Redox controls UPR to control redox

Journal of Cell Science

Volumn 127, Issue 17, 2014, Pages 3649-3658

  Eletto, Davide ^a   Chevet, Eric ^b   Argon, Yair ^a   Appenzeller Herzog, Christian ^c  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Endoplasmic reticulum; Endoplasmic reticulum stress; Mitochondria; Protein disulfide isomerase; Reactive oxygen species; Unfolded protein response

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ANIMAL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMAN; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PHYSIOLOGY; UNFOLDED PROTEIN RESPONSE;

ANIMALS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; MITOCHONDRIA; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; UNFOLDED PROTEIN RESPONSE;

EID: 84906877433     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.153643     Document Type: Note

References (121)

1. Adler, V., Yin, Z., Fuchs, S. Y., Benezra, M., Rosario, L., Tew, K. D., Pincus, M. R., Sardana, M., Henderson, C. J., Wolf, C. R. et al. (1999). Regulation of JNK signaling by GSTp. EMBO J. 18, 1321-1334
2. Alzayady, K. J., Chandrasekhar, R. and Yule, D. I. (2013). Fragmented inositol 1,4,5-trisphosphate receptors retain tetrameric architecture and form functional Ca2+ release channels. J. Biol. Chem. 288, 11122-11134
3. Anelli, T., Bergamelli, L., Margittai, E., Rimessi, A., Fagioli, C., Malgaroli, A., Pinton, P., Ripamonti, M., Rizzuto, R. and Sitia, R. (2012). Ero1α regulates Ca(2+) fluxes at the endoplasmic reticulum-mitochondria interface (MAM) Antioxid. Redox Signal. 16, 1077-1087
4. Appenzeller-Herzog, C. (2011). Glutathione- and non-glutathione-based oxidant control in the endoplasmic reticulum. J. Cell Sci. 124, 847-855
5. Appenzeller-Herzog, C. and Ellgaard, L. (2008). The human PDI family: versatility packed into a single fold. Biochim. Biophys. Acta 1783, 535-548
6. Araki, K., Iemura, S., Kamiya, Y., Ron, D., Kato, K., Natsume, T. and Nagata, K (2013). Ero1-α and PDIs constitute a hierarchical electron transfer network of endoplasmic reticulum oxidoreductases. J. Cell Biol. 202, 861-874
7. Austgen, K., Johnson, E. T., Park, T. J., Curran, T. and Oakes, S. A. (2011). The adaptor protein CRK is a pro-apoptotic transducer of endoplasmic reticulum stress. Nat. Cell Biol. 14, 87-92
8. Avezov, E., Cross, B. C., Kaminski Schierle, G. S., Winters, M., Harding, H. P., Melo, E. P., Kaminski, C. F. and Ron, D. (2013). Lifetime imaging of a fluorescent protein sensor reveals surprising stability of ER thiol redox. J. Cell Biol. 201, 337-349
9. Awazawa, M., Futami, T., Sakada, M., Kaneko, K., Ohsugi, M., Nakaya, K., Terai, A., Suzuki, R., Koike, M., Uchiyama, Y. et al. (2014). Deregulation of pancreas-specific oxidoreductin ERO1β in the pathogenesis of diabetes mellitus. Mol. Cell. Biol. 34, 1290-1299
10. Back, S. H., Scheuner, D., Han, J., Song, B., Ribick, M., Wang, J., Gildersleeve, R. D., Pennathur, S. and Kaufman, R. J. (2009). Translation attenuation through eIF2alpha phosphorylation prevents oxidative stress and maintains the differentiated state in beta cells. Cell Metab. 10, 13-26
11. Bansaghi, S., Golenar, T., Madesh, M., Csordas, G., Ramachandrarao, S., Sharma, K., Yule, D. I., Joseph, S. K. and Hajnoczky, G. (2014). Isoform- and species-specific control of inositol 1,4,5-trisphosphate (IP3) receptors by reactive oxygen species. J. Biol. Chem. 289, 8170-8181
