lymphopoiesis. J. Clin. Invest. 115, 268-281.
27. Iwawaki, T., Akai, R., Yamanaka, S., and, Kohno, K,. (2009) Function of IRE1α in the placenta is essential for placental development and embryonic viability. Proc. Natl. Acad. Sci. USA 106, 16657-16662.
28. Iwawaki, T., Akai, R., and, Kohno, K,. (2010) IRE1α disruption causes histological abnormality of exocrine tissues, increase of blood glucose level, and decrease of serum immunoglobulin level. PLoS One 5, e13052.
29. Bertolotti, A., Wang, X., Novoa, I., Jungreis, R., Schlessinger, K., et al. (2001) Increased sensitivity to dextran sodium sulfate colitis in IRE1β-deficient mice. J. Clin. Invest. 107, 585-593.
30. Martino, M. B., Jones, L., Brighton, B., Ehre, C., Abdulah, L., et al. (2013) The ER stress transducer IRE1β is required for airway epithelial mucin production. Mucosal Immunol. 6, 639-654.
31. Iqbal, J., Dai, K., Seimon, T., Jungreis, R., Oyadomari, M., et al. (2008) IRE1β inhibits chylomicron production by selectively degrading MTP mRNA. Cell Metab. 7, 445-455.
32. Tsuru, A., Fujimoto, N., Takahashi, S., Saito, M., Nakamura, D., et al. (2013) Negative feedback by IRE1β optimizes mucin production in goblet cells. Proc. Natl. Acad. Sci. USA 110, 2864-2869.
33. Reimold, A. M., Etkin, A., Clauss, I., Perkins, A., Friend, D. S., et al. (2000) An essential role in liver development for transcription factor XBP-1. Genes Dev. 14, 152-157.
34. Iwakoshi, N. N., Lee, A. H., Vallabhajosyula, P., Otipoby, K. L., Rajewsky, K., et al. (2003) Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat. Immunol. 4, 321-329.
35. 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.
36. Reimold, A. M., Iwakoshi, N. N., Manis, J., Vallabhajosyula, P., Szomolanyi-Tsuda, E., et al. (2001) Plasma cell differentiation requires the transcription factor XBP-1. Nature 412, 300-307.
37. 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.
38. Lee, A. H., Heidtman, K., Hotamisligil, G. S., and, Glimcher, L. H,. (2011) Dual and opposing roles of the unfolded protein response regulated by IRE1α and XBP1 in proinsulin processing and insulin secretion. Proc. Natl. Acad. Sci. USA 108, 8885-8890.
39. Akiyama, M., Liew, C. W., Lu, S., Hu, J., Martinez, R., et al. (2013) X-box binding protein 1 is essential for insulin regulation of pancreatic α cell function. Diabetes 62, 2439-2449.
40. Kaser, A., Lee, A. H., Franke, A., Glickman, J. N., Zeissig, S., et al. (2008) XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134, 743-756.
41. Harding, H. P., Zeng, H., Zhang, Y., Jungries, R., Chung, P., et al. (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.
42. Zhang, P., McGrath, B., Li, S., Frank, A., Zambito, F., et al. (2002) The PERK eukaryotic initiation factor 2α kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol. Cell. Biol. 22, 3864-3874.
43. Iida, K., Li, Y., McGrath, B. C., Frank, A., and, Cavener, D. R,. (2007) PERK eIF2α kinase is required to regulate the viability of the exocrine pancreas in mice. BMC Cell Biol. 8, 38.
44. Gao, Y., Sartori, D. J., Li, C., Yu, Q. C., Kushner, J. A., et al. (2012) PERK is required in the adult pancreas and is essential for maintenance of glucose homeostasis. Mol. Cell. Biol. 32, 5129-5139.
45. Trinh, M. A., Kaphzan, H., Wek, R. C., Pierre, P., Cavener, D. R., et al. (2012) Brain-specific disruption of the eIF2α kinase PERK decreases ATF4 expression and impairs behavioral flexibility. Cell Rep. 1, 676-688.
46. Scheuner, D., Song, B., McEwen, E., Liu, C., Laybutt, R., et al. (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7, 1165-1176.
47. Scheuner, D., Vander Mierde, D., Song, B., Flamez, D., Creemers, J. W., et al. (2005) Control of mRNA translation preserves endoplasmic reticulum function in β-cells and maintains glucose homeostasis. Nat. Med. 11, 757-764.
