Modulating stress responses by the UPRosome: A matter of life and death

Trends in Biochemical Sciences

Volumn 36, Issue 6, 2011, Pages 329-337

  Woehlbier, Ute ^a   Hetz, Claudio ^a,b,c  

^a UNIVERSITY OF CHILE   (Chile)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c Neurounion Biomedical Foundation   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ADAPTOR PROTEIN; CCAAT ENHANCER BINDING PROTEIN; PROTEIN IRE1; PROTEIN KINASE R;

APOPTOSIS; CELL DEATH; CELL FATE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; HUMANS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; UNFOLDED PROTEIN RESPONSE;

EID: 79958033194     PISSN: 09680004     EISSN: 09680004     Source Type: Journal    
DOI: 10.1016/j.tibs.2011.03.001     Document Type: Review

References (100)

1. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 2005, 74:739-789.
2. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8:519-529.
3. Hetz C., Glimcher L.H. Fine-tuning of the unfolded protein response: assembling the IRE1alpha interactome. Mol. Cell 2009, 35:551-561.
4. Rodriguez D., et al. Integrating stress signals at the endoplasmic reticulum: the BCL-2 protein family rheostat. Biochim. Biophys. Acta 2010, 1813:564-574.
5. Matus, S. et al. (2011) Protein folding stress in neurodegenerative diseases: a glimpse into the ER. Curr. Opin. Cell Biol. Jan 31. doi:10.1016/j.ceb.2011.01.003.
6. Calfon M., et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002, 415:92-96.
7. Lee K., et al. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 2002, 16:452-466.
8. Yoshida H., et al. 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.
9. Bertolotti A., et al. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2000, 2:326-332.
10. Okamura K., et al. Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem. Biophys. Res. Commun. 2000, 279:445-450.
11. Kimata Y., et al. Genetic evidence for a role of BiP/Kar2 that regulates Ire1 in response to accumulation of unfolded proteins. Mol. Biol. Cell 2003, 14:2559-2569.
12. Credle J.J., et al. On the mechanism of sensing unfolded protein in the endoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:18773-18784.
13. Kimata Y., et al. Two regulatory steps of ER-stress sensor Ire1 involving its cluster formation and interaction with unfolded proteins. J. Cell Biol. 2007, 179:75-86.
14. Kimata Y., et al. A role for BiP as an adjustor for the endoplasmic reticulum stress-sensing protein Ire1. J. Cell Biol. 2004, 167:445-456.
15. Oikawa D., et al. Activation of mammalian IRE1alpha upon ER stress depends on dissociation of BiP rather than on direct interaction with unfolded proteins. Exp. Cell Res. 2009, 315:2496-2504.
16. Zhou J., et al. The crystal structure of human IRE1 luminal domain reveals a conserved dimerization interface required for activation of the unfolded protein response. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:14343-14348.
17. Pincus D., et al. BiP binding to the ER-stress sensor Ire1 tunes the homeostatic behavior of the unfolded protein response. PLoS Biol. 2010, 8:e1000415.
18. Liu C.Y., et al. Ligand-independent dimerization activates the stress response kinases IRE1 and PERK in the lumen of the endoplasmic reticulum. J. Biol. Chem. 2000, 275:24881-24885.
19. Harding H.P., et al. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999, 397:271-274.
20. Ameri K., Harris A.L. Activating transcription factor 4. Int. J. Biochem. Cell Biol. 2008, 40:14-21.
21. Harding H.P., et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 2003, 11:619-633.
22. Lange P.S., et al. ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J. Exp. Med. 2008, 205:1227-1242.
23. Nadanaka S., et al. Analysis of ATF6 activation in Site-2 protease-deficient Chinese hamster ovary cells. Cell Struct. Funct. 2006, 31:109-116.
24. Shen J., et al. Stable binding of ATF6 to BiP in the endoplasmic reticulum stress response. Mol. Cell Biol. 2005, 25:921-932.
25. Haze K., et al. 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.
26. Trusina A., et al. Rationalizing translation attenuation in the network architecture of the unfolded protein response. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:20280-20285.
27. Hollien J., Weissman J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 2006, 313:104-107.
28. Hollien J., et al. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 2009, 186:323-331.
29. Han D., et al. IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 2009, 138:562-575.
30. Aragon T., et al. Messenger RNA targeting to endoplasmic reticulum stress signalling sites. Nature 2009, 457:736-740.
