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J Biol Chem, Vol. 273, Issue 21, 12703-12709, May 22, 1998

Disruption of the Intracellular Sulfhydryl Homeostasis by Cadmium-induced Oxidative Stress Leads to Protein Thiolation and Ubiquitination in Neuronal Cells

Maria E. Figueiredo-PereiraDagger , Svetlana Yakushin, and Gerald Cohen

From the Dagger  Department of Biological Sciences, Hunter College of City University of New York, New York 10021 and  Department of Neurology, Mount Sinai School of Medicine of City University of New York, New York 10029

Cadmium is a potent cell poison known to cause oxidative stress by increasing lipid peroxidation and/or by changing intracellular glutathione levels and to affect the ubiquitin/ATP-dependent proteolytic pathway. However, the cellular mechanisms involved in cadmium toxicity are still not well understood, especially in neuronal cells. To investigate the relationship between cadmium-induced oxidative stress and the ubiquitin/ATP-dependent pathway, we treated cultures of neuronal cells with different concentrations of the metal ion. In addition to decreases in glutathione levels, we observed marked increases in protein-mixed disulfides (Pr-SSGs) after exposure of HT4 cells (a mouse neuronal cell line) or rat primary mesencephalic cultures to Cd2+. The increases in intracellular levels of Pr-SSGs were concurrent with increases in the levels of ubiquitinated proteins (Ub proteins) when the HT4 cells were subjected to lower (25 µM or less) concentrations of cadmium. However, higher concentrations of cadmium (50 µM), which were toxic, led to increases in Pr-SSGs but inhibited ubiquitination, probably reflecting inhibition of ubiquitinating enzymes. The cadmium-induced changes in Pr-SSGs and Ub proteins were not affected when more than 85% of intracellular glutathione was removed from the cells by the glutathione synthetase inhibitor L-buthionine-(S,R)-sulfoximine. However, the reducing agent dithiothreitol, which prevented the build up of Pr-SSGs in the cell, also blocked the accumulation of Ub proteins induced by cadmium. In addition, dithiothreitol blocked the effects of the higher toxic (50 µM) concentrations of cadmium on cytotoxicity and on glutathione, Pr-SSGs, and Ub proteins. Together, these results strongly suggest that changes in the levels of intracellular Pr-SSGs and ubiquitin-protein conjugates in neuronal cells are responses closely associated with the disruption of intracellular sulfhydryl homeostasis caused by cadmium-mediated oxidative stress.

Copyright © 1998 by The American Society for Biochemistry and Molecular Biology, Inc.


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