12. Belal, C., Ameli, N. J., El Kommos, A., Bezalel, S., Al'Khafaji, A. M., Mughal, M. R., Mattson, M. P., Kyriazis, G. A., Tyrberg, B. and Chan, S. L. (2012). The homocysteine-inducible endoplasmic reticulum (ER) stress protein Herp counteracts mutant a-synuclein-induced ER stress via the homeostatic regulation of ER-resident calcium release channel proteins. Hum. Mol. Genet 21, 963-977
13. Berridge, M. J., Bootman, M. D. and Roderick, H. L. (2003). Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529
14. Birk, J., Meyer, M., Aller, I., Hansen, H. G., Odermatt, A., Dick, T. P., Meyer, A. J. and Appenzeller-Herzog, C. (2013). Endoplasmic reticulum: reduced and oxidized glutathione revisited. J. Cell Sci. 126, 1604-1617
15. Boehning, D., Patterson, R. L., Sedaghat, L., Glebova, N. O., Kurosaki, T. and Snyder, S. H. (2003). Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat. Cell Biol. 5, 1051-1061
16. Bulleid, N. J. and Ellgaard, L. (2011). Multiple ways to make disulfides. Trends Biochem. Sci. 36, 485-492
17. 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
18. Cardozo, A. K., Ortis, F., Storling, J., Feng, Y. M., Rasschaert, J., Tonnesen, M., Van Eylen, F., Mandrup-Poulsen, T., Herchuelz, A. and Eizirik, D. L (2005). Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic beta-cells. Diabetes 54, 452-461
19. Chami, M., Oule' s, B., Szabadkai, G., Tacine, R., Rizzuto, R. and Paterlini-Bréchot, P. (2008). Role of SERCA1 truncated isoform in the proapoptotic calcium transfer from ER to mitochondria during ER stress. Mol. Cell 32, 641-651
20. Csordás, G., Renken, C., Várnai, P., Walter, L., Weaver, D., Buttle, K. F., Balla, T., Mannella, C. A. and Hajnóczky, G. (2006). Structural and functional features and significance of the physical linkage between ER and mitochondria J. Cell Biol. 174, 915-921
21. Cullinan, S. B. and Diehl, J. A. (2004). PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. J. Biol. Chem. 279, 20108-20117
22. Cunha, D. A., Igoillo-Esteve, M., Gurzov, E. N., Germano, C. M., Naamane, N., Marhfour, I., Fukaya, M., Vanderwinden, J. M., Gysemans, C., Mathieu, C et al. (2012). Death protein 5 and p53-upregulated modulator of apoptosis mediate the endoplasmic reticulum stress-mitochondrial dialog triggering lipotoxic rodent and human β-cell apoptosis. Diabetes 61, 2763-2775
23. Czabotar, P. E., Lessene, G., Strasser, A. and Adams, J. M. (2014). Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy Nat. Rev. Mol. Cell Biol. 15, 49-63
24. Dejeans, N., Tajeddine, N., Beck, R., Verrax, J., Taper, H., Gailly, P. and Calderon, P. B. (2010). Endoplasmic reticulum calcium release potentiates the ER stress and cell death caused by an oxidative stress in MCF-7 cells Biochem. Pharmacol. 79, 1221-1230
25. DuRose, J. B., Tam, A. B. and Niwa, M. (2006). Intrinsic capacities of molecular sensors of the unfolded protein response to sense alternate forms of endoplasmic reticulum stress. Mol. Biol. Cell 17, 3095-3107
26. Eletto, D., Eletto, D., Dersh, D., Gidalevitz, T. and Argon, Y. (2014). Protein disulfide isomerase A6 controls the decay of IRE1a signaling via disulfidedependent association. Mol. Cell 53, 562-576
27. Enyedi, B., Várnai, P. and Geiszt, M. (2010). Redox state of the endoplasmic reticulum is controlled by Ero1L-alpha and intraluminal calcium. Antioxid. Redox Signal. 13, 721-729
28. Figueira, T. R., Barros, M. H., Camargo, A. A., Castilho, R. F., Ferreira, J. C., Kowaltowski, A. J., Sluse, F. E., Souza-Pinto, N. C. and Vercesi, A. E. (2013) Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health. Antioxid. Redox Signal. 18, 2029-2074