48. Back, S. H., Scheuner, D., Han, J., Song, B., Ribick, M., et al. (2009) Translation attenuation through eIF2α phosphorylation prevents oxidative stress and maintains the differentiated state in β-cells. Cell Metab. 10, 13-26.
49. Wang, W., Lian, N., Li, L., Moss, H. E., Perrien, D. S., et al. (2009) Atf4 regulates chondrocyte proliferation and differentiation during endochondral ossification by activating Ihh transcription. Development 136, 4143-4153.
50. Tanaka, T., Tsujimura, T., Takeda, K., Sugihara, A., Maekawa, A., et al. (1998) Targeted disruption of ATF4 discloses its essential role in the formation of eye lens fibres. Genes Cells 3, 801-810.
51. Hettmann, T., Barton, K., and, Leiden, J. M,. (2000) Microphthalmia due to p53-mediated apoptosis of anterior lens epithelial cells in mice lacking the CREB-2 transcription factor. Dev. Biol. 222, 110-123.
52. Masuoka, H. C., and, Townes, T. M,. (2002) Targeted disruption of the activating transcription factor 4 gene results in severe fetal anemia in mice. Blood 99, 736-745.
53. Wu, J., Rutkowski, D. T., Dubois, M., Swathirajan, J., Saunders, T., et al. (2007) ATF6α optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev. Cell 13, 351-364.
54. Rutkowski, D. T., Wu, J., Back, S. H., Callaghan, M. U., Ferris, S. P., et al. (2008) UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev. Cell 15, 829-840.
55. Yamamoto, K., Takahara, K., Oyadomari, S., Okada, T., Sato, T., et al. (2010) Induction of liver steatosis and lipid droplet formation in ATF6α-knockout mice burdened with pharmacological endoplasmic reticulum stress. Mol. Biol. Cell 21, 2975-2986.
56. Usui, M., Yamaguchi, S., Tanji, Y., Tominaga, R., Ishigaki, Y., et al. (2012) Atf6α-null mice are glucose intolerant due to pancreatic β-cell failure on a high-fat diet but partially resistant to diet-induced insulin resistance. Metabolism 61, 1118-1128.
57. Wu, J., Ruas, J. L., Estall, J. L., Rasbach, K. A., Choi, J. H., et al. (2011) The unfolded protein response mediates adaptation to exercise in skeletal muscle through a PGC-1α/ATF6α complex. Cell Metab. 13, 160-169.
58. Murakami, T., Saito, A., Hino, S., Kondo, S., Kanemoto, S., et al. (2009) Signalling mediated by the endoplasmic reticulum stress transducer OASIS is involved in bone formation. Nat. Cell Biol. 11, 1205-1211.
59. Saito, A., Hino, S., Murakami, T., Kanemoto, S., Kondo, S., et al. (2009) Regulation of endoplasmic reticulum stress response by a BBF2H7-mediated Sec23a pathway is essential for chondrogenesis. Nat. Cell. Biol. 11, 1197-1204.
60. Lee, M. W., Chanda, D., Yang, J., Oh, H., Kim, S. S., et al. (2010) Regulation of hepatic gluconeogenesis by an ER-bound transcription factor, CREBH. Cell Metab. 11, 331-339.
61. Zhang, K., Shen, X., Wu, J., Sakaki, K., Saunders, T., et al. (2006) Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124, 587-599.
62. Gupta, S., McGrath, B., and, Cavener, D. R,. (2009) PERK regulates the proliferation and development of insulin-secreting β-cell tumors in the endocrine pancreas of mice. PLoS One 4, e8008.
63. Cavener, D. R., Gupta, S., and, McGrath, B. C,. (2010) PERK in β-cell biology and insulin biogenesis. Trends Endocrinol. Metab. 21, 714-721.
64. Wei, J., Sheng, X., Feng, D., McGrath, B., and, Cavener, D. R,. (2008) PERK is essential for neonatal skeletal development to regulate osteoblast proliferation and differentiation. J. Cell. Physiol. 217, 693-707.
65. Saito, A., Ochiai, K., Kondo, S., Tsumagari, K., Murakami, T., et al. (2011) Endoplasmic reticulum stress response mediated by the PERK-eIF2(α)-ATF4 pathway is involved in osteoblast differentiation induced by BMP2. J. Biol. Chem. 286, 4809-4818.
