Dissection of Drosophila MTF-1 reveals a domain for differential target gene activation upon copper overload vs. copper starvation

International Journal of Biochemistry and Cell Biology

Volumn 44, Issue 2, 2012, Pages 404-411

  Günther, Viola ^a   Waldvogel, Dominique ^a   Nosswitz, Michael ^a   Georgiev, Oleg ^a   Schaffner, Walter ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Drosophila; Heavy metal homeostasis; Metal responsive transcription factor 1; Metallothioneins; Transcriptional regulation

Indexed keywords

CARRIER PROTEIN; COPPER; CYSTEINE; HYBRID PROTEIN; METAL RESPONSIVE TRANSCRIPTION FACTOR 1; METALLOTHIONEIN; MUTANT PROTEIN; PROTEIN CTR1B; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DROSOPHILA; FEMALE; FEMALE STERILITY; FORELIMB; GENE ACTIVATION; GENE DELETION; GENE TARGETING; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; LIFESPAN; MALE; NONHUMAN; NUCLEAR EXPORT; NUCLEAR EXPORT SIGNAL; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; NUCLEOCYTOPLASMIC TRANSPORT; PHENOTYPE; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TRANSGENIC ANIMAL;

AMINO ACID SEQUENCE; ANIMALS; COPPER; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION; HEK293 CELLS; HUMANS; METALLOTHIONEIN; METALS, HEAVY; MOLECULAR SEQUENCE DATA; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS; ZINC FINGERS;

HEXAPODA; MAMMALIA;

EID: 84855575157     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2011.11.016     Document Type: Article

References (35)