29. Fu, S., Yang, L., Li, P., Hofmann, O., Dicker, L., Hide, W., Lin, X., Watkins, S. M., Ivanov, A. R. and Hotamisligil, G. S. (2011). Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 473, 528-531
30. Galluzzi, L., Vitale, I., Abrams, J. M., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., Dawson, T. M., Dawson, V. L., El-Deiry, W. S., Fulda, S et al. (2012). Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 19, 107-120
31. Garg, A. D. and Agostinis, P. (2014). ER stress, autophagy and immunogenic cell death in photodynamic therapy-induced anti-cancer immune responses Photochem. Photobiol. Sci. 13, 474-487
32. Gidalevitz, T., Stevens, F. and Argon, Y. (2013). Orchestration of secretory protein folding by ER chaperones. Biochim. Biophys. Acta 1833, 2410-2424
33. Glover-Cutter, K. M., Lin, S. and Blackwell, T. K. (2013). Integration of the unfolded protein and oxidative stress responses through SKN-1/Nrf. PLoS Genet. 9, e1003701
34. Gough, D. R. and Cotter, T. G. (2011). Hydrogen peroxide: a Jekyll and Hyde signalling molecule. Cell Death Dis. 2, e213
35. Han, J., Back, S. H., Hur, J., Lin, Y. H., Gildersleeve, R., Shan, J., Yuan, C. L., Krokowski, D., Wang, S., Hatzoglou, M. et al. (2013). ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol. 15, 481-490
36. Hara, T., Mahadevan, J., Kanekura, K., Hara, M., Lu, S. and Urano, F. (2014) Calcium efflux from the endoplasmic reticulum leads to β-cell death Endocrinology 155, 758-768
37. Harding, H. P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M. and Ron, D. (2000a). Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6, 1099-1108
38. Harding, H. P., Zhang, Y., Bertolotti, A., Zeng, H. and Ron, D. (2000b). Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5, 897-904
39. Harding, H. P., Zhang, Y., Zeng, H., Novoa, I., Lu, P. D., Calfon, M., Sadri, N., Yun, C., Popko, B., Paules, R. et al. (2003). An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619-633
40. Hayashi, T. and Su, T. P. (2007). Sigma-1 receptor chaperones at the ERmitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 131, 596-610
41. Haynes, C. M., Titus, E. A. and Cooper, A. A. (2004). Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol. Cell 15, 767-776
42. Haze, K., Yoshida, H., Yanagi, H., Yura, T. and Mori, K. (1999). Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol Cell 10, 3787-3799
43. Hetz, C. (2012). The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13, 89-102
44. Hetz, C., Bernasconi, P., Fisher, J., Lee, A. H., Bassik, M. C., Antonsson, B., Brandt, G. S., Iwakoshi, N. N., Schinzel, A., Glimcher, L. H. et al. (2006) Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 312, 572-576
45. Higa, A., Taouji, S., Lhomond, S., Jensen, D., Fernandez-Zapico, M. E., Simpson, J. C., Pasquet, J. M., Schekman, R. and Chevet, E. (2014) Endoplasmic reticulum stress-activated transcription factor ATF6α requires the disulfide isomerase PDIA5 to modulate chemoresistance. Mol. Cell. Biol. 34, 1839-1849
46. 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
47. Horibe, T., Gomi, M., Iguchi, D., Ito, H., Kitamura, Y., Masuoka, T., Tsujimoto, I., Kimura, T. and Kikuchi, M. (2004). Different contributions of the three CXXC motifs of human protein-disulfide isomerase-related protein to isomerase activity and oxidative refolding. J. Biol. Chem. 279, 4604-4611
48. Inoue, T. and Suzuki-Karasaki, Y. (2013). Mitochondrial superoxide mediates mitochondrial and endoplasmic reticulum dysfunctions in TRAIL-induced apoptosis in Jurkat cells. Free Radic. Biol. Med. 61, 273-284
