Copper homeostasis in eukaryotes: Teetering on a tightrope

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1763, Issue 7, 2006, Pages 737-746

  Balamurugan, Kuppusamy ^a   Schaffner, Walter ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Copper detoxification; Copper importers; Copper load; Copper scarcity; Ctr1B; Metallothioneins; MTF 1

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; COPPER; METAL RESPONSIVE TRANSCRIPTION FACTOR 1; METALLOTHIONEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

DETOXIFICATION; DROSOPHILA; EUKARYOTE; HOMEOSTASIS; HUMAN; MAMMAL; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION; YEAST;

ANIMALS; COPPER; EUKARYOTIC CELLS; HOMEOSTASIS;

EUKARYOTA; HEXAPODA; LYCAENA VIRGAUREAE; MAMMALIA; PROKARYOTA;

EID: 33746889803     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2006.05.001     Document Type: Review

References (124)

1. Pena M.M., Lee J., and Thiele D.J. A delicate balance: homeostatic control of copper uptake and distribution. J. Nutr. 129 (1999) 1251-1260
2. Harris E.D. Cellular copper transport and metabolism. Annu. Rev. Nutr. 20 (2000) 291-310
3. Uauy R., Olivares M., and Gonzalez M. Essentiality of copper in humans. Am. J. Clin. Nutr. 67 (1998) 952S-959S
4. Koch K.A., Pena M.M., and Thiele D.J. Copper-binding motifs in catalysis, transport, detoxification and signaling. Chem. Biol. 4 (1997) 549-560
5. Bartsch H., and Nair J. Oxidative stress and lipid peroxidation-derived DNA-lesions in inflammation driven carcinogenesis. Cancer Detect. Prev. 28 (2004) 385-391
6. Valko M., Morris H., and Cronin M.T. Metals, toxicity and oxidative stress. Curr. Med. Chem. 12 (2005) 1161-1208
7. Uriu-Adams J.Y., and Keen C.L. Copper, oxidative stress, and human health. Mol. Aspects Med. 26 (2005) 268-298
8. Puig S., and Thiele D.J. Molecular mechanisms of copper uptake and distribution. Curr. Opin. Chem. Biol. 6 (2002) 171-180
9. Bertinato J., and Abbe M.R.L. Maintaining copper homeostasis: regulation of copper-trafficking proteins in response to copper deficiency or overload. J. Nutr. Biochem. 15 (2004) 316-322
10. Camakaris J., Voskoboinik I., and Mercer J.F. Molecular mechanisms of copper homeostasis. Biochem. Biophys. Res. Commun. 261 (1999) 225-232
11. Rutherford J.C., and Bird A.J. Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot. Cell 3 (2004) 1-13
12. Puig S., Lee J., Lau M., and Thiele D.J. Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J. Biol. Chem. 277 (2002) 26021-26030
13. Prohaska J.R., and Gybina A.A. Intracellular copper transport in mammals. J. Nutr. 134 (2004) 1003-1006
14. DiDonato M., and Sarkar B. Copper transport and its alterations in Menkes and Wilson diseases. Biochim. Biophys. Acta 1360 (1997) 3-16
15. Perry G., Sayre L.M., Atwood C.S., Castellani R.J., Cash A.D., Rottkamp C.A., and Smith M.A. The role of iron and copper in the aetiology of neurodegenerative disorders: therapeutic implications. CNS Drugs 16 (2002) 339-352
16. Shim H., and Harris Z.L. Genetic defects in copper metabolism. J. Nutr. 133 (2003) 1527S-1531S
17. Dhawan A., Ferenci P., Geubel A., Houwen R., Lerut J., and Sokal E. Genes and metals: a deadly combination. Acta Gastroenterol. Belg. 68 (2005) 26-32
18. Barceloux D.G., and Copper J. Toxicol. Clin. Toxicol 37 (1999) 217-230
19. Georgopoulos P.G., Roy A., Yonone-Lioy M.J., Opiekum R.E., and Lioy P.J. Environmental copper: its dynamics and human exposure issues. J. Toxicol. Environ. Health B Crit. Rev. 4 (2001) 341-394
20. Fox P.L. The copper-iron chronicles: the story of an intimate relationship. Biometals 16 (2003) 9-40
21. Van Ho A., Ward D.M., and Kaplan J. Transition metal transport in yeast. Annu. Rev. Microbiol. 56 (2002) 237-261
22. Harris E.D. Basic and clinical aspects of copper. Crit. Rev. Clin. Lab. Sci. 40 (2003) 547-586
23. Tanner M.S. Role of copper in Indian childhood cirrhosis. Am. J. Clin. Nutr. 67 (1998) 1074S-1081S
