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Volume 272, Number 18, Issue of May 2, 1997 pp. 11763-11769
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.

Negative Control of Heavy Metal Uptake by the Saccharomyces cerevisiae BSD2 Gene

(Received for publication, January 30, 1997)

Xiu Fen Liu Dagger , Frantisek Supek , Nathan Nelson par and Valeria Cizewski Culotta Dagger

From the Dagger  Division of Toxicological Sciences, Department of Environmental Health Sciences, Johns Hopkins University School of Public Health, Baltimore, Maryland 21205, the  Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, California 94720-3202, and the par  Department of Biochemistry, Tel Aviv University, Tel Aviv 69978, Israel

We have previously shown that mutations in the Saccharomyces cerevisiae BSD2 gene suppress oxidative damage in cells lacking superoxide dismutase and also lead to hyperaccumulation of copper ions. We demonstrate here that bsd2 mutant cells additionally accumulate high levels of cadmium and cobalt. By biochemical fractionation and immunofluorescence microscopy, BSD2 exhibited localization to the endoplasmic reticulum, suggesting that BSD2 acts at a distance to inhibit metal uptake from the growth medium. This BSD2 control of ion transport occurs independently of the CTR1 and FET4 metal transport systems. Genetic suppressor analysis revealed that hyperaccumulation of copper and cadmium in bsd2 mutants is mediated through SMF1, previously shown to encode a plasma membrane transporter for manganese. A nonsense mutation removing the carboxyl-terminal hydrophobic domain of SMF1 was found to mimic a smf1 gene deletion by eliminating the copper and cadmium toxicity of bsd2 mutants and also by precluding the bsd2 suppression of superoxide dismutase deficiency. However, inactivation of SMF1 did not eliminate the elevated cobalt levels in bsd2 mutants. Instead, this cobalt accumulation was found to be specifically mediated through the SMF1 homologue, SMF2. Hence, BSD2 prevents metal hyperaccumulation by exerting negative control over the SMF1 and SMF2 metal transport systems.


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