49. Iwasawa, R., Mahul-Mellier, A. L., Datler, C., Pazarentzos, E. and Grimm, S (2011). Fis1 and Bap31 bridge the mitochondria-ER interface to establish a platform for apoptosis induction. EMBO J. 30, 556-568
50. Jansen, G., Määttänen, P., Denisov, A. Y., Scarffe, L., Schade, B., Balghi, H., Dejgaard, K., Chen, L. Y., Muller, W. J., Gehring, K. et al. (2012). An interaction map of endoplasmic reticulum chaperones and foldases. Mol. Cell Proteomics 11, 710-723
51. Jarvis, R. M., Hughes, S. M. and Ledgerwood, E. C. (2012). Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells. Free Radic. Biol. Med. 53, 1522-1530
52. Jessop, C. E., Watkins, R. H., Simmons, J. J., Tasab, M. and Bulleid, N. J. (2009). Protein disulphide isomerase family members show distinct substrate specificity: P5 is targeted to BiP client proteins. J. Cell Sci. 122, 4287-4295
53. Jin, H. O., Seo, S. K., Kim, Y. S., Woo, S. H., Lee, K. H., Yi, J. Y., Lee, S. J., Choe, T. B., Lee, J. H., An, S. et al. (2011). TXNIP potentiates Redd1-induced mTOR suppression through stabilization of Redd1. Oncogene 30, 3792-3801
54. Kim, Y. K. and Lee, A. S. (1987). Transcriptional activation of the glucoseregulated protein genes and their heterologous fusion genes by betamercaptoethanol Mol. Cell. Biol. 7, 2974-2976
55. Kim, I., Shu, C. W., Xu, W., Shiau, C. W., Grant, D., Vasile, S., Cosford, N. D and Reed, J. C. (2009). Chemical biology investigation of cell death pathways activated by endoplasmic reticulum stress reveals cytoprotective modulators of ASK1. J. Biol. Chem. 284, 1593-1603
56. Kiviluoto, S., Vervliet, T., Ivanova, H., Decuypere, J. P., De Smedt, H., Missiaen, L., Bultynck, G. and Parys, J. B. (2013). Regulation of inositol 1,4,5-trisphosphate receptors during endoplasmic reticulum stress. Biochim. Biophys Acta 1833, 1612-1624
57. Kojer, K. and Riemer, J. (2014). Balancing oxidative protein folding: The influences of reducing pathways on disulfide bond formation. Biochim. Biophys Acta 1844, 1383-1390
58. Kumar, C., Igbaria, A., D'Autreaux, B., Planson, A. G., Junot, C., Godat, E., Bachhawat, A. K., Delaunay-Moisan, A. and Toledano, M. B. (2011) Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control. EMBO J. 30, 2044-2056
59. Lee, K., Tirasophon, W., Shen, X., Michalak, M., Prywes, R., Okada, T., Yoshida, H., Mori, K. and Kaufman, R. J. (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
60. Lei, K. and Davis, R. J. (2003). JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc. Natl. Acad. Sci. USA 100, 2432-2437
61. Lerner, A. G., Upton, J. P., Praveen, P. V., Ghosh, R., Nakagawa, Y., Igbaria, A., Shen, S., Nguyen, V., Backes, B. J., Heiman, M. et al. (2012). IRE1a induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab 16, 250-264
62. Li, J., Lee, B. and Lee, A. S. (2006). Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J. Biol. Chem. 281, 7260-7270
63. Li, G., Mongillo, M., Chin, K. T., Harding, H., Ron, D., Marks, A. R. and Tabas, I (2009). Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. J. Cell Biol 186, 783-792
64. Li, G., Scull, C., Ozcan, L. and Tabas, I. (2010a). NADPH oxidase links endoplasmic reticulum stress, oxidative stress, and PKR activation to induce apoptosis. J. Cell Biol. 191, 1113-1125
65. Li, H., Korennykh, A. V., Behrman, S. L. and Walter, P. (2010b). Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering. Proc Natl. Acad. Sci. USA 107, 16113-16118
