ER and aging-Protein folding and the ER stress response

Ageing Research Reviews

Volumn 8, Issue 3, 2009, Pages 150-159

  Naidoo, Nirinjini ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Aging; Endoplasmic reticulum stress response; Protein folding; Quality control; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CALCIUM; CALNEXIN; CALRETICULIN; CASPASE; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MESSENGER RNA; OXIDOREDUCTASE; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN BCL 2; PROTEIN DISULFIDE ISOMERASE; PROTEIN SERINE THREONINE KINASE;

AMPEROMETRIC BIOSENSOR; APOPTOSIS; CALCIUM TRANSPORT; CELL AGING; DISULFIDE BOND; ENDOPLASMIC RETICULUM STRESS; GLYCOSYLATION; HUMAN; INHIBITION KINETICS; LIPOGENESIS; NONHUMAN; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN QUALITY; RNA SPLICING; SHORT SURVEY; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; UPREGULATION;

AGING; ANIMALS; CELL AGING; ENDOPLASMIC RETICULUM; HOMEOSTASIS; HUMANS; MOLECULAR CHAPERONES; PROTEIN FOLDING; PROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 67349217063     PISSN: 15681637     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.arr.2009.03.001     Document Type: Short Survey

References (89)

1. Argon Y., and Simen B.B. GRP94, an ER chaperone with protein and peptide binding properties. Semin. Cell. Dev. Biol. 10 (1999) 495-505
2. Berlett B.S., and Stadtman E.R. Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272 (1997) 20313-20316
3. Braakman I., Helenius J., and Helenius A. Role of ATP and disulphide bonds during protein folding in the endoplasmic reticulum. Nature 356 (1992) 260-262
4. Brush M.H., Weiser D.C., and Shenolikar S. 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. Mol. Cell. Biol. 23 (2003) 1292-1303
5. Calfon M., Zeng H., Urano F., Till J.H., Hubbard S.R., Harding H.P., Clark S.G., and Ron D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA [erratum appears in Nature 2002 Nov 14;420(6912):202]. Nature 415 (2002) 92-96
6. Choi B.H., and Kim J.S. Age-related decline in expression of calnexin. Exp. Mol. Med. 36 (2004) 499-503
7. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 103 (2000) 239-252
8. Dorner A.J., Wasley L.C., and Kaufman R.J. Protein dissociation from GRP78 and secretion are blocked by depletion of cellular ATP levels. Proc Natl. Acad. Sci. USA 87 (1990) 7429-7432
9. Ellgaard L., and Helenius A. Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell. Biol. 4 (2003) 181-191
10. Ellgaard L., and Ruddock L.W. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 6 (2005) 28-32
11. Erickson R.R., Dunning L.M., and Holtzman J.L. The effect of aging on the chaperone concentrations in the hepatic, endoplasmic reticulum of male rats: the possible role of protein misfolding due to the loss of chaperones in the decline in physiological function seen with age. J. Gerontol. A Biol. Sci Med. Sci. 61 (2006) 435-443
12. Finkel T., and Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 408 (2000) 239-247
13. Flynn G.C., Chappell T.G., and Rothman J.E. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 245 (1989) 385-390
14. Fonseca S.G., Lipson K.L., and Urano F. Endoplasmic reticulum stress signaling in pancreatic beta-cells. Antioxid. Redox. Signal. 9 (2007) 2335-2344
15. Gao Y., Signore A.P., Yin W., Cao G., Yin X.M., Sun F., Luo Y., Graham S.H., and Chen J. Neuroprotection against focal ischemic brain injury by inhibition of c-Jun N-terminal kinase and attenuation of the mitochondrial apoptosis-signaling pathway. J. Cereb. Blood Flow Metab. 25 (2005) 694-712
16. Garcia-Ruiz C., Colell A., Paris R., and Fernandez-Checa J.C. Direct interaction of GD3 ganglioside with mitochondria generates reactive oxygen species followed by mitochondrial permeability transition, cytochrome c release, and caspase activation. FASEB J. 14 (2000) 847-858