24. Muller T., Feichtinger H., Berger H., and Muller W. Endemic tyrolean infantile cirrhosis: an ecogenetic disorder. Lancet 347 (1996) 877-880
25. Muller T., Muller W., and Feichtinger H. Idiopathic copper toxicosis. Am. J. Clin. Nutr. 67 (1998) 1082S-1086S
26. Nittis T., and Gitlin J.D. The copper-iron connection: hereditary aceruloplasminemia. Semin. Hematol. 39 (2002) 282-289
27. Klomp A.E.M., van de Sluis B., Klomp L.W.J., and Wijmenga C. The ubiquitously expressed MURR1 protein is absent in canine copper toxicosis. J. Hepatol. 39 (2003) 703-709
28. Tao T.Y., Liu F., Klomp L., Wijmenga C., and Gitlin J.D. The copper toxicosis gene product Murr1 directly interacts with the Wilson disease protein. J. Biol. Chem. 278 (2003) 41593-41596
29. Mufti A.R., Burstein E., Csomos R.A., Graf P.C.F., Wilkinson J.C., Dick R.D., Challa M., Son J.-K., Bratton S.B., Su G.L., Brewer G.J., Jakob U., and Duckett C.S. XIAP Is a copper binding protein deregulated in Wilson's disease and other copper toxicosis disorders. Mol. Cell 21 (2006) 775-785
30. Bayer T.A., and Multhaup G. Involvement of amyloid beta precursor protein (AbetaPP) modulated copper homeostasis in Alzheimer's disease. J. Alzheimers Dis. 8 (2005) 201-206
31. Bush A.L. Metals and neuroscience. Curr. Opin. Chem. Biol. 4 (2000) 184-191
32. Maurer I., Zierz S., and Moller H.J. A selective defect of cytochrome c oxidase is present in brain of Alzheimer disease patients. Neurobiol. Aging 21 (2000) 455-462
33. Bayer T.A., Schafer S., Simons A., Kemmling A., Kamer T., Tepest R., Eckert A., Schüssel K., Eikenberg O., Sturchler-Pierrat C., Abramowski D., Staufenbiel M., and Multhaup G. Dietary Cu stabilizes brain superoxide dismutase 1 activity and reduces amyloid Abeta production in APP23 transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 14187-14192
34. Wand G.S., C.May V., May P.J., Whitehouse S.I., and Rapoport B.A. Alzheimer's disease: low levels of peptide alpha-amidation activity in brain and CSF. Neurology 37 (1987) 1057-1061
35. Brown D.R. Copper and prion diseases. Biochem. Soc. Trans. 30 (2002) 742-745
36. Erler J.T., Bennewith K.L., Nicolau M., Dornhöfer N., Kong C., Le Q.-T., Chi J.-T.A., Jeffrey S.S., and Giaccia A.J. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440 (2006) 1222-1226
37. Petris M.J. The SLC31 (Ctr) copper transporter family. Pflugers Arch. 447 (2004) 752-755
38. Valentine J.S., and Gralla E.B. Delivering copper inside yeast and human cells. Science 278 (1997) 817-818
39. Zhou B., and Gitschier J. hCTR1: a human gene for copper uptake identified by complementation in yeast. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 7481-7486
40. Zhou H., Cadigan K.M., and Thiele D.J. A Copper-regulated transporter required for copper acquisition, pigmentation, and specific stages of development in drosophila melanogaster. J. Biol. Chem. 278 (2003) 48210-48218
41. Sharp P.A. Ctr1 and its role in body copper homeostasis. Int. J. Biochem. Cell Biol. 35 (2003) 288-291
42. Rees E.M., and Thiele D.J. From aging to virulence: forging connections through the study of copper homeostasis in eukaryotic microorganisms. Curr. Opin. Microbiol. 7 (2004) 175-184
43. Guo Y., Smith K., Lee J., Thiele D.J., and Petris M.J. Identification of methionine-rich clusters that regulate copper-stimulated endocytosis of the human Ctr1 copper transporter. J. Biol. Chem. 279 (2004) 17428-17433
44. Jiang J., Nadas I.A., Kim M.A., and Franz K.J. A Mets motif peptide found in copper transport proteins selectively binds cu(i) with methionine-only coordination. Inorg. Chem. 44 (2005) 9787-9794
45. Pena M.M., Puig S., and Thiele D.J. Characterization of the Saccharomyces cerevisiae high affinity copper transporter Ctr3. J. Biol. Chem. 275 (2000) 33244-33251
46. Lee J., Pena M.M., Nose Y., and Thiele D.J. Biochemical characterization of the human copper transporter Ctr1. J. Biol. Chem. 277 (2002) 4380-4387
47. Rae T.D., Schmidt P.J., Pufahl R.A., Culotta V.C., and O'Halloran T.V. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284 (1999) 805-808
