Activity of Metal-Responsive Transcription Factor 1 by Toxic Heavy Metals and H2O2 in Vitro Is Modulated by Metallothionein

Molecular and Cellular Biology

Volumn 23, Issue 23, 2003, Pages 8471-8485

  Zhang, Bo ^a   Georgiev, Oleg ^a   Hagmann, Michael ^a   Günes, Çagatay ^a,b   Cramer, Mirjam ^a   Faller, Peter ^a,c   Vasák, Milan ^a   Schaffner, Walter ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CADMIUM; COPPER; HEAVY METAL; HYDROGEN PEROXIDE; METAL RESPONSIVE TRANSCRIPTION FACTOR 1; METALLOTHIONEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZINC; ZINC FINGER PROTEIN;

ARTICLE; BINDING SITE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA BINDING; DNA RESPONSIVE ELEMENT; EMBRYO; GENE ACTIVATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; OXIDATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; REPORTER GENE; TRANSCRIPTION INITIATION;

ANIMALS; CADMIUM; CELL LINE; CELL-FREE SYSTEM; COPPER; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; HYDROGEN PEROXIDE; METALLOTHIONEIN; METALS, HEAVY; MODELS, BIOLOGICAL; OXIDATIVE STRESS; PROMOTER REGIONS (GENETICS); RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; ZINC;

EID: 0242637400     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.23.8471-8485.2003     Document Type: Article

References (81)

1. Adilakshmi, T., and R. O. Laine. 2002. Ribosomal protein S25 mRNA partners with MTF-1 and La to provide a p53-mediated mechanism for survival or death. J. Biol. Chem. 277:4147-4151.
2. Andrews, G. K. 2000. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem. Pharmacol. 59:95-104.
3. Andrews, G. K., D. K. Lee, R. Ravindra, P. Lichtlen, M. Sirito, M. Sawadogo, and W. Schaffner. 2001. The transcription factors MTF-1 and USF1 cooperate to regulate mouse metallothionein-I expression in response to the essential metal zinc in visceral endoderm cells during early development. EMBO J. 20:1114-1122.
4. Apuy, J. L., X. Chen, D. H. Russell, T. O. Baldwin, and D. P. Giedroc. 2001. Ratiometric pulsed alkylation/mass spectrometry of the cysteine pairs in individual zinc fingers of MRE-binding transcription factor-1 (MTF-1) as a probe of zinc chelate stability. Biochemistry 40:15164-15175.
5. Arnosti, D. N., A. Merino, D. Reinberg, and W. Schaffner. 1993. Oct-2 facilitates functional preinitiation complex assembly and is continuously required at the promoter for multiple rounds of transcription. EMBO J. 12:157-166.
6. Bird, A. J., H. Zhao, H. Luo, L. T. Jensen, C. Srinivasan, M. Evans-Galea, D. R. Winge, and D. J. Eide. 2000. A dual role for zinc fingers in both DNA binding and zinc sensing by the Zapl transcriptional activator. EMBO J. 19:3704-3713.
7. Bittel, D., T. Dalton, S. L. Samson, L. Gedamu, and G. K. Andrews. 1998. The DNA binding activity of metal response element-binding transcription factor-1 is activated in vivo and in vitro by zinc, but not by other transition metals. J. Biol. Chem. 273:7127-7133.
8. a. Brown, K. R., G. I. Keller, I. J. Pickering, H. H. Harris, G. N. George, and D. R. Woinge. 2002. Structures of cuprous-thiolate clusters of the Macl and Acel transcriptional activators. Biochemistry 41:6469-6476.
9. Brugnera, E., O. Georgiev, F. Radtke, R. Heuchel, E. Baker, G. R. Sutherland, and W. Schaffner. 1994. Cloning, chromosomal mapping and characterization of the human metal-regulatory transcription factor MTF-1. Nucleic Acids Res. 22:3167-3173.
10. Buhler, R. H., and J. H. Kagi. 1974. Human hepatic metallothioneins. FEBS Lett. 39:229-234.
11. Cano-Gauci, D. F., and B. Sarkar. 1996. Reversible zinc exchange between metallothionein and the estrogen receptor zinc finger. FEBS Lett. 386:1-4.