66. Liu, C. Y., Xu, Z. and Kaufman, R. J. (2003). Structure and intermolecular interactions of the luminal dimerization domain of human IRE1alpha. J. Biol Chem. 278, 17680-17687
67. Liyanage, N. P., Fernando, M. R. and Lou, M. F. (2007). Regulation of the bioavailability of thioredoxin in the lens by a specific thioredoxin-binding protein (TBP-2). Exp. Eye Res. 85, 270-279
68. Ma, Q. (2013). Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol Toxicol. 53, 401-426
69. Malhotra, J. D., Miao, H., Zhang, K., Wolfson, A., Pennathur, S., Pipe, S. W and Kaufman, R. J. (2008). Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc. Natl. Acad. Sci. USA 105, 18525-18530
70. Marciniak, S. J., Yun, C. Y., Oyadomari, S., Novoa, I., Zhang, Y., Jungreis, R., Nagata, K., Harding, H. P. and Ron, D. (2004). CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18, 3066-3077
71. Matsuzawa, A. and Ichijo, H. (2008). Redox control of cell fate by MAP kinase: physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochim Biophys. Acta 1780, 1325-1336
72. Maurel, M., Chevet, E., Tavernier, J. and Gerlo, S. (2014). Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem. Sci. 39, 245-254
73. McCullough, K. D., Martindale, J. L., Klotz, L. O., Aw, T. Y. and Holbrook, N. J (2001). Gadd153 sensitizes cells to endoplasmic reticulum stress by downregulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21, 1249-1259
74. Meunier, L., Usherwood, Y. K., Chung, K. T. and Hendershot, L. M. (2002). A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell 13, 4456-4469
75. Montero, D., Tachibana, C., Rahr Winther, J. and Appenzeller-Herzog, C (2013). Intracellular glutathione pools are heterogeneously concentrated. Redox Biol. 1, 508-513
76. Moore, C. E., Omikorede, O., Gomez, E., Willars, G. B. and Herbert, T. P (2011). PERK activation at low glucose concentration is mediated by SERCA pump inhibition and confers preemptive cytoprotection to pancreatic β-cells Mol. Endocrinol. 25, 315-326
77. Mori, T., Hayashi, T., Hayashi, E. and Su, T. P. (2013). Sigma-1 receptor chaperone at the ER-mitochondrion interface mediates the mitochondrion-ERnucleus signaling for cellular survival. PLoS ONE 8, e76941
78. Nadanaka, S., Okada, T., Yoshida, H. and Mori, K. (2007). Role of disulfide bridges formed in the luminal domain of ATF6 in sensing endoplasmic reticulum stress. Mol. Cell. Biol. 27, 1027-1043
79. Namba, T., Tian, F., Chu, K., Hwang, S. Y., Yoon, K. W., Byun, S., Hiraki, M., Mandinova, A. and Lee, S. W. (2013). CDIP1-BAP31 complex transduces apoptotic signals from endoplasmic reticulum to mitochondria under endoplasmic reticulum stress. Cell Rep. 5, 331-339
80. Nishiyama, A., Matsui, M., Iwata, S., Hirota, K., Masutani, H., Nakamura, H., Takagi, Y., Sono, H., Gon, Y. and Yodoi, J. (1999). Identification of thioredoxin-binding protein-2/vitamin D(3) up-regulated protein 1 as a negative regulator of thioredoxin function and expression. J. Biol. Chem. 274, 21645-21650
81. Oslowski, C. M., Hara, T., O'Sullivan-Murphy, B., Kanekura, K., Lu, S., Hara, M., Ishigaki, S., Zhu, L. J., Hayashi, E., Hui, S. T. et al. (2012). Thioredoxininteracting protein mediates ER stress-induced β cell death through initiation of the inflammasome. Cell Metab. 16, 265-273
82. Parys, J. B. (2014). The IP3 receptor as a hub for Bcl-2 family proteins in cell death control and beyond. Sci. Signal. 7, pe4
