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Mol. Cell. Biol. 21 (4): 1249-1259

Copyright © 2001 by the American Society for Microbiology. All rights reserved.

Molecular and Cellular Biology, February 2001, p. 1249-1259, Vol. 21, No. 4
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.4.1249-1259.2001

Gadd153 Sensitizes Cells to Endoplasmic Reticulum Stress by Down-Regulating Bcl2 and Perturbing the Cellular Redox State

Karen D. McCullough,1 Jennifer L. Martindale,1 Lars-Oliver Klotz,1 Tak-Yee Aw,2,dagger and Nikki J. Holbrook1,*

Cell Stress and Aging Section, Laboratory of Biological Chemistry, National Institute on Aging, National Institutes of Health, Baltimore, Maryland 21224-6825,1 and Department of Molecular and Cellular Physiology, Louisiana State University Health Sciences Center, Louisiana State University, Shreveport, Louisiana 711302

Received 15 May 2000/Returned for modification 21 June 2000/Accepted 14 November 2000

gadd153, also known as chop, is a highly stress-inducible gene that is robustly expressed following disruption of homeostasis in the endoplasmic reticulum (ER) (so-called ER stress). Although all reported types of ER stress induce expression of Gadd153, its role in the stress response has remained largely undefined. Several studies have correlated Gadd153 expression with cell death, but a mechanistic link between Gadd153 and apoptosis has never been demonstrated. To address this issue we employed a cell model system in which Gadd153 is constitutively overexpressed, as well as two cell lines in which Gadd153 expression is conditional. In all cell lines, overexpression of Gadd153 sensitized cells to ER stress. Investigation of the mechanisms contributing to this effect revealed that elevated Gadd153 expression results in the down-regulation of Bcl2 expression, depletion of cellular glutathione, and exaggerated production of reactive oxygen species. Restoration of Bcl2 expression in Gadd153-overexpressing cells led to replenishment of glutathione and a reduction in levels of reactive oxygen species, and it protected cells from ER stress-induced cell death. We conclude that Gadd153 sensitizes cells to ER stress through mechanisms that involve down-regulation of Bcl2 and enhanced oxidant injury.

* Corresponding author. Mailing address: Laboratory of Biological Chemistry, 5600 Nathan Shock Dr., Baltimore, MD 21224. Phone: (410) 558-8446. Fax: (410) 558-8386. E-mail: nikki-holbrook{at}nih.gov.

dagger Present address: Institut fur Physiologische Chemie I, Heinrich-Heine-Universitat Dusseldorf, D-40225 Dusseldorf, Germany.

Molecular and Cellular Biology, February 2001, p. 1249-1259, Vol. 21, No. 4
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.4.1249-1259.2001