17. Gething M.J. Role and regulation of the ER chaperone BiP. Semin. Cell Dev. Biol. 10 (1999) 465-472
18. Gething M.J., and Sambrook J. Protein folding in the cell. Nature 355 (1992) 33-45
19. Gotoh T., and Mori M. Regulation of apoptosis by molecular chaperones. Tanpakushitsu Kakusan Koso - Protein Nucleic Acid Enzyme 49 (2004) 1010-1013
20. Haas I.G. BiP-a heat shock protein involved in immunoglobulin chain assembly. Curr. Top. Microbiol. Immunol. 167 (1991) 71-82
21. Hamman B.D., Hendershot L.M., and Johnson A.E. BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell 92 (1998) 747-758
22. Hampton R.Y. ER stress response: getting the UPR hand on misfolded proteins. Curr. Biol. 10 (2000) R518-R521
23. Harding H.P., Calfon M., Urano F., Novoa I., and Ron D. Transcriptional and translational control in the Mammalian unfolded protein response. Ann. Rev. Cell Develop. Biol. 18 (2002) 575-599
24. Harding H.P., and Ron D. Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes. 51 Suppl 3: (2002) S455-S461
25. Harding H.P., Zhang Y., Bertolotti A., Zeng H., and Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5 (2000) 897-904
26. Hebert D.N., and Molinari M. In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol. Rev. 87 (2007) 1377-1408
27. Hollien J., and Weissman J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313 (2006) 104-107 [see comment]
28. Hussain S.G., and Ramaiah K.V. Reduced eIF2alpha phosphorylation and increased proapoptotic proteins in aging. Biochem. Biophys. Res. Commun. 355 (2007) 365-370
29. Hwang C., Sinskey A.J., and Lodish H.F. Oxidized redox state of glutathione in the endoplasmic reticulum. Science. 257 (1992) 1496-1502
30. Ikeyama S., Wang X.T., Li J., Podlutsky A., Martindale J.L., Kokkonen G., van Huizen R., Gorospe M., and Holbrook N.J. Expression of the pro-apoptotic gene gadd153/chop is elevated in liver with aging and sensitizes cells to oxidant injury. J. Biol. Chem. 278 (2003) 16726-16731
31. Katayama T., Imaizumi K., Sato N., Miyoshi K., Kudo T., Hitomi J., Morihara T., Yoneda T., Gomi F., Mori Y., Nakano Y., Takeda J., Tsuda T., Itoyama Y., Murayama O., Takashima A., St George-Hyslop P., Takeda M., and Tohyama M. Presenilin-1 mutations downregulate the signalling pathway of the unfolded-protein response. Nat. Cell Biol. 1 (1999) 479-485
32. Kaufman R.J. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13 (1999) 1211-1233
33. Kaufman R.J. Orchestrating the unfolded protein response in health and disease. J. Clin. Invest. 110 (2002) 1389-1398
34. Kaufman R.J., Scheuner D., Schroder M., Shen X., Lee K., Liu C.Y., and Arnold S.M. The unfolded protein response in nutrient sensing and differentiation. Nat. Rev. Mol. Cell Biol. 3 (2002) 411-421
35. Kim H.G., Hong S.M., Kim S.J., Park H.J., Jung H.I., Lee Y.Y., Moon J.S., Lim H.W., Park E.H., and Lim C.J. Age-related changes in the activity of antioxidant and redox enzymes in rats. Mol. Cells 16 (2003) 278-284
36. Kim S.J., Zhang Z., Lee Y.C., and Mukherjee A.B. Palmitoyl-protein thioesterase-1 deficiency leads to the activation of caspase-9 and contributes to rapid neurodegeneration in INCL. Hum. Mol. Genet. 15 (2006) 1580-1586
37. Kornfeld R., and Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54 (1985) 631-664
38. Lee K., Neigeborn L., and Kaufman R.J. The unfolded protein response is required for haploid tolerance in yeast [erratum appears in J Biol Chem. 2003 May 30;278(22):20444]. J. Biol. Chem. 278 (2003) 11818-11827
39. Lee K., Tirasophon W., Shen X., Michalak M., Prywes R., Okada T., Yoshida H., Mori K., and Kaufman R.J. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Develop. 16 (2002) 452-466