83. Pedruzzi, E., Guichard, C., Ollivier, V., Driss, F., Fay, M., Prunet, C., Marie, J. C., Pouzet, C., Samadi, M., Elbim, C. et al. (2004). NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol. Cell. Biol. 24, 10703-10717
84. Persson, T., Popescu, B. O. and Cedazo-Minguez, A. (2014). Oxidative stress in Alzheimer's disease: why did antioxidant therapy fail? Oxid. Med. Cell. Longev 2014, 427318
85. Putcha, G. V., Le, S., Frank, S., Besirli, C. G., Clark, K., Chu, B., Alix, S., Youle, R. J., LaMarche, A., Maroney, A. C. et al. (2003). JNK-mediated BIM phosphorylation potentiates BAX-dependent apoptosis. Neuron 38, 899-914
86. 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
87. Ramming, T. and Appenzeller-Herzog, C. (2012). The physiological functions of mammalian endoplasmic oxidoreductin 1: on disulfides and more. Antioxid Redox Signal. 16, 1109-1118
88. Ramming, T. and Appenzeller-Herzog, C. (2013). Destroy and exploit: catalyzed removal of hydroperoxides from the endoplasmic reticulum. Int. J. Cell Biol 2013, 180906
89. Ramming, T., Hansen, H. G., Nagata, K., Ellgaard, L. and Appenzeller-Herzog, C. (2014). GPx8 peroxidase prevents leakage of H2O2 from the endoplasmic reticulum. Free Radic. Biol. Med. 70, 106-116
90. 2+ signaling. Histol. Histopathol. 29, 543-552
91. Rizzuto, R., De Stefani, D., Raffaello, A. and Mammucari, C. (2012) Mitochondria as sensors and regulators of calcium signalling. Nat. Rev. Mol Cell Biol. 13, 566-578
92. Rodriguez, D. A., Zamorano, S., Lisbona, F., Rojas-Rivera, D., Urra, H., Cubillos-Ruiz, J. R., Armisen, R., Henriquez, D. R., Cheng, E. H., Letek, M et al. (2012). BH3-only proteins are part of a regulatory network that control the sustained signalling of the unfolded protein response sensor IRE1α. EMBO J 31, 2322-2335
93. Rong, Y. P., Barr, P., Yee, V. C. and Distelhorst, C. W. (2009). Targeting Bcl-2 based on the interaction of its BH4 domain with the inositol 1,4,5-trisphosphate receptor. Biochim. Biophys. Acta 1793, 971-978
94. Rutkevich, L. A., Cohen-Doyle, M. F., Brockmeier, U. and Williams, D. B (2010). Functional relationship between protein disulfide isomerase family members during the oxidative folding of human secretory proteins. Mol. Biol Cell 21, 3093-3105
95. Saitoh, M., Nishitoh, H., Fujii, M., Takeda, K., Tobiume, K., Sawada, Y., Kawabata, M., Miyazono, K. and Ichijo, H. (1998). Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17, 2596-2606
96. Sandow, J. J., Dorstyn, L., O'Reilly, L. A., Tailler, M., Kumar, S., Strasser, A and Ekert, P. G. (2014). ER stress does not cause upregulation and activation of caspase-2 to initiate apoptosis. Cell Death Differ. 21, 475-480
97. Santos, C. X., Tanaka, L. Y., Wosniak, J. and Laurindo, F. R. (2009) Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid. Redox Signal 11, 2409-2427
98. Schafer, F. Q. and Buettner, G. R. (2001). Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Free Radic. Biol. Med. 30, 1191-1212
99. Tabas, I. and Ron, D. (2011). Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 13, 184-190
100. Tavender, T. J. and Bulleid, N. J. (2010). Peroxiredoxin IV protects cells from oxidative stress by removing H2O2 produced during disulphide formation J. Cell Sci. 123, 2672-2679
101. Tong, X., Evangelista, A. and Cohen, R. A. (2010). Targeting the redox regulation of SERCA in vascular physiology and disease. Curr. Opin Pharmacol. 10, 133-138
102. Tu, B. P. and Weissman, J. S. (2004). Oxidative protein folding in eukaryotes: mechanisms and consequences. J. Cell Biol. 164, 341-346