31. Kim I., et al. Chemical biology investigation of cell death pathways activated by endoplasmic reticulum stress reveals cytoprotective modulators of ASK1. J. Biol. Chem. 2009, 284:1593-1603.
32. Nishitoh H., et al. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 2002, 16:1345-1355.
33. Urano F., et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666.
34. Criollo A., et al. The inositol trisphosphate receptor in the control of autophagy. Autophagy 2007, 3:350-353.
35. Ogata M., et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell Biol. 2006, 26:9220-9231.
36. Yamamoto K., et al. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev. Cell 2007, 13:365-376.
37. Puthalakath H., et al. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129:1337-1349.
38. Woo C.W., et al. Adaptive suppression of the ATF4-CHOP branch of the unfolded protein response by toll-like receptor signalling. Nat. Cell Biol. 2009, 11:1473-1480.
39. McCullough K.D., et al. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Nat. Cell Biol. 2001, 21:1249-1259.
40. Marciniak S.J., et al. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 2004, 18:3066-3077.
41. Lin J.H., et al. Divergent effects of PERK and IRE1 signaling on cell viability. PLoS ONE 2009, 4:e4170.
42. Lin J.H., et al. IRE1 signaling affects cell fate during the unfolded protein response. Science 2007, 318:944-949.
43. Danial N.N., Korsmeyer S.J. Cell death: critical control points. Cell 2004, 116:205-219.
44. Tait S.W., Green D.R. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 2010, 11:621-632.
45. Scorrano L., et al. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 2003, 300:135-139.
46. Zong W.X., et al. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell Biol. 2003, 162:59-69.
47. Wei M.C., et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001, 292:727-730.
48. Galehdar Z., et al. 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. 2010, 30:16938-16948.
49. Nakagawa T., et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403:98-103.
50. Hitomi J., et al. Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death. J. Cell Biol. 2004, 165:347-356.
51. Rao R.V., et al. Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J. Biol. Chem. 2002, 277:21836-21842.
52. Lisbona F., Hetz C. Turning off the unfolded protein response: an interplay between the apoptosis machinery and ER stress signaling. Cell Cycle 2009, 8:1643-1644.
53. Hetz C., et al. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 2006, 312:572-576.
54. Luo D., et al. AIP1 is critical in transducing IRE1-mediated endoplasmic reticulum stress response. J. Biol. Chem. 2008, 283:11905-11912.
55. Gupta S., et al. HSP72 protects cells from ER stress-induced apoptosis via enhancement of IRE1alpha-XBP1 signaling through a physical interaction. PLoS Biol. 2010, 8:e1000410.
56. Lisbona F., et al. BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1alpha. Mol. Cell 2009, 33:679-691.
57. Gu F., et al. Protein-tyrosine phosphatase 1B potentiates IRE1 signaling during endoplasmic reticulum stress. J. Biol. Chem. 2004, 279:49689-49693.
58. Gonzalez T.N., Walter P. Ire1p: a kinase and site-specific endoribonuclease. Methods Mol. Biol. 2001, 160:25-36.
59. Li H., et al. Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:16113-16118.
60. Lee G.H., et al. Bax inhibitor-1 regulates endoplasmic reticulum stress-associated reactive oxygen species and heme oxygenase-1 expression. J. Biol. Chem. 2007, 282:21618-21628.
61. Bailly-Maitre B., et al. Hepatic Bax inhibitor-1 inhibits IRE1alpha and protects from obesity-associated insulin resistance and glucose intolerance. J. Biol. Chem. 2010, 285:6198-6207.
62. Bailly-Maitre B., et al. Cytoprotective gene bi-1 is required for intrinsic protection from endoplasmic reticulum stress and ischemia-reperfusion injury. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:2809-2814.
63. Rong J., et al. Bifunctional apoptosis regulator (BAR), an endoplasmic reticulum-associated E3 ubiquitin ligase, modulates BI-1 protein stability and function in ER stress. J. Biol. Chem. 2011, 286:1453-1463.
64. Novoa I., et al. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J. Cell Biol. 2001, 153:1011-1022.
65. Brush M.H., et al. Growth arrest and DNA damage-inducible protein GADD34 targets protein phosphatase 1 alpha to the endoplasmic reticulum and promotes dephosphorylation of the alpha subunit of eukaryotic translation initiation factor 2. Nat. Cell Biol. 2003, 23:1292-1303.
66. Kojima E., et al. The function of GADD34 is a recovery from a shutoff of protein synthesis induced by ER stress: elucidation by GADD34-deficient mice. FASEB J. 2003, 17:1573-1575.
