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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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Glucagon-Like Peptide-1 Agonists Protect Pancreatic {beta}-Cells From Lipotoxic Endoplasmic Reticulum Stress Through Upregulation of BiP and JunB.
D. A. Cunha, L. Ladriere, F. Ortis, M. Igoillo-Esteve, E. N. Gurzov, R. Lupi, P. Marchetti, D. L. Eizirik, and M. Cnop (2009)
Diabetes 58, 2851-2862
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Xanthohumol Activates the Proapoptotic Arm of the Unfolded Protein Response in Chronic Lymphocytic Leukemia.
S. LUST, B. VANHOECKE, M. VAN GELE, J. BOELENS, H. VAN MELCKEBEKE, M. KAILEH, W. VANDEN BERGHE, G. HAEGEMAN, J. PHILIPPE, M. BRACKE, et al. (2009)
Anticancer Res 29, 3797-3805
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OSU-A9, a potent indole-3-carbinol derivative, suppresses breast tumor growth by targeting the Akt-NF-{kappa}B pathway and stress response signaling.
J.-R. Weng, C.-H. Tsai, H. A. Omar, A. M. Sargeant, D. Wang, S. K. Kulp, C. L. Shapiro, and C.-S. Chen (2009)
Carcinogenesis 30, 1702-1709
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Pleiotropic effects of negative energy balance in the postpartum dairy cow on splenic gene expression: repercussions for innate and adaptive immunity.
D. G. Morris, S. M. Waters, S. D. McCarthy, J. Patton, B. Earley, R. Fitzpatrick, J. J. Murphy, M. G. Diskin, D. A. Kenny, A. Brass, et al. (2009)
Physiol Genomics 39, 28-37
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Induction of endoplasmic reticulum stress response by TZD18, a novel dual ligand for peroxisome proliferator-activated receptor {alpha}/{gamma}, in human breast cancer cells.
C. Zang, H. Liu, J. Bertz, K. Possinger, H. P. Koeffler, E. Elstner, and J. Eucker (2009)
Mol. Cancer Ther. 8, 2296-2307
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The Homocysteine-inducible Endoplasmic Reticulum Stress Protein Counteracts Calcium Store Depletion and Induction of CCAAT Enhancer-binding Protein Homologous Protein in a Neurotoxin Model of Parkinson Disease.
S. Chigurupati, Z. Wei, C. Belal, M. Vandermey, G. A. Kyriazis, T. V. Arumugam, and S. L. Chan (2009)
J. Biol. Chem. 284, 18323-18333
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Novel Subtilase Cytotoxin Produced by Shiga-Toxigenic Escherichia coli Induces Apoptosis in Vero Cells via Mitochondrial Membrane Damage.
G. Matsuura, N. Morinaga, K. Yahiro, R. Komine, J. Moss, H. Yoshida, and M. Noda (2009)
Infect. Immun. 77, 2919-2924
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Gene Expression Profiling Identifies a Role for CHOP During Inhibition of the Mitochondrial Respiratory Chain.
F. Ishikawa, T. Akimoto, H. Yamamoto, Y. Araki, T. Yoshie, K. Mori, H. Hayashi, K. Nose, and M. Shibanuma (2009)
J. Biochem. 146, 123-132
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When separation means death: killing through the mitochondria, but starting from the endoplasmic reticulum.
V. Lamarca and L. Scorrano (2009)
EMBO J. 28, 1681-1683
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Tuberous Sclerosis Complex Activity Is Required to Control Neuronal Stress Responses in an mTOR-Dependent Manner.
A. Di Nardo, I. Kramvis, N. Cho, A. Sadowski, L. Meikle, D. J. Kwiatkowski, and M. Sahin (2009)
J. Neurosci. 29, 5926-5937
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Glycogen Synthase Kinase-3{beta} Mediates Endoplasmic Reticulum Stress-Induced Lysosomal Apoptosis in Leukemia.
W.-C. Huang, Y.-S. Lin, C.-L. Chen, C.-Y. Wang, W.-H. Chiu, and C.-F. Lin (2009)
J. Pharmacol. Exp. Ther. 329, 524-531
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Bcl-2 family on guard at the ER.
E. Szegezdi, D. C. MacDonald, T. Ni Chonghaile, S. Gupta, and A. Samali (2009)
Am J Physiol Cell Physiol 296, C941-C953
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The antitumoral effect of Paris Saponin I associated with the induction of apoptosis through the mitochondrial pathway.
X. Xiao, P. Bai, T. M. Bui Nguyen, J. Xiao, S. Liu, G. Yang, L. Hu, X. Chen, X. Zhang, J. Liu, et al. (2009)
Mol. Cancer Ther. 8, 1179-1188
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Human Cytomegalovirus Protein pUL38 Induces ATF4 Expression, Inhibits Persistent JNK Phosphorylation, and Suppresses Endoplasmic Reticulum Stress-Induced Cell Death.
B. Xuan, Z. Qian, E. Torigoi, and D. Yu (2009)
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
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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
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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
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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
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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
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