Endoplasmic reticulum: Stress, signalling and apoptosis

Current Science

Volumn 93, Issue 12, 2007, Pages 1684-1696

  Hussain, Syed G ^a   Ramaiah, Kolluru V A ^a  

^a UNIVERSITY OF HYDERABAD   (India)

Author keywords

Apoptosis; Endoplasmic reticulum; Signalling; Stress

Indexed keywords

MAMMALIA;

EID: 38149122020     PISSN: 00113891     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (100)

1. Sitia, R. and Braakman, I., Quality control in the endoplasmic reticulum protein factory. Nature, 2003, 426, 891-894.
2. Selkoe, D. J., Folding proteins in fatal ways. Nature, 2003, 426, 900-904.
3. Tu, B. P. and Weissman, J. S., Oxidative protein folding in eukaryotes: Mechanisms and consequences. J. Cell Biol., 2004, 164, 341-346.
4. 2+ store: A view from the lumen. Trends Biochem. Sci., 1998, 23, 10-14.
5. Hendershot, L. M., The ER function BiP is a master regulator of ER function. Mt. Sinai J. Med., 2004, 71, 289-297.
6. Zhao, L. and Ackerman, S. L., Endoplasmic reticulum stress in health and disease. Curr. Opin. Cell Biol., 2006, 18, 444-452.
7. Kaufman, R. J., Stress signalling from the lumen of the endoplasmic reticulum: Coordination of gene transcriptional and translational controls. Genes Dev., 1999, 13, 1211-1233.
8. Lee, A. S., Coordinated regulation of a set of genes by glucose and calcium ionophore in mammalian cells. Trends Biochem. Sci., 1987, 12, 20-24.
9. Ng, D. T., Watowich, S. S. and Lamb, R. A., Analysis in vivo of GRP78-BiP/substrate interactions and their role in induction of the GRP78-BiP gene. Mol. Biol. Cell., 1992, 3, 143-155.
10. Wu, J. and Kaufman, R. J., From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ., 2006, 13, 374-384.
11. Tirasophon, W., Welihinda, A. A. and Kaufman, R. J., A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev., 1998, 12, 1812-1824.
12. Haze, K., Yoshida, H., Yanagi, H., Yura, T. and Mori, K., 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.
13. Shi, Y., Vattem, K. M., Sood, R., An, J., Liang, J., Stramm, L. and Wek, R. C., Identification and characterization of pancreatic eukaryotic initiation factor 2 α-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol., 1998, 18, 7499-7509.
14. Harding, H. P., Zhang, Y. and Ron, D., Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature, 1999, 397, 271-274.
15. Bertolotti, A., Zhang, Y., Hendershot, L. M., Harding, H. P. and Ron, D., Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nature Cell. Biol., 2000, 2, 326-332.
16. Dorner, A. J., Wasley, L. C. and Kaufman, R. J., Overexpression of GRP78 mitigates stress induction of glucose regulated proteins and blocks secretion of selective proteins in Chinese hamster ovary cells. EMBO J., 1992, 11, 1563-1571.
17. Lee, A. H., Iwakoshi, N, N., Anderson, K. C. and Glimcher, L. H., Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. Proc. Natl. Acad. Sci. USA, 2003, 100, 90946-90951.
18. Wang, X. Z., Harding, H. P., Zhang, Y., Jolicoeur, E. M., Kuroda, M. and Ron, D., Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J., 1998, 17, 5708-5717.
19. Bertolotti, A. et al., Increased sensitivity to dextran sodium sulfate colitis in IRE1 β-deficient mice. J. Clin. Invest., 2001, 107, 585-593.
20. Credle, J. J., Finer-Moore, J. S., Papa, F. R., Stroud, R. M. and Walter, P., On the mechanism of sensing unfolded protein in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA, 2005, 102, 18773-18784.
21. Zhou, J., Liu, C. Y., Back, S. H., Clark, R. L., Peisach, D., Xu, Z. and Kaufman, R. J., 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. USA, 2006, 103, 14343-14348.
22. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. and Mori, K., 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.
23. Sidrauski, C., Cox, J. S. and Walter, P., tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell, 1996, 87, 405-413.
24. Lee, K. et al., IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signalling the unfolded protein response. Genes Dev., 2002, 16, 452-466.
25. Lee, A. H., Iwakoshi, N. N. and Glimcher, L. H., XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol., 2003, 23, 7448-7459.
26. Yoshida, H., Matsui, T., Hosokawa, N., Kaufman, R. J., Nagata, K. and Mori, K., A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell, 2003, 4, 265-271.