66. Galehdar, Z., Swan, P., Fuerth, B., Callaghan, S. M., Park, D. S., et al. (2010) Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4-CHOP-mediated induction of the Bcl-2 homology 3-only member PUMA. J. Neurosci. 30, 16938-16948.
67. Lin, W., Lin, Y., Li, J., Fenstermaker, A. G., Way, S. W., et al. (2013) Oligodendrocyte-specific activation of PERK signaling protects mice against experimental autoimmune encephalomyelitis. J. Neurosci. 33, 5980-5991.
68. Ma, T., Trinh, M. A., Wexler, A. J., Bourbon, C., Gatti, E., et al. (2013) Suppression of eIF2α kinases alleviates Alzheimer's disease-related plasticity and memory deficits. Nat. Neurosci. 16, 1299-1305.
69. Dever, T. E,. (2002) Gene-specific regulation by general translation factors. Cell 108, 545-556.
70. Oyadomari, S., Harding, H. P., Zhang, Y., Oyadomari, M., and, Ron, D,. (2008) Dephosphorylation of translation initiation factor 2α enhances glucose tolerance and attenuates hepatosteatosis in mice. Cell Metab. 7, 520-532.
71. Yoshizawa, T., Hinoi, E., Jung, D. Y., Kajimura, D., Ferron, M., et al. (2009) The transcription factor ATF4 regulates glucose metabolism in mice through its expression in osteoblasts. J. Clin. Invest. 119, 2807-2817.
72. Seo, J., Fortuno, E. S., III, Suh, J. M., Stenesen, D., Tang, W., et al. (2009) Atf4 regulates obesity, glucose homeostasis, and energy expenditure. Diabetes 58, 2565-2573.
73. Xiao, G., Zhang, T., Yu, S., Lee, S., Calabuig-Navarro, V., et al. (2013) ATF4 protein deficiency protects against high fructose-induced hypertriglyceridemia in mice. J. Biol. Chem. 288, 25350-25361.
74. Valenzuela, V., Collyer, E., Armentano, D., Parsons, G. B., Court, F. A., et al. (2012) Activation of the unfolded protein response enhances motor recovery after spinal cord injury. Cell Death Dis. 3, e272.
75. Matus, S., Lopez, E., Valenzuela, V., Nassif, M., and, Hetz, C,. (2013) Functional contribution of the transcription factor ATF4 to the pathogenesis of amyotrophic lateral sclerosis. PLoS One 8, e66672.
76. 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.
77. Thorp, E., Li, G., Seimon, T. A., Kuriakose, G., Ron, D., et al. (2009) Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe-/- and Ldlr-/- mice lacking CHOP. Cell Metab. 9, 474-481.
78. Tamaki, N., Hatano, E., Taura, K., Tada, M., Kodama, Y., et al. (2008) CHOP deficiency attenuates cholestasis-induced liver fibrosis by reduction of hepatocyte injury. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G498-G505.
79. Ji, C., Mehrian-Shai, R., Chan, C., Hsu, Y. H., and, Kaplowitz, N,. (2005) Role of CHOP in hepatic apoptosis in the murine model of intragastric ethanol feeding. Alcohol Clin. Exp. Res. 29, 1496-1503.
80. Ariyama, Y., Shimizu, H., Satoh, T., Tsuchiya, T., Okada, S., et al. (2007) Chop-deficient mice showed increased adiposity but no glucose intolerance. Obesity (Silver Spring) 15, 1647-1656.
81. Han, J., Murthy, R., Wood, B., Song, B., Wang, S., et al. (2013) ER stress signalling through eIF2α and CHOP, but not IRE1α, attenuates adipogenesis in mice. Diabetologia 56, 911-924.
82. Maris, M., Overbergh, L., Gysemans, C., Waget, A., Cardozo, A. K., et al. (2012) Deletion of C/EBP homologous protein (Chop) in C57Bl/6 mice dissociates obesity from insulin resistance. Diabetologia 55, 1167-1178.
83. Oyadomari, S., Takeda, K., Takiguchi, M., Gotoh, T., Matsumoto, M., et al. (2001) Nitric oxide-induced apoptosis in pancreatic β-cells is mediated by the endoplasmic reticulum stress pathway. Proc. Natl. Acad. Sci. USA 98, 10845-10850.
