Mercury and cadmium trigger expression of the copper importer Ctr1B, which enables Drosophila to thrive on heavy metal-loaded food

Biological Chemistry

Volumn 390, Issue 2, 2009, Pages 109-113

  Balamurugan, Kuppusamy ^a   Hua, Haiqing ^a   Georgiev, Oleg ^a   Schaffner, Walter ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Copper transporter; Heavy metal toxicity; Metal homeostasis; MTF 1; Non essential metals

Indexed keywords

CADMIUM; CELL PROTEIN; COPPER; FIBRINOGEN; MERCURY; METALLOTHIONEIN; TENIDAP; ZINC;

ARTICLE; BACTERIAL GENE; BINDING SITE; DNA RESPONSIVE ELEMENT; DNA SEQUENCE; DROSOPHILA; FOOD; MAMMAL; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; REPORTER GENE; STARVATION;

ANIMALS; BINDING, COMPETITIVE; CADMIUM; CATION TRANSPORT PROTEINS; COPPER; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MERCURY; METALLOTHIONEIN; MODELS, BIOLOGICAL; MUSCLE PROTEINS;

HEXAPODA; MAMMALIA;

EID: 59949087862     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2009.020     Document Type: Article

References (29)

1. Andrews, G.K. (2001). Cellular zinc sensors: MTF-1 regulation of gene expression. Biometals 14, 223-237.
2. Balamurugan, K. and Schaffner, W. (2006). Copper homeostasis in eukaryotes: teetering on a tightrope. Biochim. Biophys. Acta 1763, 737-746.
3. Balamurugan, K., Egli, D., Selvaraj, A., Zhang, B., Georgiev, O., and Schaffner, W. (2004). Metal-responsive transcription factor (MTF-1) and heavy metal stress response in Drosophila and mammalian cells: a functional comparison. Biol. Chem. 385, 597-603.
4. Balamurugan, K., Egli, D., Hua, H., Rajaram, R., Seisenbacher, G., Georgiev, O., and Schaffner, W. (2007). Copper homeostasis in Drosophila by complex interplay of import, storage and behavioral avoidance. EMBO J. 26, 1035-1044.
5. Chen, X., Hua, H., Balamurugan, K., Kong, X., Zhang, L., George, G.N., Georgiev, O., Schaffner, W., and Giedroc, D.P. (2008). Copper sensing function of Drosophila metal-responsive transcription factor-1 is mediated by a tetranuclear Cu(I) cluster. Nucleic Acids Res. 36, 3128-3138.
6. Dancis, A., Yuan, D.S., Haile, D., Askwith, C., Eide, D., Moehle, C., Kaplan, J., and Klausner, R. (1994). Molecular characterization of a copper transport protein in S. cerevisiae: an unexpected role for copper in iron transport. Cell 76, 393-402.
7. Egli, D., Selvaraj, A., Yepiskoposyan, H., Zhang, B., Hafen, E., Georgiev, O., and Schaffner, W. (2003). Knockout of 'metal-responsive transcription factor' MTF-1 in Drosophila by homologous recombination reveals its central role in heavy metal homeostasis. EMBO J. 22, 100-108.
8. Egli, D., Yepiskoposyan, H., Selvaraj, A., Balamurugan, K., Rajaram, R., Simons, A., Multhaup, G., Mettler, S., Vardanyan, A., Georgiev, O., et al. (2006). A family knockout of all four Drosophila metallothioneins reveals a central role in copper homeostasis and detoxification. Mol. Cell. Biol. 26, 2286-2296.
9. Giedroc, D.P., Chen, X., and Apuy, J.L. (2001). Metal response element (MRE)-binding transcription factor-1 (MTF-1): structure, function, and regulation. Antiox. Redox Signal. 3, 577-596.
10. Halliwell, B. and Gutteridge, J.M. (1990). Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol. 186, 1-85.
11. Kim, B.E., Nevitt, T., and Thiele, D.J. (2008). Mechanisms for copper acquisition, distribution and regulation. Nat. Chem. Biol. 4, 176-185.
12. Kuo, Y.M., Zhou, B., Cosco, D., and Gitschier, J. (2001). The copper transporter CTR1 provides an essential function in mammalian embryonic development. Proc. Natl. Acad. Sci. USA 98, 6836-6841.