48. Rees E.M., Lee J., and Thiele D.J. Mobilization of intracellular copper stores by the ctr2 vacuolar copper transporter. J. Biol. Chem. 279 (2004) 54221-54229
49. Huang W.P., and Klionsky D.J. Autophagy in yeast: a review of the molecular machinery. Cell Struct. Funct. 27 (2002) 409-420
50. Eisses J.F., and Kaplan J.H. Molecular characterization of hCTR1, the human copper uptake protein. J. Biol. Chem. 277 (2002) 29162-29171
51. Selvaraj A., Balamurugan K., Yepiskoposyan H., Zhou H., Egli D., Georgiev O., Thiele D.J., and Schaffner W. Metal-responsive transcription factor (MTF-1) handles both extremes, copper load and copper starvation, by activating different genes. Genes Dev. 19 (2005) 891-896
52. Askwith C., Eide D., Van Ho A., Bernard P.S., Li L., Davsi-Kaplan S., Sipe D.M., and Kaplan J. The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76 (1994) 403-410
53. Ooi C.E., Rabinovich E., Dancis A., Bonifacino J.S., and Klausner R.D. Copper dependent degradation of the Saccharomyces cerevisiae plasma membrane copper transporter Ctr1p in the apparent absence of endocytosis. EMBO J. 15 (1996) 3515-3523
54. Egli D., Selvaraj A., Yepiskoposyan H., Zhang B., Hafen E., Georgiev O., and Schaffner W. 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
55. Lee J., Prohaska J.R., and Thiele D.J. Essential role for mammalian copper transporter Ctr1 in copper homeostasis and embryonic development. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 6842-6847
56. Kuo Y.M., Zhou B., Cosco D., and Gitschier J. The copper transporter CTR1 provides an essential function in mammalian embryonic development. Proc. Natl. Acad. Sci. U.S. A. 98 (2001) 6836-6841
57. Perafan-Riveros C., Franca L.F., Alves A.C., and Sanches Jr. J.A. Acrodermatitis enteropathica: case report and review of the literature. Pediatr. Dermatol. 19 (2002) 426-431
58. Harrison M.D., Jones C.E., Solioz M., and Dameron C.T. Intracellular copper routing: the role of copper chaperones. Trends Biochem. Sci. 25 (2000) 29-32
59. O'Halloran T.V., and Culotta V.C. Metallochaperones, an intracellular shuttle service for metal ions. J. Biol. Chem. 275 (2000) 25057-25060
60. Harrison M.D., Jones C.E., and Dameron C.T. Copper chaperones: function, structure and copper-binding properties. J. Biol. Inorg. Chem. 4 (1999) 145-153
61. Arnesano F., Banci L., Bertini I., Cantini F., Ciofi-Baffoni S., Huffman D.L., and O'Halloran T.V. Characterization of the binding interface between the copper chaperone Atx1 and the first cytosolic domain of Ccc2 ATPase. J. Biol. Chem. 276 (2001) 41365-41376
62. Walker J.M., Tsivkovskii R., and Lutsenko S. Metallochaperone Atox1 transfers copper to the NH2-terminal domain of the Wilson's disease protein and regulates its catalytic activity. J. Biol. Chem. 277 (2002) 27953-27959
63. Hellman N.E., and Gitlin J.D. Ceruloplasmin metabolism and function. Annu. Rev. Nutr. 22 (2002) 439-458
64. Cobine P., Wickramasinghe W.A., Harrison M.D., Weber T., Solioz M., and Dameron C.T. The Enterococcus hirae copper chaperone CopZ delivers copper(I) to the CopY repressor. FEBS Lett. 445 (1999) 27-30
65. Schmidt P.J., Kunst C., and Culotta V.C. Copper activation of superoxide dismutase 1 (SOD1) in vivo. Role for protein-protein interactions with the copper chaperone for SOD1. J. Biol. Chem. 275 (2000) 33771-33776
66. Wong P.C., Waggoner D., Subramaniam J.R., Tessarollo L., Bartnikas T.B., Culotta V.C., Price D.L., Rothstein J., and Gitlin J.D. Copper chaperone for superoxide dismutase is essential to activate mammalian Cu/Zn superoxide dismutase. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 2886-2891
67. Lamb A.L., Torres A.S., O'Halloran T.V., and Rosenzweig A.C. Heterodimer formation between superoxide dismutase and its copper chaperone. Biochemistry 39 (2000) 14720-14727
68. Horng Y.C., Cobine P.A., Maxfield A.B., Carr H.S., and Winge D.R. Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome C oxidase. J. Biol. Chem. 279 (2004) 35334-35340