84. Song, B., Scheuner, D., Ron, D., Pennathur, S., and, Kaufman, R. J,. (2008) Chop deletion reduces oxidative stress, improves β-cell function, and promotes cell survival in multiple mouse models of diabetes. J. Clin. Invest. 118, 3378-3389.
85. Oyadomari, S., Koizumi, A., Takeda, K., Gotoh, T., Akira, S., et al. (2002) Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Invest. 109, 525-532.
86. Chen, C. M., Wu, C. T., Chiang, C. K., Liao, B. W., and, Liu, S. H,. (2012) C/EBP homologous protein (CHOP) deficiency aggravates hippocampal cell apoptosis and impairs memory performance. PLoS One 7, e40801.
87. Tajiri, S., Oyadomari, S., Yano, S., Morioka, M., Gotoh, T., et al. (2004) Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ. 11, 403-415.
88. Ohri, S. S., Maddie, M. A., Zhang, Y., Shields, C. B., Hetman, M., et al. (2012) Deletion of the pro-apoptotic endoplasmic reticulum stress response effector CHOP does not result in improved locomotor function after severe contusive spinal cord injury. J. Neurotrauma 29, 579-588.
89. Silva, R. M., Ries, V., Oo, T. F., Yarygina, O., Jackson-Lewis, V., et al. (2005) CHOP/GADD153 is a mediator of apoptotic death in substantia nigra dopamine neurons in an in vivo neurotoxin model of parkinsonism. J. Neurochem. 95, 974-986.
90. Pennuto, M., Tinelli, E., Malaguti, M., Del Carro, U., D'Antonio, M., et al. (2008) Ablation of the UPR-mediator CHOP restores motor function and reduces demyelination in Charcot-Marie-Tooth 1B mice. Neuron 57, 393-405.
91. Wang, Y., Vera, L., Fischer, W. H., and, Montminy, M,. (2009) The CREB coactivator CRTC2 links hepatic ER stress and fasting gluconeogenesis. Nature 460, 534-537.
92. Kondo, S., Saito, A., Asada, R., Kanemoto, S., and, Imaizumi, K,. (2011) Physiological unfolded protein response regulated by OASIS family members, transmembrane bZIP transcription factors. IUBMB Life 63, 233-239.
93. Kondo, S., Murakami, T., Tatsumi, K., Ogata, M., Kanemoto, S., et al. (2005) OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes. Nat. Cell Biol. 7, 186-194.
94. Omori, Y., Imai, J., Watanabe, M., Komatsu, T., Suzuki, Y., et al. (2001) CREB-H: a novel mammalian transcription factor belonging to the CREB/ATF family and functioning via the box-B element with a liver-specific expression. Nucleic Acids Res. 29, 2154-2162.
95. Zhang, C., Wang, G., Zheng, Z., Maddipati, K. R., Zhang, X., et al. (2012) Endoplasmic reticulum-tethered transcription factor cAMP responsive element-binding protein, hepatocyte specific, regulates hepatic lipogenesis, fatty acid oxidation, and lipolysis upon metabolic stress in mice. Hepatology 55, 1070-1082.
96. Lee, A. H., 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.
97. Liou, H. C., Boothby, M. R., Finn, P. W., Davidon, R., Nabavi, N., et al. (1990) A new member of the leucine zipper class of proteins that binds to the HLA DRα promoter. Science 247, 1581-1584.
98. Shaffer, A. L., Shapiro-Shelef, M., Iwakoshi, N. N., Lee, A. H., Qian, S. B., 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.
99. Tirosh, B., Iwakoshi, N. N., Glimcher, L. H., and, Ploegh, H. L,. (2005) XBP-1 specifically promotes IgM synthesis and secretion, but is dispensable for degradation of glycoproteins in primary B cells. J. Exp. Med. 202, 505-516.
100. Hu, C. C., Dougan, S. K., McGehee, A. M., Love, J. C., and, Ploegh, H. L,. (2009) XBP-1 regulates signal transduction, transcription factors and bone marrow colonization in B cells. EMBO J. 28, 1624-1636.
101. Todd, D. J., McHeyzer-Williams, L. J., Kowal, C., Lee, A. H., Volpe, B. T., et al. (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.
102. Glas, J., Seiderer, J., Czamara, D., Pasciuto, G., Diegelmann, J., et al. (2012) PTGER4 expression-modulating polymorphisms in the 5p13.1 region predispose to Crohn's disease and affect NF-κB and XBP1 binding sites. PLoS One 7, e52873.