12. Chen, X., M. Chu, and D. P. Giedroc. 1999. MRE-Binding transcription factor-1: weak zinc-binding finger domains 5 and 6 modulate the structure, affinity, and specificity of the metal-response element complex. Biochemistry 38:12915-12925.
13. Culotta, V. C., and D. H. Hamer. 1989. Fine mapping of a mouse metallothionein gene metal response element. Mol. Cell. Biol. 9:1376-1380.
14. Culotta, V. C., T. Hsu, S. Hu, P. Furst, and D. Hamer. 1989. Copper and the ACE1 regulatory protein reversibly induce yeast metallothionein gene transcription in a mouse extract. Proc. Natl. Acad. Sci. 86:8377-8381.
15. Dalton, T., R. D. Palmiter, and G. K. Andrews. 1994. Transcriptional induction of the mouse metallothionein-I gene in hydrogen peroxide-treated Hepa cells involves a composite major late transcription factor/antioxidant response element and metal response promoter elements. Nucleic Acids Res. 22:5016-5023.
16. Dalton, T. P., D. Bittel, and G. K. Andrews. 1997. Reversible activation of mouse metal response element-binding transcription factor 1 DNA binding involves zinc interaction with the zinc finger domain. Mol. Cell. Biol. 17:2781-2789.
17. Dalton, T. P., Q. Li, D. Bittel, L. Liang, and G. K. Andrews. 1996. Oxidative stress activates metal-responsive transcription factor-1 binding activity. Occupancy in vivo of metal response elements in the metallothionein-I gene promoter. J. Biol. Chem. 271:26233-26241.
18. Daniels, P. J., D. Bittel, I. V. Smirnova, D. R. Winge, and G. K. Andrews. 2002. Mammalian metal response element-binding transcription factor-1 functions as a zinc sensor in yeast, but not as a sensor of cadmium or oxidative stress. Nucleic Acids Res. 30:3130-3140.
19. Datta, P. K., and S. T. Jacob. 1997. Activation of the metallothionein-I gene promoter in response to cadmium and USF in vitro. Biochem. Biophys. Res. Commun. 230:159-163.
20. Davis, S. R., and R. J. Cousins. 2000. Metallothionein expression in animals: a physiological perspective on function. J. Nutr. 130:1085-1088.
21. Furst, P., S. Hu, R. Hackett, and D. Hamer. 1988. Copper activates metallothionein gene transcription by altering the conformation of a specific DNA binding protein. Cell 55:705-717.
22. Giedroc, D. P., X. Chen, and J. L. Apuy. 2001. Metal response element (MRE)-binding transcription factor-1 (MTF-1): structure, function, and regulation. Antioxid. Redox Signal. 3:577-596.
23. Giedroc, D. P., X. Chen, M. A. Pennella, and A. C. LiWang. 2001. Conformational heterogeneity in the C-terminal zinc fingers of human MTF-1: an NMR and zinc-binding study. J. Biol. Chem. 276:42322-42332.
24. Green, C. J., P. Lichtlen, N. T. Huynh, M. Yanovsky, K. R. Laderoute, W. Schaffner, and B. J. Murphy. 2001. Placenta growth factor gene expression is induced by hypoxia in fibroblasts: a central role for metal transcription factor-1. Cancer Res. 61:2696-2703.
25. Gunes, C., R. Heuchel, O. Georgiev, K. H. Muller, P. Lichtlen, H. Bluthmann, S. Marino, A. Aguzzi, and W. Schaffner. 1998. Embryonic lethality and liver degeneration in mice lacking the metal-responsive transcriptional activator MTF-1. EMBO J. 17:2846-2854.
26. Hentze, M. W., and L. C. Kuhn. 1996. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. 93:8175-8182.
27. Heuchel, R., F. Radtke, O. Georgiev, G. Stark, M. Aguet, and W. Schaffner. 1994. The transcription factor MTF-1 is essential for basal and heavy metal-induced metallothionein gene expression. EMBO J. 13:2870-2875.
