The unpredictability of prolonged activation of stress response pathways

Journal of Cell Biology

Volumn 209, Issue 6, 2015, Pages 781-787

  Lamech, Lilian T ^a   Haynes, Cole M ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR; E1A ASSOCIATED P300 PROTEIN; HEAT SHOCK PROTEIN 90; HEAT SHOCK TRANSCRIPTION FACTOR 1; MITOCHONDRIAL PROTEIN; X BOX BINDING PROTEIN 1; ACTIVATING TRANSCRIPTION FACTOR 1; DNA BINDING PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ARTICLE; CELL DEATH; CELL STRESS; CYTOSOL; DEACETYLATION; DEGENERATIVE DISEASE; GLYCOLYSIS; HEAT SHOCK RESPONSE; HOMEOSTASIS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; PROTEIN PROCESSING; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UNFOLDED PROTEIN RESPONSE; AGING; HUMAN; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEOSTASIS DEFICIENCY;

ACTIVATING TRANSCRIPTION FACTOR 1; AGING; DNA-BINDING PROTEINS; HEAT-SHOCK RESPONSE; HUMANS; PROTEOSTASIS DEFICIENCIES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; UNFOLDED PROTEIN RESPONSE;

EID: 84946416503     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201503107     Document Type: Article

References (93)

1. Åkerfelt, M., R.I. Morimoto, and L. Sistonen. 2010. Heat shock factors: integrators of cell stress, development and lifespan. Nat. Rev. Mol. Cell Biol. 11:545-555. http://dx.doi.org/10.1038/nrm2938
2. Ananthan, J., A.L. Goldberg, and R. Voellmy. 1986. Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science. 232:522-524. http://dx.doi.org/10.1126/science.3083508
3. Anckar, J., and L. Sistonen. 2011. Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu. Rev. Biochem. 80:1089-1115. http://dx.doi.org/10.1146/annurev-biochem-060809-095203
4. Baird, N.A., P.M. Douglas, M.S. Simic, A.R. Grant, J.J. Moresco, S.C. Wolff, J.R. Yates III, G. Manning, and A. Dillin. 2014. HSF-1-mediated cytoskeletal integrity determines thermotolerance and life span. Science. 346:360-363. http://dx.doi.org/10.1126/science.1253168
5. Baker, B.M., A.M. Nargund, T. Sun, and C.M. Haynes. 2012. Protective coupling of mitochondrial function and protein synthesis via the eIF2α kinase GCN-2. PLoS Genet. 8:e1002760. http://dx.doi.org/10.1371/journal.pgen.1002760
6. Ben-Zvi, A., E.A. Miller, and R.I. Morimoto. 2009. Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc. Natl. Acad. Sci. USA. 106:14914-14919. http://dx.doi.org/10.1073/pnas.0902882106
7. Bersuker, K., M.S. Hipp, B. Calamini, R.I. Morimoto, and R.R. Kopito. 2013. Heat shock response activation exacerbates inclusion body formation in a cellular model of Huntington disease. J. Biol. Chem. 288:23633-23638. http://dx.doi.org/10.1074/jbc.C113.481945
8. Boyce, M., K.F. Bryant, C. Jousse, K. Long, H.P. Harding, D. Scheuner, R.J. Kaufman, D. Ma, D.M. Coen, D. Ron, and J. Yuan. 2005. A selective inhibitor of eIF2α dephosphorylation protects cells from ER stress. Science. 307:935-939. http://dx.doi.org/10.1126/science.1101902
9. Brandman, O., J. Stewart-Ornstein, D. Wong, A. Larson, C.C. Williams, G.W. Li, S. Zhou, D. King, P.S. Shen, J. Weibezahn, et al. 2012. A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell. 151:1042-1054. http://dx.doi.org/10.1016/j.cell.2012.10.044
10. Bratic, A., and N.G. Larsson. 2013. The role of mitochondria in aging. J. Clin. Invest. 123:951-957. http://dx.doi.org/10.1172/JCI64125
11. Brunquell, J., P. Bowers, and S.D. Westerheide. 2014. Fluorodeoxyuridine enhances the heat shock response and decreases polyglutamine aggregation in an HSF-1-dependent manner in Caenorhabditis elegans. Mech. Ageing Dev. 141-142:1-4. http://dx.doi.org/10.1016/j.mad.2014.08.002
12. Calamini, B., M.C. Silva, F. Madoux, D.M. Hutt, S. Khanna, M.A. Chalfant, S.A. Saldanha, P. Hodder, B.D. Tait, D. Garza, et al. 2012. Small-molecule proteostasis regulators for protein conformational diseases. Nat. Chem. Biol. 8:185-196. http://dx.doi.org/10.1038/nchembio.763