40. Lei K., and Davis R.J. JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc. Natl. Acad. Sci. USA 100 (2003) 2432-2437
41. Lindholm D., Wootz H., and Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ. 13 (2006) 385-392
42. Ma Y., Brewer J.W., Diehl J.A., and Hendershot L.M. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318 (2002) 1351-1365
43. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.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. 21 (2001) 1249-1259
44. Melnick J., Dul J.L., and Argon Y. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 370 (1994) 373-375
45. Molinari M., Calanca V., Galli C., Lucca P., and Paganetti P. Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299 (2003) 1397-1400
46. Naidoo N., Ferber M., Master M., Zhu Y., and Pack A.I. Aging impairs the unfolded protein response to sleep deprivation and leads to proapoptotic signaling. J. Neurosci. 28 (2008) 6539-6548
47. Naidoo N., Giang W., Galante R.J., and Pack A.I. Sleep deprivation induces the unfolded protein response in mouse cerebral cortex. J. Neurochem. 92 (2005) 1150-1157
48. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., and Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403 (2000) 98-103
49. Nechushtan A., Smith C.L., Hsu Y.T., and Youle R.J. Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J. 18 (1999) 2330-2341
50. Nunez G., Benedict M.A., Hu Y., and Inohara N. Caspases: the proteases of the apoptotic pathway. Oncogene 17 (1998) 3237-3245
51. Nuss J.E., Choksi K.B., DeFord J.H., and Papaconstantinou J. Decreased enzyme activities of chaperones PDI and BiP in aged mouse livers. Biochem. Biophys. Res. Commun. 365 (2008) 355-361
52. Oda Y., Hosokawa N., Wada I., and Nagata K. EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299 (2003) 1394-1397
53. Okada T., Yoshida H., Akazawa R., Negishi M., and Mori K. Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem. J. 366 (2002) 585-594
54. Oliver J.D., Roderick H.L., Llewellyn D.H., and High S. ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Mol. Biol. Cell. 10 (1999) 2573-2582
55. Oyadomari S., and Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11 (2004) 381-389
56. Paz Gavilan M., Vela J., Castano A., Ramos B., del Rio J.C., Vitorica J., and Ruano D. Cellular environment facilitates protein accumulation in aged rat hippocampus. Neurobiol. Aging 27 (2006) 973-982
57. Pirot P., Naamane N., Libert F., Magnusson N.E., Orntoft T.F., Cardozo A.K., and Eizirik D.L. Global profiling of genes modified by endoplasmic reticulum stress in pancreatic beta cells reveals the early degradation of insulin mRNAs. Diabetologia 50 (2007) 1006-1014
58. Prostko C.R., Brostrom M.A., and Brostrom C.O. Reversible phosphorylation of eukaryotic initiation factor 2 alpha in response to endoplasmic reticular signaling. Mol. Cell. Biochem. 127-128 (1993) 255-265
59. Rabek J.P., Boylston III W.H., and Papaconstantinou J. Carbonylation of ER chaperone proteins in aged mouse liver. Biochem. Biophys. Res. Commun. 305 (2003) 566-572
60. Ron D. Translational control in the endoplasmic reticulum stress response. J. Clin. Invest. 110 (2002) 1383-1388
61. Schrag J.D., Procopio D.O., Cygler M., Thomas D.Y., and Bergeron J.J. Lectin control of protein folding and sorting in the secretory pathway. Trends Biochem. Sci. 28 (2003) 49-57
62. Schroder M. The unfolded protein response. Mol. Biotechnol. 34 (2006) 279-290
63. Schroder M., and Kaufman R.J. ER stress and the unfolded protein response. Mutat. Res. 569 (2005) 29-63
64. Schroder M., and Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 74 (2005) 739-789