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J. Virol. 83, 3463-3474
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Oxidized Low-Density Lipoproteins Trigger Endoplasmic Reticulum Stress in Vascular Cells: Prevention by Oxygen-Regulated Protein 150 Expression.
M. Sanson, N. Auge, C. Vindis, C. Muller, Y. Bando, J.-C. Thiers, M.-A. Marachet, K. Zarkovic, Y. Sawa, R. Salvayre, et al. (2009)
Circ. Res. 104, 328-336
   Abstract »    Full Text »    PDF »
Implication of nitric oxide in the increased islet-cells vulnerability of adult progeny from protein-restricted mothers and its prevention by taurine.
K Goosse, T Bouckenooghe, M Balteau, B Reusens, and C Remacle (2009)
J. Endocrinol. 200, 177-187
   Abstract »    Full Text »    PDF »
Glucose-regulated protein 78 antagonizes cisplatin and adriamycin in human melanoma cells.
C. C. Jiang, Z. G. Mao, K. A. Avery-Kiejda, M. Wade, P. Hersey, and X. D. Zhang (2009)
Carcinogenesis 30, 197-204
   Abstract »    Full Text »    PDF »
Chemical Biology Investigation of Cell Death Pathways Activated by Endoplasmic Reticulum Stress Reveals Cytoprotective Modulators of ASK1.
I. Kim, C.-W. Shu, W. Xu, C.-W. Shiau, D. Grant, S. Vasile, N. D. P. Cosford, and J. C. Reed (2009)
J. Biol. Chem. 284, 1593-1603
   Abstract »    Full Text »    PDF »
CHAC1/MGC4504 Is a Novel Proapoptotic Component of the Unfolded Protein Response, Downstream of the ATF4-ATF3-CHOP Cascade.
I. N. Mungrue, J. Pagnon, O. Kohannim, P. S. Gargalovic, and A. J. Lusis (2009)
J. Immunol. 182, 466-476
   Abstract »    Full Text »    PDF »
The Molecular Mechanism of Endoplasmic Reticulum Stress-Induced Apoptosis in PC-12 Neuronal Cells: The Protective Effect of Insulin-Like Growth Factor I.
C.-G. Zou, X.-Z. Cao, Y.-S. Zhao, S.-Y. Gao, S.-D. Li, X.-Y. Liu, Y. Zhang, and K.-Q. Zhang (2009)
Endocrinology 150, 277-285
   Abstract »    Full Text »    PDF »
Antagonism of E2F-1 regulated Bnip3 transcription by NF-{kappa}B is essential for basal cell survival.
J. Shaw, N. Yurkova, T. Zhang, H. Gang, F. Aguilar, D. Weidman, C. Scramstad, H. Weisman, and L. A. Kirshenbaum (2008)
PNAS 105, 20734-20739
   Abstract »    Full Text »    PDF »
Antioxidants reduce endoplasmic reticulum stress and improve protein secretion.
J. D. Malhotra, H. Miao, K. Zhang, A. Wolfson, S. Pennathur, S. W. Pipe, and R. J. Kaufman (2008)
PNAS 105, 18525-18530
   Abstract »    Full Text »    PDF »
Enhancement of Cisplatin [cis-Diammine Dichloroplatinum (II)] Cytotoxicity by O6-Benzylguanine Involves Endoplasmic Reticulum Stress.
C. A. Rabik, M. L. Fishel, J. L. Holleran, K. Kasza, M. R. Kelley, M. J. Egorin, and M. E. Dolan (2008)
J. Pharmacol. Exp. Ther. 327, 442-452
   Abstract »    Full Text »    PDF »
Cytokine-Induced {beta}-Cell Death Is Independent of Endoplasmic Reticulum Stress Signaling.
M. C. Akerfeldt, J. Howes, J. Y. Chan, V. A. Stevens, N. Boubenna, H. M. McGuire, C. King, T. J. Biden, and D. R. Laybutt (2008)
Diabetes 57, 3034-3044
   Abstract »    Full Text »    PDF »
Mechanisms of Renal Apoptosis in Health and Disease.
A. B. Sanz, B. Santamaria, M. Ruiz-Ortega, J. Egido, and A. Ortiz (2008)
J. Am. Soc. Nephrol. 19, 1634-1642
   Abstract »    Full Text »    PDF »
Up-regulation of Mcl-1 Is Critical for Survival of Human Melanoma Cells upon Endoplasmic Reticulum Stress.
C. C. Jiang, K. Lucas, K. A. Avery-Kiejda, M. Wade, C. E. deBock, R. F. Thorne, J. Allen, P. Hersey, and X. D. Zhang (2008)
Cancer Res. 68, 6708-6717
   Abstract »    Full Text »    PDF »
Differential Control of the CCAAT/Enhancer-binding Protein {beta} (C/EBP{beta}) Products Liver-enriched Transcriptional Activating Protein (LAP) and Liver-enriched Transcriptional Inhibitory Protein (LIP) and the Regulation of Gene Expression during the Response to Endoplasmic Reticulum Stress.
Y. Li, E. Bevilacqua, C.-B. Chiribau, M. Majumder, C. Wang, C. M. Croniger, M. D. Snider, P. F. Johnson, and M. Hatzoglou (2008)
J. Biol. Chem. 283, 22443-22456
   Abstract »    Full Text »    PDF »
Endoplasmic reticulum stress and unfolded protein response in renal pathophysiology: Janus faces.
M. Kitamura (2008)
Am J Physiol Renal Physiol 295, F323-F334
   Abstract »    Full Text »    PDF »
Aging Impairs the Unfolded Protein Response to Sleep Deprivation and Leads to Proapoptotic Signaling.
N. Naidoo, M. Ferber, M. Master, Y. Zhu, and A. I. Pack (2008)
J. Neurosci. 28, 6539-6548
   Abstract »    Full Text »    PDF »
Differential Effect of the Protein Synthesis Inhibitors Puromycin and Cycloheximide on Vascular Smooth Muscle Cell Viability.
V. Croons, W. Martinet, A. G. Herman, and G. R. Y. De Meyer (2008)
J. Pharmacol. Exp. Ther. 325, 824-832
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Apoptosis induced by t10,c12-conjugated linoleic acid is mediated by an atypical endoplasmic reticulum stress response.
L. Ou, Y. Wu, C. Ip, X. Meng, Y.-C. Hsu, and M. M. Ip (2008)
J. Lipid Res. 49, 985-994
   Abstract »    Full Text »    PDF »
The Unfolded Protein Response: A Pathway That Links Insulin Demand with {beta}-Cell Failure and Diabetes.
D. Scheuner and R. J. Kaufman (2008)
Endocr. Rev. 29, 317-333
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Mitochondrial regulation by c-Myc and hypoxia-inducible factor-1{alpha} controls sensitivity to econazole.
Y. Yu, M. Niapour, Y. Zhang, and S. A. Berger (2008)
Mol. Cancer Ther. 7, 483-491
   Abstract »    Full Text »    PDF »
Inhibition of Endoplasmic Reticulum Stress-Induced Apoptosis of Melanoma Cells by the ARC Protein.
L. H. Chen, C. C. Jiang, R. Watts, R. F. Thorne, K. A. Kiejda, X. D. Zhang, and P. Hersey (2008)
Cancer Res. 68, 834-842
   Abstract »    Full Text »    PDF »
The Role for Endoplasmic Reticulum Stress in Diabetes Mellitus.
D. L. Eizirik, A. K. Cardozo, and M. Cnop (2008)
Endocr. Rev. 29, 42-61
   Abstract »    Full Text »    PDF »

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