13. Calfon, M., H. Zeng, F. Urano, J.H. Till, S.R. Hubbard, H.P. Harding, S.G. Clark, and D. Ron. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature. 415:92-96. http://dx.doi.org/10.1038/415092a
14. Chawla, A., S. Chakrabarti, G. Ghosh, and M. Niwa. 2011. Attenuation of yeast UPR is essential for survival and is mediated by IRE1 kinase. J. Cell Biol. 193:41-50. http://dx.doi.org/10.1083/jcb.201008071
15. Chiang, W.C., C. Messah, and J.H. Lin. 2012. IRE1 directs proteasomal and lysosomal degradation of misfolded rhodopsin. Mol. Biol. Cell. 23:758-770. http://dx.doi.org/10.1091/mbc.E11-08-0663
16. Cohen, E., J. Bieschke, R.M. Perciavalle, J.W. Kelly, and A. Dillin. 2006. Opposing activities protect against age-onset proteotoxicity. Science. 313:1604-1610. http://dx.doi.org/10.1126/science.1124646
17. Cooley, C.B., L.M. Ryno, L. Plate, G.J. Morgan, J.D. Hulleman, J.W. Kelly, and R.L. Wiseman. 2014. Unfolded protein response activation reduces secretion and extracellular aggregation of amyloidogenic immunoglobulin light chain. Proc. Natl. Acad. Sci. USA. 111:13046-13051. http://dx.doi.org/10.1073/pnas.1406050111
18. Cox, J.S., and P. Walter. 1996. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell. 87:391-404. http://dx.doi.org/10.1016/S0092-8674(00)81360-4
19. Cox, J.S., C.E. Shamu, and P. Walter. 1993. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell. 73:1197-1206. http://dx.doi.org/10.1016/0092-8674(93)90648-A
20. Dai, C., L. Whitesell, A.B. Rogers, and S. Lindquist. 2007. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell. 130:1005-1018. http://dx.doi.org/10.1016/j.cell.2007.07.020
21. Das, I., A. Krzyzosiak, K. Schneider, L. Wrabetz, M. D'Antonio, N. Barry, A. Sigurdardottir, and A. Bertolotti. 2015. Preventing proteostasis diseases by selective inhibition of a phosphatase regulatory subunit. Science. 348:239-242. http://dx.doi.org/10.1126/science.aaa4484
22. David, D.C., N. Ollikainen, J.C. Trinidad, M.P. Cary, A.L. Burlingame, and C. Kenyon. 2010. Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol. 8:e1000450. http://dx.doi.org/10.1371/journal.pbio.1000450
23. Dillin, A., D.K. Crawford, and C. Kenyon. 2002a. Timing requirements for insulin/IGF-1 signaling in C. elegans. Science. 298:830-834. http://dx.doi.org/10.1126/science.1074240
24. Dillin, A., A.L. Hsu, N. Arantes-Oliveira, J. Lehrer-Graiwer, H. Hsin, A.G. Fraser, R.S. Kamath, J. Ahringer, and C. Kenyon. 2002b. Rates of behavior and aging specified by mitochondrial function during development. Science. 298:2398-2401. http://dx.doi.org/10.1126/science.1077780
25. Durieux, J., S. Wolff, and A. Dillin. 2011. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell. 144:79-91. http://dx.doi.org/10.1016/j.cell.2010.12.016
26. Eletto, D., D. Eletto, D. Dersh, T. Gidalevitz, and Y. Argon. 2014. Protein disulfide isomerase A6 controls the decay of IRE1a signaling via disulfide-dependent association. Mol. Cell. 53:562-576. http://dx.doi.org/10.1016/j.molcel.2014.01.004
27. Gardner, B.M., and P. Walter. 2011. Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science. 333:1891-1894. http://dx.doi.org/10.1126/science.1209126
28. Hamamichi, S., R.N. Rivas, A.L. Knight, S. Cao, K.A. Caldwell, and G.A. Caldwell. 2008. Hypothesis-based RNAi screening identifies neuroprotective genes in a Parkinson's disease model. Proc. Natl. Acad. Sci. USA. 105:728-733. http://dx.doi.org/10.1073/pnas.0711018105
29. Han, D., A.G. Lerner, L. Vande Walle, J.P. Upton, W. Xu, A. Hagen, B.J. Backes, S.A. Oakes, and F.R. Papa. 2009. IRE1a kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell. 138:562-575. http://dx.doi.org/10.1016/j.cell.2009.07.017
30. Harbauer, A.B., R.P. Zahedi, A. Sickmann, N. Pfanner, and C. Meisinger. 2014. The protein import machinery of mitochondria-a regulatory hub in metabolism, stress, and disease. Cell Metab. 19:357-372. http://dx.doi.org/10.1016/j.cmet.2014.01.010