65. Senderek J., Krieger M., Stendel C., Bergmann C., Moser M., Breitbach-Faller N., Rudnik-Schoneborn S., Blaschek A., Wolf N.I., Harting I., North K., Smith J., Muntoni F., Brockington M., Quijano-Roy S., Renault F., Herrmann R., Hendershot L.M., Schroder J.M., Lochmuller H., Topaloglu H., Voit T., Weis J., Ebinger F., and Zerres K. Mutations in SIL1 cause Marinesco-Sjogren syndrome, a cerebellar ataxia with cataract and myopathy. Nat. Genet. 37 (2005) 1312-1314
66. Sohal R.S., and Weindruch R. Oxidative stress, caloric restriction, and aging. Science 273 (1996) 59-63
67. Stevens F.J., and Argon Y. Protein folding in the ER. Semin. Cell. Dev. Biol. 10 (1999) 443-454
68. Szegezdi E., Fitzgerald U., and Samali A. Caspase-12 and ER-stress-mediated apoptosis: the story so far. Ann. N.Y. Acad. Sci. 1010 (2003) 186-194
69. Szegezdi E., Logue S.E., Gorman A.M., and Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 7 (2006) 880-885
70. Thornberry N.A., and Lazebnik Y. Caspases: enemies within. Science 281 (1998) 1312-1316
71. Tomassini B., Malisan F., Franchi L., Nicolo C., Calvo G.B., Saito T., and Testi R. Calnexin suppresses GD3 synthase-induced apoptosis. FASEB J. 18 (2004) 1553-1555
72. Tsuruta F., Sunayama J., Mori Y., Hattori S., Shimizu S., Tsujimoto Y., Yoshioka K., Masuyama N., and Gotoh Y. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J. 23 (2004) 1889-1899
73. Tu B.P., and Weissman J.S. Oxidative protein folding in eukaryotes: mechanisms and consequences. J. Cell. Biol. 164 (2004) 341-346
74. Urano F., Bertolotti A., and Ron D. IRE1 and efferent signaling from the endoplasmic reticulum. J. Cell Sci. 113 Pt 21 (2000) 3697-3702
75. van der Vlies D., Pap E.H., Post J.A., Celis J.E., and Wirtz K.W. Endoplasmic reticulum resident proteins of normal human dermal fibroblasts are the major targets for oxidative stress induced by hydrogen peroxide. Biochem. J. 366 (2002) 825-830
76. Vasa-Nicotera M. The new kid on the block: the unfolded protein response in the pathogenesis of atherosclerosis. Cell Death. Differ. 11 Suppl 1 (2004) S10-S11
77. Vogel J.P., Misra L.M., and Rose M.D. Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast. J. Cell. Biol. 110 (1990) 1885-1895
78. Wang X.Z., Lawson B., Brewer J.W., Zinszner H., Sanjay A., Mi L.J., Boorstein R., Kreibich G., Hendershot L.M., and Ron D. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol. Cell. Biol. 16 (1996) 4273-4280
79. Wolter K.G., Hsu Y.T., Smith C.L., Nechushtan A., Xi X.G., and Youle R.J. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell. Biol. 139 (1997) 1281-1292
80. Wu J., and Kaufman R.J. From acute ER stress to physiological roles of the Unfolded Protein Response. Cell Death Differ. 13 (2006) 374-384
81. Xu C., Bailly-Maitre B., and Reed J.C. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 115 (2005) 2656-2664
82. Yoshida H. ER stress and diseases. FEBS J. 274 (2007) 630-658
83. Yoshida H., Haze K., Yanagi H., Yura T., and Mori K. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors [erratum appears in J Biol Chem 1999 Jan 22;274(4):2592]. J. Biol. Chem. 273 (1998) 33741-33749
84. 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 [see comment]. Devel. Cell. 4 (2003) 265-271
85. 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 107 (2001) 881-891
86. Zhang K., and Kaufman R.J. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66 (2006) S102-S109
87. Zhao L., and Ackerman S.L. Endoplasmic reticulum stress in health and disease. Curr. Opin. Cell. Biol. 18 (2006) 444-452
88. Zhu Y., Carvey P.M., and Ling Z. Age-related changes in glutathione and glutathione-related enzymes in rat brain. Brain Res. 1090 (2006) 35-44
89. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., Stevens J.L., and Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12 (1998) 982-995