28. Hidalgo, J., M. Aschner, P. Zatta, and M. Vasak. 2001. Roles of the metallothionein family of proteins in the central nervous system. Brain Res. Bull. 55:133-145.
29. Hider, R. C., D. Bittel, and G. K. Andrews. 1999. Competition between iron (III)-selective chelators and zinc finger domains for zinc(II). Biochem. Pharmacol. 57:1031-1035.
30. Jacob, S. T., K. Ghoshal, and J. F. Sheridan. 1999. Induction of metallothionein by stress and its molecular mechanisms. Gene Expr. 7:301-310.
31. Jiang, H., P. J. Daniels, and G. K. Andrews. 2003. Putative zinc-sensing zinc fingers of metal response element-binding transcription factor-1 stabilize a metal-dependent chromatin complex on the endogenous metallothionein-I promoter. J. Biol. Chem. 278:30394-30402.
32. Jimenez, I., M. Gotteland, A. Zarzuelo, R. Uauy, and H. Speisky. 1997. Loss of the metal binding properties of metallothionein induced by hydrogen peroxide and free radicals. Toxicology 120:37-46.
33. Kimura, T., N. Itoh, M. Takehara, I. Oguro, J. Ishizaki, T. Nakanishi, and K. Tanaka. 2002. MRE-binding transcription factor-1 is activated during endotoxemia: a central role for metallothionein. Toxicol. Lett. 129:77-84.
34. Kobayashi, H., Y. Uchida, Y. Ihara, K. Nakajima, S. Kohsaka, T. Miyatake, and S. Tsuji. 1993. Molecular cloning of rat growth inhibitory factor cDNA and the expression in the central nervous system. Brain Res. Mol. Brain Res. 19:188-194.
35. Langmade, S. J., R. Ravindra, P. J. Daniels, and G. K. Andrews. 2000. The transcription factor MTF-1 mediates metal regulation of the mouse ZnT1 gene. J. Biol. Chem. 275:34803-34809.
36. LaRochelle, O., V. Gagne, J. Charron, J. W. Soh, and C. Seguin. 2001. Phosphorylation is involved in the activation of metal-regulatory transcription factor 1 in response to metal ions. J. Biol. Chem. 276:41879-41888.
37. Li, Q., N. Hu, M. A. Daggett, W. A. Chu, D. Bittel, J. A. Johnson, and G. K. Andrews. 1998. Participation of upstream stimulator factor (USF) in cadmium-induction of the mouse metallothionein-I gene. Nucleic Acids Res. 26:5182-5189.
38. Lichtlen, P., Y. Wang, T. Belser, O. Georgiev, U. Certa, R. Sack, and W. Schaffner. 2001. Target gene search for the metal-responsive transcription factor MTF-1. Nucleic Acids Res. 29:1514-1523.
39. Lichtlen, P., and W. Schaffner. 2001. Putting its fingers on stressful situations: the heavy metal-regulatory transcription factor MTF-1. Bioassays 23:1010-1017.
40. Masters, B. A., E. J. Kelly, C. J. Quaife, R. L. Brinster, and R. D. Palmiter. 1994. Targeted disruption of metallothionein I and II genes increases sensitivity to cadmium. Proc. Natl. Acad. Sci. 91:584-588.
41. Matsuo, K., J. Silke, O. Georgiev, P. Marti, N. Giovannini, and D. Rungger. 1998. An embryonic demethylation mechanism involving binding of transcription factors to replicating DNA. EMBO J. 17:1446-1453.
42. Mueller, P. R., S. J. Salser, and B. Wold. 1988. Constitutive and metal-inducible protein:DNA interactions at the mouse metallothionein I promoter examined by in vivo and in vitro footprinting. Genes Dev. 2:412-427.
43. Mueller-Storm, H. P., J. M. Sogo, and W. Schaffner. 1989. An enhancer stimulates transcription in trans when attached to the promoter via a protein bridge. Cell 58:767-777.