31. Harding, H.P., Y. Zhang, A. Bertolotti, H. Zeng, and D. Ron. 2000. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell. 5:897-904. http://dx.doi.org/10.1016/S1097-2765(00)80330-5
32. Harding, H.P., Y. Zhang, D. Scheuner, J.J. Chen, R.J. Kaufman, and D. Ron. 2009. Ppp1r15 gene knockout reveals an essential role for translation initiation factor 2 alpha (eIF2α) dephosphorylation in mammalian development. Proc. Natl. Acad. Sci. USA. 106:1832-1837. http://dx.doi.org/10.1073/pnas.0809632106
33. Haynes, C.M., C.J. Fiorese, and Y.F. Lin. 2013. Evaluating and responding to mitochondrial dysfunction: the mitochondrial unfolded-protein response and beyond. Trends Cell Biol. 23:311-318. http://dx.doi.org/10.1016/j.tcb.2013.02.002
34. Henis-Korenblit, S., P. Zhang, M. Hansen, M. McCormick, S.J. Lee, M. Cary, and C. Kenyon. 2010. Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity. Proc. Natl. Acad. Sci. USA. 107:9730-9735. http://dx.doi.org/10.1073/pnas.1002575107
35. Hollien, J., J.H. Lin, H. Li, N. Stevens, P. Walter, and J.S. Weissman. 2009. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 186:323-331. http://dx.doi.org/10.1083/jcb.200903014
36. Houtkooper, R.H., L. Mouchiroud, D. Ryu, N. Moullan, E. Katsyuba, G. Knott, R.W. Williams, and J. Auwerx. 2013. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature. 497:451-457. http://dx.doi.org/10.1038/nature12188
37. Hsu, A.L., C.T. Murphy, and C. Kenyon. 2003. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science. 300:1142-1145. http://dx.doi.org/10.1126/science.1083701
38. Jensen, M.B., and H. Jasper. 2014. Mitochondrial proteostasis in the control of aging and longevity. Cell Metab. 20:214-225. http://dx.doi.org/10.1016/j.cmet.2014.05.006
39. Kimura, K.D., H.A. Tissenbaum, Y. Liu, and G. Ruvkun. 1997. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science. 277:942-946. http://dx.doi.org/10.1126/science.277.5328.942
40. Korennykh, A.V., P.F. Egea, A.A. Korostelev, J. Finer-Moore, C. Zhang, K.M. Shokat, R.M. Stroud, and P. Walter. 2009. The unfolded protein response signals through high-order assembly of Ire1. Nature. 457:687-693. http://dx.doi.org/10.1038/nature07661
41. Lapierre, L.R., C.D. De Magalhaes Filho, P.R. McQuary, C.C. Chu, O. Visvikis, J.T. Chang, S. Gelino, B. Ong, A.E. Davis, J.E. Irazoqui, et al. 2013. The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans. Nat. Commun. 4:2267. http://dx.doi.org/10.1038/ncomms3267
42. Lee, S.J., A.B. Hwang, and C. Kenyon. 2010. Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity. Curr. Biol. 20:2131-2136. http://dx.doi.org/10.1016/j.cub.2010.10.057
43. Lin, K., J.B. Dorman, A. Rodan, and C. Kenyon. 1997. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science. 278:1319-1322. http://dx.doi.org/10.1126/science.278.5341.1319
44. Lin, J.H., H. Li, Y. Zhang, D. Ron, and P. Walter. 2009. Divergent effects of PERK and IRE1 signaling on cell viability. PLoS ONE. 4:e4170. http://dx.doi.org/10.1371/journal.pone.0004170
45. Lu, M., D.A. Lawrence, S. Marsters, D. Acosta-Alvear, P. Kimmig, A.S. Mendez, A.W. Paton, J.C. Paton, P. Walter, and A. Ashkenazi. 2014. Cell death. Opposing unfolded-protein-response signals converge on death receptor 5 to control apoptosis. Science. 345:98-101. http://dx.doi.org/10.1126/science.1254312
46. Mendillo, M.L., S. Santagata, M. Koeva, G.W. Bell, R. Hu, R.M. Tamimi, E. Fraenkel, T.A. Ince, L. Whitesell, and S. Lindquist. 2012. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell. 150:549-562. http://dx.doi.org/10.1016/j.cell.2012.06.031
47. Morano, K.A., N. Santoro, K.A. Koch, and D.J. Thiele. 1999. A trans-activation domain in yeast heat shock transcription factor is essential for cell cycle progression during stress. Mol. Cell. Biol. 19:402-411.