67. Ma Y., Hendershot L.M. Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J. Biol. Chem. 2003, 278:34864-34873.
68. Lemin A.J., et al. Activation of the unfolded protein response and alternative splicing of ATF6alpha in HLA-B27 positive lymphocytes. FEBS Lett. 2007, 581:1819-1824.
69. Paschen W., et al. Transient cerebral ischemia activates processing of xbp1 messenger RNA indicative of endoplasmic reticulum stress. J. Cereb. Blood Flow Metab. 2003, 23:449-461.
70. Szegezdi E., et al. ER stress contributes to ischemia-induced cardiomyocyte apoptosis. Biochem. Biophys. Res. Commun. 2006, 349:1406-1411.
71. Qiu Y., et al. A crucial role for RACK1 in the regulation of glucose-stimulated IRE1alpha activation in pancreatic beta cells. Sci. Signal. 2010, 3:ra7.
72. Marcu M.G., et al. Heat shock protein 90 modulates the unfolded protein response by stabilizing IRE1alpha. Nat. Cell Biol. 2002, 22:8506-8513.
73. Mandal A.K., et al. Cdc37 has distinct roles in protein kinase quality control that protect nascent chains from degradation and promote posttranslational maturation. J. Cell Biol. 2007, 176:319-328.
74. Nguyen D.T., et al. Nck-dependent activation of extracellular signal-regulated kinase-1 and regulation of cell survival during endoplasmic reticulum stress. Mol. Biol. Cell 2004, 15:4248-4260.
75. Yoneda T., et al. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J. Biol. Chem. 2001, 276:13935-13940.
76. Oono K., et al. JAB1 participates in unfolded protein responses by association and dissociation with IRE1. Neurochem. Int. 2004, 45:765-772.
77. Niwa M., et al. A role for presenilin-1 in nuclear accumulation of Ire1 fragments and induction of the mammalian unfolded protein response. Cell 1999, 99:691-702.
78. Wang F.M., Ouyang H.J. Regulation of unfolded protein response modulator XBP1s by acetylation and deacetylation. Biochem. J. 2010, 433:245-252.
79. Chen H., Qi L. SUMO modification regulates the transcriptional activity of XBP1. Biochem. J. 2010, 429:95-102.
80. Yoshida H., et al. pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J. Cell Biol. 2006, 172:565-575.
81. Yanagitani K., et al. Translational pausing ensures membrane targeting and cytoplasmic splicing of XBP1u mRNA. Science 2011, 331:586-589.
82. Ma Y., Hendershot L.M. The role of the unfolded protein response in tumour development: friend or foe?. Nat. Rev. Cancer 2004, 4:966-977.
83. Healy S.J.M., et al. Targeting the endoplasmic reticulum-stress response as an anticancer strategy. Eur. J. Pharmacol. 2009, 625:234-246.
84. Koong A.C., et al. Targeting XBP-1 as a novel anti-cancer strategy. Cancer Biol. Ther. 2006, 5:756-759.
85. Romero-Ramirez L., et al. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res. 2004, 64:5943-5947.
86. Hotamisligil G.S. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010, 140:900-917.
87. Lipson K.L., et al. The role of IRE1alpha in the degradation of insulin mRNA in pancreatic beta-cells. PLoS ONE 2008, 3:e1648.
88. Lipson K.L., et al. Endoplasmic reticulum stress-induced apoptosis and auto-immunity in diabetes. Curr. Mol. Med. 2006, 6:71-77.
89. Ozcan U., et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004, 306:457-461.
90. Martinon F., Glimcher L.H. Regulation of innate immunity by signaling pathways emerging from the endoplasmic reticulum. Curr. Opin. Immunol. 2011, 23:35-40.
91. Richardson C.E., et al. An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 2011, 463:1092-1095.
92. Todd D.J., et al. The endoplasmic reticulum stress response in immunity and autoimmunity. Nat. Rev. Immunol. 2008, 8:663-674.
93. Wang L., et al. The unfolded protein response in familial amyotrophic lateral sclerosis. Hum. Mol. Genet. 2011, 20:1008-1015.
94. Saxena S., et al. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat. Neurosci. 2009, 12:627-636.
95. Hetz C., et al. XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Genes Dev. 2009, 23:2294-2306.
96. Hetz C., et al. Unfolded protein response transcription factor XBP-1 does not influence prion replication or pathogenesis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:757-762.
97. Hetz C., et al. Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J. 2003, 22:5435-5445.
98. Hetz C., Glimcher L.H. The UPRosome and XBP-1: mastering secretory cell function. Curr. Immunol. Rev. 2008, 4:1-10.
99. Wiseman R.L., et al. Flavonol activation defines an unanticipated ligand-binding site in the kinase-RNase domain of IRE1. Mol. Cell 2010, 38:291-304.
100. Schroder M. Endoplasmic reticulum stress responses. Cell Mol. Life Sci. 2008, 65:862-894.