27. Sriburi, R., Jackowski, S., Mori, K. and Brewer, J. W., XBP1: A link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol., 2004, 167, 35-41.
28. Ramaiah, K. V., Davies, M. V., Chen, J. J. and Kaufman, R. J., Expression of mutant eukaryotic initiation factor 2 alpha subunit (eIF-2 alpha) reduces inhibition of guanine nucleotide exchange activity of eIF-2B mediated by eIF-2 alpha phosphorylation. Mol. Cell. Biol., 1994, 14, 4546-4553.
29. Harding, H. P. et al., An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell, 2003, 11, 619-633.
30. Oyadomari, S. and Mori, M., Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell. Death Differ., 2004, 11, 381-389.
31. Cullinan, S. B. and Diehl, J. A., Coordination of ER and oxidative stress signalling: The PERK/Nrf2 signaling pathway. Int J. Biochem. Cell Biol., 2006, 38, 317-332.
32. Schroder, M. and Kaufman, R. J., ER stress and the unfolded protein response. Mutat. Res., 2005, 569, 29-63.
33. Nadanaka, S., Yoshida, H. and Mori, K., Reduction of disulphide bridges in the lumenal domain of ATF6 in response to glucose starvation. Cell Structure Funct., 2006, 31, 127-134.
34. Hong, M., Luo, S., Baumeister, P., Huang, J. M., Gogia, R. K., Li, M. and Lee, A. S., Underglycosylation of ATF6 as a novel sensing mechanism for activation of the unfolded protein response. J. Biol. Chem., 2004, 279, 11354-11363.
35. Yoshida, H., ER stress and diseases. FEBS J., 2007, 274, 630-658.
36. Thuerauf, D. J., Marcinko, M., Belmont, P. J. and Glembotski, C. C., Effects of the isoform-specific characteristics of ATF6alpha and ATF6beta on ER stress response gene expression and cell viability. J. Biol Chem., 2007 (Epub ahead of print).
37. Kaufman, R. J., Scheuner, D., Schröder, M., Shen, X., Lee, K., Liu, C. Y. and Arnold, S. M., The unfolded protein response in nutrient sensing and differentiation. Nature Rev. Mol. Cell Biol., 2002, 3, 411-421.
38. Luo, S., Mao, C., Lee, B. and Lee, A. S., GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol. Cell. Biol., 2006, 26, 5688-5697.
39. Iwakoshi, N. N., Lee, A. H., Vallabhajosyula, P., Otipoby, K. L., Rajewsky, K. and Glimcher, L. H., Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nature Immunol., 2003, 4, 321-329.
40. Marciniak, S. J. and Ron, D., Endoplasmic reticulum stress signalling in disease. Physiol. Rev., 2006, 86, 1133-1149.
41. Koumenis, C., ER stress, hypoxia tolerance and tumour progression. Curr. Mol. Med., 2006, 6, 55-69.
42. Szegezdi, E., Logue, S. E., Gorman, A. M. and Samali, A., Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep., 2006, 7, 880-885.
43. Galonek, H. L. and Hardwick, J. M., Upgrading the BCL-2 network. Nature Cell Biol., 2006, 8, 1317-1319.
44. Oakes, S. A., Lin, S. S. and Bassik, M. C., The control of endoplasmic reticulum-initiated apoptosis by the BCL-2 family of proteins. Curr. Mol. Med., 2006, 6, 99-109.
45. Häcki, J., Egger, L., Monney, L., Conus, S., Rossé, T., Fellay, I. and Borner, C., Apoptotic crosstalk between the endoplasmic reticulum and mitochondria controlled by Bcl-2. Oncogene, 2000, 19, 2286-2295.
46. Thomenius, M. J. and Distelhorst, C. W., Bcl-2 on the endoplasmic reticulum: Protecting the mitochondria from a distance. J. Cell Sci., 2003, 116, 4493-4499.
47. Lee, G. H. et al., Bax inhibitor-1 regulates endoplasmic reticulum stress-associated reactive oxygen species and heme oxygenase-I expression. J. Biol. Chem., 2007 (Epub ahead of print).
48. Wei, M. C. et al., Pro-apoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science, 2001, 292, 727-730.
49. Li, J., Lee, B. and Lee, A. S., Endoplasmic reticulum stress-induced apoptosis: Multiple pathways and activation of p53-upregulated modulator of apoptosis (PUMA) and NOXA by p53. J. Biol. Chem., 2006, 281, 7260-7270.
50. Morishima, N., Nakanishi, K., Tsuchiya, K., Shibata, T. and Seiwa, E., Translocation of Bim to the endoplasmic reticulum (ER) mediates ER stress signalling for activation of caspase-12 during ER stress-induced apoptosis. J. Biol. Chem., 2004, 279, 50375-50381.
51. Berridge, M. J., Lipp, P. and Bootman, M. D., The versatility and universality of calcium signalling. Nature Rev. Mol. Cell Biol., 2000, 1, 11-21.