44. Muller, H. P., Brugnera, E., Georgiev, O., Badzong, M., Müller, K. H., and Schaffner, W. 1995. Analysis of the heavy metal-responsive transcription factor MTF-1 from human and mouse. Somat. Cell Mol. Genet. 21:289-297.
45. Muller, M. M., S. Ruppert, W. Schaffner, and P. Matthias. 1988. A cloned octamer transcription factor stimulates transcription from lymphoid-specific promoters in non-B cells. Nature 336:544-551.
46. Murata, M., P. Gong, K. Suzuki, and S. Koizumi. 1999. Differential metal response and regulation of human heavy metal-inducible genes. J. Cell Physiol. 180:105-113.
47. Murphy, B. J., G. K. Andrews, D. Bittel, D. J. Discher, J. McCue, C. J. Green, M. Yanovsky, A. Giaccia, R. M. Sutherland, K. R. Laderoute, and K. A. Webster. 1999. Activation of metallothionein gene expression by hypoxia involves metal response elements and metal transcription factor-1. Cancer Res. 59:1315-1322.
48. Ogra, Y., K. Suzuki, P. Gong, F. Otsuka, and S. Koizumi. 2001. Negative regulatory role of Sp1 in metal responsive element-mediated transcriptional activation. J. Biol. Chem. 276:16534-16539.
49. Onosaka, S., K. S. Min, C. Fukuhara, K. Tanaka, S. Tashiro, I. Shimizu, M. Furuta, T. Yasutomi, K. Kobashi, and K. Yamamoto. 1986. Concentrations of metallothionein and metals in malignant and non-malignant tissues in human liver. Toxicology 38:261-268.
50. Palmiter, R. D. 1998. The elusive function of metallothioneins. Proc. Natl. Acad. Sci. 95:8428-8430.
51. Palmiter, R. D. 1994. Regulation of metallothionein genes by heavy metals appears to be mediated by a zinc-sensitive inhibitor that interacts with a constitutively active transcription factor, MTF-1. Proc. Natl. Acad. Sci. 91:1219-1223.
52. Palmiter, R. D., S. D. Findley, T. E. Whitmore, and D. M. Durnam. 1992. MT-III, a brain-specific member of the metallothionein gene family. Proc. Natl. Acad. Sci. 89:6333-6337.
53. Pena, M. M., K. A. Koch, and D. J. Thiele. 1998. Dynamic regulation of copper uptake and detoxification genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:2514-2523.
54. Quaife, C. J., S. D. Findley, J. C. Erickson, G. J. Froelick, E. J. Kelly, B. P. Zambrowicz, and R. D. Palmiter. 1994. Induction of a new metallothionein isoform (MT-IV) occurs during differentiation of stratified squamous epithelia. Biochemistry 33:7250-7259.
55. Quesada, A. R., R. W. Byrnes, S. O. Krezoski, and D. H. Petering. 1996. Direct reaction of H2O2 with sulfhydryl groups in HL-60 cells: zinc-metallothionein and other sites. Arch. Biochem. Biophys. 334:241-250.
56. Radtke, F., R. Heuchel, O. Georgiev, M. Hergersberg, M. Gariglio, Z. Dembic, and W. Schaffner. 1993. Cloned transcription factor MTF-1 activates the mouse metallothionein I promoter. EMBO J. 12:1355-1362.
57. Roesijadi, G., R. Bogumil, M. Vasak, and J. H. Kagi. 1998. Modulation of DNA binding of a tramtrack zinc finger peptide by the metallothioneinthionein conjugate pair. J. Biol. Chem. 273:17425-17432.
58. Rouault, T., and R. Klausner. 1997. Regulation of iron metabolism in eukaryotes. Curr. Top. Cell Regul. 35:1-19.
59. Saydam, N., T. K. Adams, F. Steiner, W. Schaffner, and J. H. Freedman. 2002. 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. 277:20438-20445.
60. Saydam, N., O. Georgiev, M. Y. Nakano, U. F. Greber, and W. Schaffner. 2001. Nucleo-cytoplasmic trafficking of metal-regulatory transcription factor 1 is regulated by diverse stress signals. J. Biol. Chem. 276:25487-25495.