103. Tufo, G., Jones, A. W., Wang, Z., Hamelin, J., Tajeddine, N., Esposti, D. D., Martel, C., Boursier, C., Gallerne, C., Migdal, C. et al. (2014). The protein disulfide isomerases PDIA4 and PDIA6 mediate resistance to cisplatin-induced cell death in lung adenocarcinoma. Cell Death Differ. 21, 685-695
104. Uehara, T., Nakamura, T., Yao, D., Shi, Z. Q., Gu, Z., Ma, Y., Masliah, E., Nomura, Y. and Lipton, S. A. (2006). S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441, 513-517
105. Upton, J. P., Austgen, K., Nishino, M., Coakley, K. M., Hagen, A., Han, D., Papa, F. R. and Oakes, S. A. (2008). Caspase-2 cleavage of BID is a critical apoptotic signal downstream of endoplasmic reticulum stress. Mol. Cell. Biol 28, 3943-3951
106. 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
107. van Vliet, A. R., Verfaillie, T. and Agostinis, P. (2014). New functions of mitochondria associated membranes in cellular signaling. Biochim. Biophys Acta. [Epub ahead of print] doi:10.1016/j.bbamcr.2014.03.009
108. Verfaillie, T., Rubio, N., Garg, A. D., Bultynck, G., Rizzuto, R., Decuypere, J. P., Piette, J., Linehan, C., Gupta, S., Samali, A. et al. (2012). PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress. Cell Death Differ. 19, 1880-1891
109. Vinaik, R., Kozlov, G. and Gehring, K. (2013). Structure of the non-catalytic domain of the protein disulfide isomerase-related protein (PDIR) reveals function in protein binding. PLoS ONE 8, e62021
110. Vincenz, L. and Hartl, F. U. (2014). Sugarcoating ER Stress. Cell 156, 1125-1127
111. Wali, J. A., Rondas, D., McKenzie, M. D., Zhao, Y., Elkerbout, L., Fynch, S., Gurzov, E. N., Akira, S., Mathieu, C., Kay, T. W. et al. (2014). The proapoptotic BH3-only proteins Bim and Puma are downstream of endoplasmic reticulum and mitochondrial oxidative stress in pancreatic islets in response to glucotoxicity Cell Death Dis. 5, e1124
112. Walter, P. and Ron, D. (2011). The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086
113. Watson, J. D. (2014). Type 2 diabetes as a redox disease. Lancet 383, 841-843
114. Wei, P. C., Hsieh, Y. H., Su, M. I., Jiang, X., Hsu, P. H., Lo, W. T., Weng, J. Y., Jeng, Y. M., Wang, J. M., Chen, P. L. et al. (2012). Loss of the oxidative stress sensor NPGPx compromises GRP78 chaperone activity and induces systemic disease. Mol. Cell 48, 747-759
115. Win, S., Than, T. A., Fernandez-Checa, J. C. and Kaplowitz, N. (2014). JNK interaction with Sab mediates ER stress induced inhibition of mitochondrial respiration and cell death. Cell Death Dis. 5, e989
116. Wright, J., Birk, J., Haataja, L., Liu, M., Ramming, T., Weiss, M. A., Appenzeller-Herzog, C. and Arvan, P. (2013). Endoplasmic reticulum oxidoreductin-1α (Ero1α) improves folding and secretion of mutant proinsulin and limits mutant proinsulin-induced endoplasmic reticulum stress. J. Biol Chem. 288, 31010-31018
117. Wu, T., Zhao, F., Gao, B., Tan, C., Yagishita, N., Nakajima, T., Wong, P. K., Chapman, E., Fang, D. and Zhang, D. D. (2014). Hrd1 suppresses Nrf2-mediated cellular protection during liver cirrhosis. Genes Dev. 28, 708-722
118. Xu, S., Sankar, S. and Neamati, N. (2014). Protein disulfide isomerase: a promising target for cancer therapy. Drug Discov. Today 19, 222-240
119. Yamamoto, K., Ichijo, H. and Korsmeyer, S. J. (1999). BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol. 19, 8469-8478
120. 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
121. Zhou, R., Tardivel, A., Thorens, B., Choi, I. and Tschopp, J. (2010) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 11, 136-140