52. Camello, C., Lomax, R., Petersen, O. H. and Tepikin, A. V., Calcium leak from intracellular stores - The enigma of calcium signalling. Cell Calcium, 2002, 32, 355-361.
53. Demaurex, N. and Distelhorst, C., Cell biology. Apoptosis - the calcium connection. Science, 2003, 300, 65-67.
54. 2+ responses. Science, 1998, 280, 1763-1766.
55. 2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: Significance for the molecular mechanism of Bcl-2 action. EMBO J., 2001, 20, 2670-2690.
56. Nakamura, K. et al., Changes in endoplasmic reticulum luminal environment affect cell sensitivity to apoptosis. J. Cell. Biol., 2000, 150, 731-740.
57. Scorrano, L., Penzo, D., Petronilli, V., Pagano, F. and Bernardi, P., Arachidonic acid causes cell death through the mitochondrial permeability transition. Implications for tumour necrosis factor-alpha aopototic signalling. J. Biol. Chem., 2001, 276, 12035-12040.
58. Penzo, D. et al., Arachidonic acid released by phospholipase A(2) activation triggers Ca(2+)-dependent apoptosis through the mitochondrial pathway. J. Biol. Chem., 2004, 279, 25219-25225.
59. 2+ stores. J. Biol. Chem., 2002, 277, 9219-9225.
60. 2+: A control point for apoptosis. Science, 2003, 300, 135-139.
61. Zuppini, A., Groenendyk, J., Cormack, L. A., Shore, G., Opas, M., Bleackley, R. C. and Michalak, M., Calnexin deficiency and endoplasmic reticulum stress-induced apoptosis. Biochemistry, 2002, 41, 2850-2858.
62. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science, 1999, 284, 339-343.
63. Zong, W. X., Li, C., Hatzivassiliou, G., Lindsten, T., Yu, Q. C., Yuan, J. and Thompson, C. B., Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell. Biol., 2003, 162, 59-69.
64. Contreras, J. L. et al., Coupling endoplasmic reticulum stress to cell death program in isolated human pancreatic islets: effects of gene transfer of Bcl-2. Transplant. Int., 2003, 16, 537-542.
65. Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., Harding, H. P. and Ron, D., Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science, 2000, 287, 664-666.
66. Nishitoh, H. et al., ASK1 is essential for JNK/SAPK activation by TRAF2. Mol. Cell, 1998, 2, 389-395.
67. Zhang, C., Kawauchi, J., Adachi, M. T., Hashimoto, Y., Oshiro, S., Aso, T. and Kitajima, S., Activation of JNK and transcriptional repressor ATF3?LRF1 through the IRE1?TRAF2 pathway is implicated in human vascular endothelial cell death by homocysteine. Biochem. Biophys. Res. Commun., 2001, 289, 718-724.
68. Roux, P. P. and Blenis, J., ERK and p38 MAPK-activated protein kinases: A family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev., 2004, 68, 320-344.
69. Hetz, C. et al., Pro-apoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science, 2006, 312, 572-576.
70. 2+ homeostasis and apoptosis. EMBO J., 2004, 23, 1207-1216.
71. Lin, S. S. et al., PP2A regulates BCL-2 phosphorylation and proteasome-mediated degradation at the endoplasmic reticulum. J. Biol. Chem., 2006, 281, 23003-23012.
72. Harding, H. P., Novoa, I. I., Zhang, Y., Zeng, H., Wek, R., Schapira, M. and Ron, D., Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell, 2000, 6, 1099-1108.
73. Scheuner, D. et al., Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell, 2001, 7, 1165-1176.
74. Ohoka, N., Yoshii, S., Hattori, T., Onozaki, K. and Hayashi, H., TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J., 2005, 24, 1243-1255.
75. 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.
76. Novoa, I., Zeng, H., Harding, H. P. and Ron, D., Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J. Cell. Biol., 2001, 153, 1011-1022.
77. Zinszner, H. et al., CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev., 1998, 12, 982-995.
78. Maytin, E. V., Ubeda, M., Lin, J. C. and Habener, J. F., Stress-inducible transcription factor CHOP/gadd153 induces apoptosis in mammalian cells via p38 kinase-dependent and -independent mechanisms. Exp. Cell Res., 2001, 267, 193-204.
79. McCullough, K. D., Martindale, J. L., Klotz, L. O., Aw, Z. Y. and Holbrook, N. J., Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol., 2001, 21, 1249-1259.