103. 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.
104. Carrasco, D. R., Sukhdeo, K., Protopopova, M., Sinha, R., Enos, M., et al. (2007) The differentiation and stress response factor XBP-1 drives multiple myeloma pathogenesis. Cancer Cell 11, 349-360.
105. Xu, G., Liu, K., Anderson, J., Patrene, K., Lentzsch, S., et al. (2012) Expression of XBP1s in bone marrow stromal cells is critical for myeloma cell growth and osteoclast formation. Blood 119, 4205-4214.
106. Huh, W. J., Esen, E., Geahlen, J. H., Bredemeyer, A. J., Lee, A. H., et al. (2010) XBP1 controls maturation of gastric zymogenic cells by induction of MIST1 and expansion of the rough endoplasmic reticulum. Gastroenterology 139, 2038-2049.
107. So, J. S., Hur, K. Y., Tarrio, M., Ruda, V., Frank-Kamenetsky, M., et al. (2012) Silencing of lipid metabolism genes through IRE1α-mediated mRNA decay lowers plasma lipids in mice. Cell Metab. 16, 487-499.
108. Hayashi, A., Kasahara, T., Kametani, M., and, Kato, T,. (2008) Attenuated BDNF-induced upregulation of GABAergic markers in neurons lacking Xbp1. Biochem. Biophys. Res. Commun. 376, 758-763.
109. Hetz, C., Thielen, P., Matus, S., Nassif, M., Court, F., et al. (2009) XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Genes Dev. 23, 2294-2306.
110. Vidal, R. L., Figueroa, A., Court, F. A., Thielen, P., Molina, C., et al. (2012) Targeting the UPR transcription factor XBP1 protects against Huntington's disease through the regulation of FoxO1 and autophagy. Hum. Mol. Genet. 21, 2245-2262.
111. Zuleta, A., Vidal, R. L., Armentano, D., Parsons, G., and, Hetz, C,. (2012) AAV-mediated delivery of the transcription factor XBP1s into the striatum reduces mutant Huntingtin aggregation in a mouse model of Huntington's disease. Biochem. Biophys. Res. Commun. 420, 558-563.
112. Hu, Y., Park, K. K., Yang, L., Wei, X., Yang, Q., et al. (2012) Differential effects of unfolded protein response pathways on axon injury-induced death of retinal ganglion cells. Neuron 73, 445-452.
113. Hetz, C., Lee, A. H., Gonzalez-Romero, D., Thielen, P., Castilla, J., et al. (2008) Unfolded protein response transcription factor XBP-1 does not influence prion replication or pathogenesis. Proc. Natl. Acad. Sci. USA 105, 757-762.
114. Ozcan, L., Ergin, A. S., Lu, A., Chung, J., Sarkar, S., et al. (2009) Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab. 9, 35-51.
115. Hur, K. Y., So, J. S., Ruda, V., Frank-Kamenetsky, M., Fitzgerald, K., et al. (2012) IRE1α activation protects mice against acetaminophen-induced hepatotoxicity. J. Exp. Med. 209, 307-318.
116. Iqbal, J., Queiroz, J., Li, Y., Jiang, X. C., Ron, D., et al. (2012) Increased intestinal lipid absorption caused by Ire1β deficiency contributes to hyperlipidemia and atherosclerosis in apolipoprotein E-deficient mice. Circ. Res. 110, 1575-1584.
117. Matsuzawa, A., Nishitoh, H., Tobiume, K., Takeda, K., and, Ichijo, H,. (2002) Physiological roles of ASK1-mediated signal transduction in oxidative stress- and endoplasmic reticulum stress-induced apoptosis: advanced findings from ASK1 knockout mice. Antioxid. Redox Signal. 4, 415-425.
118. Tobiume, K., Matsuzawa, A., Takahashi, T., Nishitoh, H., Morita, K., et al. (2001) ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep. 2, 222-228.
119. Nishitoh, H., Kadowaki, H., Nagai, A., Maruyama, T., Yokota, T., et al. (2008) ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev. 22, 1451-1464.
120. 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.
121. Martinez, G., and, Hetz, C,. (2012) Cell-nonautonomous control of the UPR. EMBO Rep. 13, 767-768.
122. Taylor, R. C., and, Dillin, A,. (2013) XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 153, 1435-1447.