48. Morgan, W.D., G.T. Williams, R.I. Morimoto, J. Greene, R.E. Kingston, and R. Tjian. 1987. Two transcriptional activators, CCAAT-box-binding transcription factor and heat shock transcription factor, interact with a human hsp70 gene promoter. Mol. Cell. Biol. 7:1129-1138.
49. Morimoto, R.I. 1998. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12:3788-3796. http://dx.doi.org/10.1101/gad.12.24.3788
50. Morley, J.F., and R.I. Morimoto. 2004. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol. Biol. Cell. 15:657-664. http://dx.doi.org/10.1091/mbc.E03-07-0532
51. Mouchiroud, L., R.H. Houtkooper, N. Moullan, E. Katsyuba, D. Ryu, C. Cantó, A. Mottis, Y.S. Jo, M. Viswanathan, K. Schoonjans, et al. 2013. The NAD+/Sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell. 154:430-441. http://dx.doi.org/10.1016/j.cell.2013.06.016
52. Mu, T.W., D.S. Ong, Y.J. Wang, W.E. Balch, J.R. Yates III, L. Segatori, and J.W. Kelly. 2008. Chemical and biological approaches synergize to ameliorate protein-folding diseases. Cell. 134:769-781. http://dx.doi.org/10.1016/j.cell.2008.06.037
53. Nargund, A.M., M.W. Pellegrino, C.J. Fiorese, B.M. Baker, and C.M. Haynes. 2012. Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science. 337:587-590. http://dx.doi.org/10.1126/science.1223560
54. Nargund, A.M., C.J. Fiorese, M.W. Pellegrino, P. Deng, and C.M. Haynes. 2015. Mitochondrial and nuclear accumulation of the transcription factor ATFS-1 promotes OXPHOS recovery during the UPR(mt). Mol. Cell. 58:123-133. http://dx.doi.org/10.1016/j.molcel.2015.02.008
55. Novoa, I., H. Zeng, H.P. Harding, and D. Ron. 2001. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol. 153:1011-1022.
56. Owusu-Ansah, E., W. Song, and N. Perrimon. 2013. Muscle mitohormesis promotes longevity via systemic repression of insulin signaling. Cell. 155:699-712. http://dx.doi.org/10.1016/j.cell.2013.09.021
57. Pellegrino, M.W., A.M. Nargund, N.V. Kirienko, R. Gillis, C.J. Fiorese, and C.M. Haynes. 2014. Mitochondrial UPR-regulated innate immunity provides resistance to pathogen infection. Nature. 516:414-417. http://dx.doi.org/10.1038/nature13818
58. Powers, E.T., R.I. Morimoto, A. Dillin, J.W. Kelly, and W.E. Balch. 2009. Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem. 78:959-991. http://dx.doi.org/10.1146/annurev.biochem.052308.114844
59. Prahlad, V., and R.I. Morimoto. 2011. Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins. Proc. Natl. Acad. Sci. USA. 108:14204-14209. http://dx.doi.org/10.1073/pnas.1106557108
60. Prahlad, V., T. Cornelius, and R.I. Morimoto. 2008. Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science. 320:811-814. http://dx.doi.org/10.1126/science.1156093
61. Qian, S.B., H. McDonough, F. Boellmann, D.M. Cyr, and C. Patterson. 2006. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature. 440:551-555. http://dx.doi.org/10.1038/nature04600
62. Rauthan, M., P. Ranji, N. Aguilera Pradenas, C. Pitot, and M. Pilon. 2013. The mitochondrial unfolded protein response activator ATFS-1 protects cells from inhibition of the mevalonate pathway. Proc. Natl. Acad. Sci. USA. 110:5981-5986. http://dx.doi.org/10.1073/pnas.1218778110
63. Raychaudhuri, S., C. Loew, R. Körner, S. Pinkert, M. Theis, M. Hayer-Hartl, F. Buchholz, and F.U. Hartl. 2014. Interplay of acetyltransferase EP300 and the proteasome system in regulating heat shock transcription factor 1. Cell. 156:975-985. http://dx.doi.org/10.1016/j.cell.2014.01.055