80. Aparna, G., Bhuyan, A. K., Sahdev, S., Hasnain, S. E., Kaufman, R. J. and Ramaiah, K. V., Stress-induced apoptosis in Spodoptera frugiperda (Sf9) cells: Baculovirus p35 mitigates eIF2 alpha phosphorylation. Biochemistry, 2003, 42, 15352-15360.
81. Saelens, X., Kalai, M. and Vandenabeele, P., Translation inhibition in apoptosis: Caspase-dependent PKR activation and eIF2-alpha phosphorylation. J. Biol. Chem., 2001, 276, 41620-41628.
82. Wek, R. C., Jiang, H. Y. and Anthony, T. G., Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans., 2006, 34, 7-11.
83. Boyce, M. et al., A selective inhibitor of eIF2α dephosphorylation protects cells from ER stress. Science, 2005, 307, 935-939.
84. -/- mice reveals a role for translational control in secretory cell survival. Mol. Cell, 2001, 7, 1153-1163.
85. Babu, S. V. and Ramaiah, K. V., Type 1 protein phosphatase inhibitors reduce the restoration of guanine nucleotide exchange activity of eukaryotic initiation factor 2B inhibited reticulocyte lysates rescued by hemin. Arch. Biochem. Biophys., 1996, 327, 201-208.
86. He, B., Gross, M. and Roizman, B., The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1 alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA activated protein kinase. Proc. Natl. Acad. Sci. USA, 1997, 94, 843-848.
87. Cnop, M. et al., Selective inhibition of eukaryotic translation initiation factor 2 alpha dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic beta-cell dysfunction and apoptosis. J. Biol. Chem., 2007, 282, 3989-3997.
88. Yan, W., Frank, C. L., Korth, M. J., Sopher, B. L., Novoa, I., Ron, D. and Katze, M. G., Control of PERK eIF2α kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc. Natl. Acad. Sci. USA, 2002, 99, 15920-15925.
89. Ladiges, W. C. et al., Pancreatic β-cell failure and diabetes in mice with a deletion mutation of the endoplasmic reticulum molecular chaperone gene P58IPK. Diabetes, 2005, 54, 1074-1081.
90. Scheuner, D. et al., Double-stranded RNA-dependent protein kinase phosphorylation of the alpha-subunit of eukaryotic translation initiation factor 2 mediates apoptosis. J. Biol. Chem., 2006, 281, 21458-21468.
91. Stephens, S. B., Dodd, R. D., Brewer, J. W., Lager, P. J., Keene, J. D. and Nicchitta, C. V., Stable ribosome binding to the endoplasmic reticulum enables compartment-specific regulation of mRNA translation. Mol. Biol. Cell, 2005, 16, 5819-5831.
92. Jousse, C., Oyadomari, S., Novoa, I., Lu, P., Zhang, Y., Harding, H. P. and Ron, D., Inhibition of a constitutive translation initiation factor 2 alpha phosphatase, CReP, promotes survival of stressed cells. J. Cell. Biol., 2003, 163, 767-775.
93. Latreille, M. and Larose, L., Nck in a complex containing the catalytic subunit of protein phosphatase 1 regulates eukaryotic initiation factor 2 alpha signalling and cell survival to endoplasmic reticulum stress. J. Biol. Chem., 2006, 281, 26633-26644.
94. Hussain, S. G. and Ramaiah, K. V. A., Reduced eIF2alpha phosphorylation and increased pro-apoptotic proteins in aging. Biochem. Biophys. Res. Commun., 2007, 355, 365-370.
95. Onuki, R. et al., An RNA-dependent protein kinase is involved in tunicamycin-induced apoptosis and Alzheimer's disease. EMBO J., 2004, 23, 959-968.
96. Shimazawa, M. and Hara, H., Inhibitor of double stranded RNA-dependent protein kinase protects against cell damage induced by ER stress. Neurosci. Lett., 2006 409, 192-195.
97. Warnakulasuriyarachchi, D., Cerquozzi, S., Cheung, H. H. and Holcik, M., Translational induction of the inhibitor of apoptosis protein HIAP2 during endoplasmic reticulum stress attenuates cell death and is mediated via an inducible internal ribosome entry site element. J. Biol. Chem., 2004, 279, 17148-17157.
98. Yoneda, T., Imaizumi, K., Oono, K., Yui, D., Gomi, F., Katayama, T. and Tohyama, M., Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumour necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J. Biol. Chem., 2001, 276, 13935-13940.
99. Szegezdi, E., Fitzgerald, U. and Samali, A., Caspase-12 and ER-stress-mediated apoptosis: The story so far. Ann. NY Acad. Sci., 2003, 1010, 186-194.
100. Xu, C., Bailly-Maitre, B. and Reed, J. C., Endoplasmic reticulum stress: Cell life and death decisions. J. Clin. Invest., 2005, 115, 2656-2664.