1. K. Balamurugan, D. Egli, A. Selvaraj, B. Zhang, O. Georgiev, and W. Schaffner Metal-responsive transcription factor (MTF-1) and heavy metal stress response in Drosophila and mammalian cells: a functional comparison Biol Chem 385 2004 597 603 (Pubitemid 39144941)
2. X. Bi, T. Jones, F. Abbasi, H. Lee, B. Stultz, and D.A. Hursh Drosophila caliban, a nuclear export mediator, can function as a tumor suppressor in human lung cancer cells Oncogene 24 2005 8229 8239 (Pubitemid 43250915)
3. J. Bischof, R.K. Maeda, M. Hediger, F. Karch, and K. Basler An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases Proc Natl Acad Sci USA 104 2007 3312 3317 (Pubitemid 46364156)
4. B. Bodenmiller, D. Campbell, B. Gerrits, H. Lam, M. Jovanovic, and P. Picotti PhosphoPep - a database of protein phosphorylation sites in model organisms Nat Biotechnol 26 2008 1339 1340
5. E. Brugnera, O. Georgiev, F. Radtke, R. Heuchel, E. Baker, and G.R. Sutherland Cloning, chromosomal mapping and characterization of the human metal-regulatory transcription factor MTF-1 Nucleic Acids Res 22 1994 3167 3173 (Pubitemid 24260652)
6. R. Burke, E. Commons, and J. Camakaris Expression and localisation of the essential copper transporter DmATP7 in Drosophila neuronal and intestinal tissues Int J Biochem Cell Biol 40 2008 1850 1860
7. X. Chen, H. Hua, K. Balamurugan, X. Kong, L. Zhang, and G.N. George Copper sensing function of Drosophila metal-responsive transcription factor-1 is mediated by a tetranuclear Cu(I) cluster Nucleic Acids Res 36 2008 3128 3138 (Pubitemid 351737204)
8. X. Chen, B. Zhang, P.M. Harmon, W. Schaffner, D.O. Peterson, and D.P. Giedroc A novel cysteine cluster in human metal-responsive transcription factor 1 is required for heavy metal-induced transcriptional activation in vivo J Biol Chem 279 2004 4515 4522 (Pubitemid 38199042)
9. D. Egli, A. Selvaraj, H. Yepiskoposyan, B. Zhang, E. Hafen, and O. Georgiev Knockout of metal-responsive transcription factor MTF-1 in Drosophila by homologous recombination reveals its central role in heavy metal homeostasis EMBO J 22 2003 100 108 (Pubitemid 36091273)
10. D. Egli, H. Yepiskoposyan, A. Selvaraj, K. Balamurugan, R. Rajaram, and A. Simons A family knockout of all four Drosophila metallothioneins reveals a central role in copper homeostasis and detoxification Mol Cell Biol 26 2006 2286 2296 (Pubitemid 43346928)
11. T.A. Godenschwege, N. Pohar, S. Buchner, and E. Buchner Inflated wings, tissue autolysis and early death in tissue inhibitor of metalloproteinases mutants of Drosophila Eur J Cell Biol 79 2000 495 501 (Pubitemid 30612204)
12. C. Günes, R. Heuchel, O. Georgiev, K.H. Müller, P. Lichtlen, and H. Blüthmann Embryonic lethality and liver degeneration in mice lacking the metal-responsive transcriptional activator MTF-1 EMBO J 17 1998 2846 2854 (Pubitemid 28227131)
13. R. Heuchel, F. Radtke, O. Georgiev, G. Stark, M. Aguet, and W. Schaffner The transcription factor MTF-1 is essential for basal and heavy metal-induced metallothionein gene expression EMBO J 13 1994 2870 2875 (Pubitemid 24191697)
14. H. Hua, V. Günther, O. Georgiev, and W. Schaffner Distorted copper homeostasis with decreased sensitivity to cisplatin upon chaperone Atox1 deletion in Drosophila Biometals 24 2011 445 453
15. U. Kutay, and S. Güttinger Leucine-rich nuclear-export signals: born to be weak Trends Cell Biol 15 2005 121 124 (Pubitemid 40332533)
16. O. LaRochelle, V. Gagné, J. Charron, J.W. Soh, and C. Séguin Phosphorylation is involved in the activation of metal-regulatory transcription factor 1 in response to metal ions J Biol Chem 276 2001 41879 41888
17. U. Lindert, M. Cramer, M. Meuli, O. Georgiev, and W. Schaffner Metal-responsive transcription factor 1 (MTF-1) activity is regulated by a nonconventional nuclear localization signal and a metal-responsive transactivation domain Mol Cell Biol 29 2009 6283 6293
18. M.T. Marr 2nd, Y. Isogai, K.J. Wright, and R. Tjian Coactivator cross-talk specifies transcriptional output Genes Dev 20 2006 1458 1469 (Pubitemid 43830653)
19. N. Murai, Y. Murakami, and S. Matsufuji Identification of nuclear export signals in antizyme-1 J Biol Chem 278 2003 44791 44798 (Pubitemid 37377237)
20. F. Otsuka, A. Iwamatsu, K. Suzuki, M. Ohsawa, D.H. Hamer, and S. Koizumi Purification and characterization of a protein that binds to metal responsive elements of the human metallothionein IIA gene J Biol Chem 269 1994 23700 23707 (Pubitemid 24293577)
21. F. Otsuka, I. Okugaito, M. Ohsawa, A. Iwamatsu, K. Suzuki, and S. Koizumi Novel responses of ZRF, a variant of human MTF-1, to in vivo treatment with heavy metals Biochim Biophys Acta 1492 2000 330 340 (Pubitemid 30427344)
22. F. Radtke, O. Georgiev, H.P. Müller, E. Brugnera, and W. Schaffner Functional domains of the heavy metal-responsive transcription regulator MTF-1 Nucleic Acids Res 23 1995 2277 2286
23. F. Radtke, R. Heuchel, O. Georgiev, M. Hergersberg, M. Gariglio, and Z. Dembic Cloned transcription factor MTF-1 activates the mouse metallothionein I promoter EMBO J 12 1993 1355 1362 (Pubitemid 23112790)
24. N. Saydam, O. Georgiev, M.Y. Nakano, U.F. Greber, and W. Schaffner Nucleo-cytoplasmic trafficking of metal-regulatory transcription factor 1 is regulated by diverse stress signals J Biol Chem 276 2001 25487 25495
25. N. Saydam, T.K. Adams, F. Steiner, W. Schaffner, and J.H. Freedman Regulation of metallothionein transcription by the metal-responsive transcription factor MTF-1: identification of signal transduction cascades that control metal-inducible transcription J Biol Chem 277 2002 20438 20445 (Pubitemid 34967340)
26. E. Schreiber, P. Matthias, M.M. Müller, and W. Schaffner Rapid detection of octamer binding proteins with mini-extracts, prepared from a small number of cells Nucleic Acids Res 17 1989 6419 (Pubitemid 19198635)
27. K. Seipel, O. Georgiev, and W. Schaffner Different activation domains stimulate transcription from remote ('enhancer') and proximal ('promoter') positions EMBO J 11 1992 4961 4968 (Pubitemid 23023440)
28. A. Selvaraj, K. Balamurugan, H. Yepiskoposyan, H. Zhou, D. Egli, and O. Georgiev Metal-responsive transcription factor (MTF-1) handles both extremes, copper load and copper starvation, by activating different genes Genes Dev 19 2005 891 896 (Pubitemid 40548057)
29. H. Siomi, and G. Dreyfuss A nuclear localization domain in the hnRNP A1 protein J Cell Biol 129 1995 551 560
30. I.V. Smirnova, D.C. Bittel, R. Ravindra, H. Jiang, and G.K. Andrews Zinc and cadmium can promote rapid nuclear translocation of metal response element-binding transcription factor-1 J Biol Chem 275 2000 9377 9384 (Pubitemid 30185162)
31. D. Steiger, M. Fetchko, A. Vardanyan, L. Atanesyan, K. Steiner, and M.L. Turski The Drosophila copper transporter Ctr1C functions in male fertility J Biol Chem 285 2010 17089 17097
32. R.F. Weaver, and C. Weissmann Mapping of RNA by a modification of the Berk-Sharp procedure: the 5′ termini of 15 S beta-globin mRNA precursor and mature 10 s beta-globin mRNA have identical map coordinates Nucleic Acids Res 7 1979 1175 1193
33. G. Westin, T. Gerster, M.M. Müller, G. Schaffner, and W. Schaffner OVEC, a versatile system to study transcription in mammalian cells and cell-free extracts Nucleic Acids Res 15 1987 6787 6798
34. G. Westin, and W. Schaffner A zinc-responsive factor interacts with a metal-regulated enhancer element (MRE) of the mouse metallothionein-I gene EMBO J 7 1988 3763 3770
35. B. Zhang, D. Egli, O. Georgiev, and W. Schaffner The Drosophila homolog of mammalian zinc finger factor MTF-1 activates transcription in response to heavy metals Mol Cell Biol 21 2001 4505 4514 (Pubitemid 32588235)