64. Rea, S.L., N. Ventura, and T.E. Johnson. 2007. Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans. PLoS Biol. 5:e259. http://dx.doi.org/10.1371/journal.pbio.0050259
65. Richardson, C.E., T. Kooistra, and D.H. Kim. 2010. An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature. 463:1092-1095. http://dx.doi.org/10.1038/nature08762
66. Roth, D.M., D.M. Hutt, J. Tong, M. Bouchecareilh, N. Wang, T. Seeley, J.F. Dekkers, J.M. Beekman, D. Garza, L. Drew, et al. 2014. Modulation of the maladaptive stress response to manage diseases of protein folding. PLoS Biol. 12:e1001998. http://dx.doi.org/10.1371/journal.pbio.1001998
67. Rubio, C., D. Pincus, A. Korennykh, S. Schuck, H. El-Samad, and P. Walter. 2011. Homeostatic adaptation to endoplasmic reticulum stress depends on Ire1 kinase activity. J. Cell Biol. 193:171-184.
68. Ryno, L.M., R.L. Wiseman, and J.W. Kelly. 2013. Targeting unfolded protein response signaling pathways to ameliorate protein misfolding diseases. Curr. Opin. Chem. Biol. 17:346-352. http://dx.doi.org/10.1016/j.cbpa.2013.04.009
69. Ryno, L.M., J.C. Genereux, T. Naito, R.I. Morimoto, E.T. Powers, M.D. Shoulders, and R.L. Wiseman. 2014. Characterizing the altered cellular proteome induced by the stress-independent activation of heat shock factor 1. ACS Chem. Biol. 9:1273-1283. http://dx.doi.org/10.1021/cb500062n
70. Santagata, S., R. Hu, N.U. Lin, M.L. Mendillo, L.C. Collins, S.E. Hankinson, S.J. Schnitt, L. Whitesell, R.M. Tamimi, S. Lindquist, and T.A. Ince. 2011. High levels of nuclear heat-shock factor 1 (HSF1) are associated with poor prognosis in breast cancer. Proc. Natl. Acad. Sci. USA. 108:18378-18383. http://dx.doi.org/10.1073/pnas.1115031108
71. Schieber, M., and N.S. Chandel. 2014. TOR signaling couples oxygen sensing to lifespan in C. elegans. Cell Reports. 9:9-15. http://dx.doi.org/10.1016/j.celrep.2014.08.075
72. Shen, X., R.E. Ellis, K. Lee, C.Y. Liu, K. Yang, A. Solomon, H. Yoshida, R. Morimoto, D.M. Kurnit, K. Mori, and R.J. Kaufman. 2001. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell. 107:893-903. http://dx.doi.org/10.1016/S0092-8674(01)00612-2
73. Shi, Y., D.D. Mosser, and R.I. Morimoto. 1998. Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev. 12:654-666. http://dx.doi.org/10.1101/gad.12.5.654
74. Shoulders, M.D., L.M. Ryno, J.C. Genereux, J.J. Moresco, P.G. Tu, C. Wu, J.R. Yates III, A.I. Su, J.W. Kelly, and R.L. Wiseman. 2013. Stressindependent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Reports. 3:1279-1292. http://dx.doi.org/10.1016/j.celrep.2013.03.024
75. Steele, A.D., G. Hutter, W.S. Jackson, F.L. Heppner, A.W. Borkowski, O.D. King, G.J. Raymond, A. Aguzzi, and S. Lindquist. 2008. Heat shock factor 1 regulates lifespan as distinct from disease onset in prion disease. Proc. Natl. Acad. Sci. USA. 105:13626-13631. http://dx.doi.org/10.1073/pnas.0806319105
76. Tabas, I., and D. Ron. 2011. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 13:184-190. http://dx.doi.org/10.1038/ncb0311-184
77. Taylor, R.C., and A. Dillin. 2013. XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell. 153:1435-1447. http://dx.doi.org/10.1016/j.cell.2013.05.042
78. Todd-Corlett, A., E. Jones, C. Seghers, and M.J. Gething. 2007. Lobe IB of the ATPase domain of Kar2p/BiP interacts with Ire1p to negatively regulate the unfolded protein response in Saccharomyces cerevisiae. J. Mol. Biol. 367:770-787. http://dx.doi.org/10.1016/j.jmb.2007.01.009