13. Lee, J., Prohaska, J.R., Dagenais, S.L., Glover, T.W., and Thiele, D.J. (2000). Isolation of a murine copper transporter gene, tissue specific expression and functional complementation of a yeast copper transport mutant. Gene 254, 87-96.
14. Lee, J., Prohaska, J.R., and Thiele, D.J. (2001). Essential role for mammalian copper transporter Ctr1 in copper homeostasis and embryonic development. Proc. Natl. Acad. Sci. USA 98, 6842-6847.
15. Lichtlen, P. and Schaffner, W. (2001). Putting its fingers on stressful situations: the heavy metal-regulatory transcription factor MTF-1. Bioessays 23, 1010-1017.
16. Mathews, W.R., Wang, F., Eide, D.J., and Van Doren, M. (2005). Drosophila fear of intimacy encodes a Zrt/IRT-like protein (ZIP) family zinc transporter functionally related to mammalian ZIP proteins. J. Biol. Chem. 280, 787-795.
17. Mercer, J.F. and Llanos, R.M. (2003). Molecular and cellular aspects of copper transport in developing mammals. J. Nutr. 133 (5 Suppl. 1), 1481S-1484S.
18. O'Halloran, T.V. and Culotta, V.C. (2000). Metallochaperones, an intracellular shuttle service for metal ions. J. Biol. Chem. 275, 25057-25060.
19. Otsuka, F., Okugaito, I., Ohsawa, M., Iwamatsu, A., Suzuki, K., and Koizumi, S. (2000). Novel responses of ZRF, a variant of human MTF-1, to in vivo treatment with heavy metals. Biochim. Biophys. Acta 1492, 330-340.
20. Puig, S. and Thiele, D.J. (2002). Molecular mechanisms of copper uptake and distribution. Curr. Opin. Chem. Biol. 6, 171-180.
21. Radtke, F., Heuchel, R., Georgiev, O., Hergersberg, M., Gariglio, M., Dembic, Z., and Schaffner, W. (1993). Cloned transcription factor MTF-1 activates the mouse metallothionein I promoter. EMBO J. 12, 1355-1362.
22. Rutherford, J.C. and Bird, A.J. (2004). Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot. Cell 3, 1-13.
23. Selvaraj, A., Balamurugan, K., Yepiskoposyan, H., Zhou, H., Egli, D., Georgiev, O., Thiele, D.J., and Schaffner, W. (2005). Metal-responsive transcription factor (MTF-1) handles both extremes, copper load and copper starvation, by activating different genes. Genes Dev. 19, 891-896.
24. Stuart, G.W., Searle, P.F., Chen, H.Y., Brinster, R.L., and Palmiter, R.D. (1984). A 12-base-pair DNA motif that is repeated several times in metallothionein gene promoters confers metal regulation to a heterologous gene. Proc. Natl. Acad. Sci. USA 81, 7318-7322.
25. Turski, M.L. and Thiele, D.J. (2007). Drosophila Ctr1A functions as a copper transporter essential for development. J. Biol. Chem. 282, 24017-24026.
26. Wang, Y., Lorenzi, I., Georgiev, O., and Schaffner, W. (2004). Metal-responsive transcription factor-1 (MTF-1) selects different types of metal response elements at low vs. high zinc concentration. Biol. Chem. 385, 623-632.
27. Yepiskoposyan, H., Egli, D., Fergestad, T., Selvaraj, A., Treiber, C., Multhaup, G., Georgiev, O., and Schaffner, W. (2006). Transcriptome response to heavy metal stress in Drosophila reveals a new zinc transporter that confers resistance to zinc. Nucleic Acids Res. 34, 4866-4877.
28. Zhang, B., Egli, D., Georgiev, O., and Schaffner, W. (2001). The Drosophila homolog of mammalian zinc finger factor MTF-1 activates transcription in response to heavy metals. Mol. Cell. Biol. 21, 4505-4514.
29. Zhou, H., Cadigan, K.M., and Thiele, D.J. (2003). A copper-regulated transporter required for copper acquisition, pigmentation, and specific stages of development in Drosophila melanogaster. J. Biol. Chem. 278, 48210-48218.