61. Schreiber, E., P. Matthias, M. M. Muller, and W. Schaffner. 1989. Rapid detection of octamer binding proteins with mini-extracts prepared from a small number of cells. Nucleic Acids Res. 17:6419.
62. Searle, P. F. 1990. Zinc dependent binding of a liver nuclear factor to metal response element MRE-a of the mouse metallothionein-I gene and variant sequences. Nucleic Acids Res. 18:4683-4690.
63. Smirnova, I. V., D. C. Bittel, R. Ravindra, H. Jiang, G. K. Andrews. 2000. Zinc and cadmium can promote rapid nuclear translocation of metal response element-binding transcription factor-1. J. Biol. Chem. 275:9377-9384.
64. Stillman, M. J. 1995. Metallothioneins. Coord. Chem. Rev. 144:461-511.
65. Stuart, G. W., P. F. Searle, and R. D. Palmiter. 1985. Identification of multiple metal regulatory elements in mouse metallothionein-I promoter by assaying synthetic sequences. Nature 317:828-831.
66. Thiele, D. J. 1988. ACE1 regulates expression of the Saccharomyces cerevisiae metallothionein gene. Mol. Cell. Biol. 8:2745-2752.
67. Vallee, B. L., and K. H. Falchuk. 1993. The biochemical basis of zinc physiology. Physiol. Rev. 73:79-118.
68. Vanacore, R. M., J. D. Eskew, P. J. Morales, L. Sung, and A. Smith. 2000. Role for copper in transient oxidation and nuclear translocation of MTF-1, but not of NF-kappa B, by the heme-hemopexin transport system. Antioxid. Redox Signal. 2:739-752.
69. Vasak, M. 1991. Metal removal and substitution in vertebrate and invertebrate metallothioneins. Methods Enzymol. 205:452-458.
70. Vasak, M. 1991. Standard isolation procedure for metallothionein. Methods Enzymol. 205:41-44.
71. Vasak, M., and D. W. Hasler. 2000. Metallothioneins: new functional and structural insights. Curr. Opi. Chem. Biol. 4:177-183.
72. Vasak, M., and J. H. Kagi. 1994. Metallothioneins, vol. 4. Wiley and Sons, Chichester, England.
73. Weaver, R. F., and C. Weissmann. 1979. 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. 7:1175-1193.
74. Westin, G., T. Gerster, M. M. Müller, G. Schaffner, and W. Schaffner. 1987. OVEC, a versatile system to study transcription in mammalian cells and cell-free extracts. Nucleic Acids Res. 15:6787-6798.
75. Westin, G., and W. Schaffner. 1988. Heavy metal ions in transcription factors from HeLa cells: Sp1, but not octamer transcription factor requires zinc for DNA binding and for activator function. Nucleic Acids Res. 16:5771-5781.
76. Westin, G., and W. Schaffner. 1988. A zinc-responsive factor interacts with a metal-regulated enhancer element (MRE) of the mouse metallothionein-I gene. EMBO J. 7:3763-3770.
77. Winge, D. R. 1998. Copper-regulatory domain involved in gene expression. Prog. Nucleic Acid Res. Mol. Biol. 58:165-195.
78. Yagle, M. K., and R. D. Palmiter. 1985. Coordinate regulation of mouse metallothionein I and II genes by heavy metals and glucocorticoids. Mol. Cell. Biol. 5:291-294.
79. Zeng, J., R. Heuchel, W. Schaffner, and J. H. Kagi. 1991. Thionein (apometallothionein) can modulate DNA binding and transcription activation by zinc finger containing factor Sp1. FEBS Lett. 279:310-312.
80. Zeng, J., B. L. Vallee, and J. H. Kagi. 1991. Zinc transfer from transcription factor IIIA fingers to thionein clusters. Proc. Natl. Acad. Sci. 88:9984-9988.
81. Zhang, B., D. Egli, O. Georgiev, and W. Schaffner. 2001. The Drosophila homolog of mammalian zinc finger factor MTF-1 activates transcription in response to heavy metals. Mol. Cell. Biol. 21:4505-4514.