79. Topol, J., D.M. Ruden, and C.S. Parker. 1985. Sequences required for in vitro transcriptional activation of a Drosophila hsp 70 gene. Cell. 42:527-537. http://dx.doi.org/10.1016/0092-8674(85)90110-2
80. Travers, K.J., C.K. Patil, L. Wodicka, D.J. Lockhart, J.S. Weissman, and P. Walter. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell. 101:249-258. http://dx.doi.org/10.1016/S0092-8674(00)80835-1
81. Tsaytler, P., H.P. Harding, D. Ron, and A. Bertolotti. 2011. Selective inhibition of a regulatory subunit of protein phosphatase 1 restores proteostasis. Science. 332:91-94. http://dx.doi.org/10.1126/science.1201396
82. Upton, J.P., L. Wang, D. Han, E.S. Wang, N.E. Huskey, L. Lim, M. Truitt, M.T. McManus, D. Ruggero, A. Goga, et al. 2012. IRE1a cleaves select microRNAs during ER stress to derepress translation of proapoptotic Caspase-2. Science. 338:818-822. http://dx.doi.org/10.1126/science.1226191
83. Vander Heiden, M.G., L.C. Cantley, and C.B. Thompson. 2009. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 324:1029-1033. http://dx.doi.org/10.1126/science.1160809
84. Walter, P., and D. Ron. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 334:1081-1086. http://dx.doi.org/10.1126/science.1209038
85. Walter, L., A. Baruah, H.W. Chang, H.M. Pace, and S.S. Lee. 2011. The homeobox protein CEH-23 mediates prolonged longevity in response to impaired mitochondrial electron transport chain in C. elegans. PLoS Biol. 9:e1001084. http://dx.doi.org/10.1371/journal.pbio.1001084
86. Wang, X., J. Venable, P. LaPointe, D.M. Hutt, A.V. Koulov, J. Coppinger, C. Gurkan, W. Kellner, J. Matteson, H. Plutner, et al. 2006. Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell. 127:803-815. http://dx.doi.org/10.1016/j.cell.2006.09.043
87. Way, S.W., J.R. Podojil, B.L. Clayton, A. Zaremba, T.L. Collins, R.B. Kunjamma, A.P. Robinson, P. Brugarolas, R.H. Miller, S.D. Miller, and B. Popko. 2015. Pharmaceutical integrated stress response enhancement protects oligodendrocytes and provides a potential multiple sclerosis therapeutic. Nat. Commun. 6:6532. http://dx.doi.org/10.1038/ncomms7532
88. Westerheide, S.D., J. Anckar, S.M. Stevens Jr., L. Sistonen, and R.I. Morimoto. 2009. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science. 323:1063-1066. http://dx.doi.org/10.1126/science.1165946
89. Wright, G., K. Terada, M. Yano, I. Sergeev, and M. Mori. 2001. Oxidative stress inhibits the mitochondrial import of preproteins and leads to their degradation. Exp. Cell Res. 263:107-117. http://dx.doi.org/10.1006/excr.2000.5096
90. Xiao, X., X. Zuo, A.A. Davis, D.R. McMillan, B.B. Curry, J.A. Richardson, and I.J. Benjamin. 1999. HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J. 18:5943-5952. http://dx.doi.org/10.1093/emboj/18.21.5943
91. Yoneda, T., C. Benedetti, F. Urano, S.G. Clark, H.P. Harding, and D. Ron. 2004. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J. Cell Sci. 117:4055-4066. http://dx.doi.org/10.1242/jcs.01275
92. Yoshida, H., T. Matsui, A. Yamamoto, T. Okada, and K. Mori. 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. http://dx.doi.org/10.1016/S0092-8674(01)00611-0
93. Zou, J., Y. Guo, T. Guettouche, D.F. Smith, and R. Voellmy. 1998. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell. 94:471-480. http://dx.doi.org/10.1016/S0092-8674(00)81588-3