69. Lode A., Kuschel M., Paret C., and Rodel G. Mitochondrial copper metabolism in yeast: interaction between Sco1p and Cox2p. FEBS Lett. 485 (2000) 19-24
70. Borghouts C., Werner A., Elthon T., and Osiewacz H.D. Copper-modulated gene expression and senescence in the filamentous fungus Podospora anserine. Mol. Cell. Biol. 21 (2001) 390-399
71. Williams J.C., Sue C., Banting G.S., Yang H., Glerum D.M., Hendrickson W.A., and Schon E.A. Crystal structure of human SCO1: implications for redox signaling by a mitochondrial cytochrome c oxidase "assembly" protein. J. Biol. Chem. 280 (2005) 15202-15211
72. Abajian C., Yatsunyk L.A., Ramirez B.E., and Rosenzweig A.C. Yeast cox17 solution structure and Copper(I) binding. J. Biol. Chem. 279 (2004) 53584-53592
73. Eisses J.F., Stasser J.P., Ralle M., Kaplan J.H., and Blackburn N.J. Domains I and III of the human copper chaperone for superoxide dismutase interact via a cysteine-bridged Dicopper(I) cluster. Biochemistry 39 (2000) 7337-7342
74. Wijmenga C., and Klomp L.W. Molecular regulation of copper excretion in the liver. Proc. Nutr. Soc. 63 (2004) 31-39
75. Solioz M., and Stoyanov J.V. Copper homeostasis in Enterococcus hirae. FEMS Microbiol. Rev. 27 (2003) 183-195
76. Vulpe C., Levinson B., Whitney S., Packman S., and Gitschier J. Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat. Genet. 3 (1993) 7-13
77. Voskoboinik I., and Camakaris J. Menkes copper-translocating P-type ATPase (ATP7A): biochemical and cell biology properties, and role in Menkes disease. J. Bioenerg. Biomembr. 34 (2002) 363-371
78. Voskoboinik I., Mar J., Strausak D., and Camakaris J. The regulation of catalytic activity of the Menkes copper-translocating P-type ATPase. Role of high affinity copper-binding sites. J. Biol. Chem. 276 (2001) 28620-28627
79. Suzuki M., and Gitlin J.D. Intracellular localization of the Menkes and Wilson's disease proteins and their role in intracellular copper transport. Pediatr. Int. 41 (1999) 436-442
80. Bull P.C., Thomas G.R., Rommens J.M., Forbes J.R., and Cox D.W. The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat. Genet. 5 (1993) 327-337
81. Vanderwerf S.M., Cooper M.J., Stetsenko I.V., and Lutsenko S. Copper specifically regulates intracellular phosphorylation of the Wilson's disease protein, a human copper-transporting ATPase. J. Biol. Chem. 276 (2001) 36289-36294
82. Oude Elferink R.O., and Groen A.K. Genetic defects in hepatobiliary transport. Biochim. Biophys. Acta 1586 (2002) 129-145
83. Brewer G.J., and Askari F.K. Wilson's disease: clinical management and therapy. J. Hepatol. 42 (2005) S13-S21
84. Southon A., Burke R., Norgate M., Batterham P., and Camakaris J. Copper homoeostasis in Drosophila melanogaster S2 cells. Biochem. J. 383 (2004) 303-309
85. Norgate M., Lee E., Southon A., Farlow A., Batterham P., Camakaris J., and Burke R. Essential roles in development and pigmentation for the Drosophila copper transporter DmATP7. Mol. Biol. Cell 17 (2006) 475-484
86. Petris M.J., Smith K., Lee J., and Thiele D.J. Copper-stimulated endocytosis and degradation of the human copper transporter, hCtr1. J. Biol. Chem. 278 (2003) 9639-9646
87. Kägi J.H.R. Overview of metallothionein. Methods Enzymol. 205 (1991) 613-626
88. Palmiter R.D. The elusive function of metallothioneins. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 8428-8430
89. Turner J.S., and Robinson N.J. Cyanobacterial metallothioneins: biochemistry and molecular genetics. J. Ind. Microbiol. 14 (1995) 119-125
90. Ecker D.J., Butt T.R., Sternberg E.J., Neeper M.P., Debouck C., Gorman J.A., and Crooke S.T. Yeast metallothionein function in metal ion detoxification. J. Biol. Chem. 261 (1986) 16890-16895
91. Andrews G.K. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem. Pharmacol. 59 (2000) 95-104
92. Bonneton F., Theodore L., Silar P., Maroni G., and Wegnez M. Response of Drosophila metallothionein promoters to metallic, heat shock and oxidative stresses. FEBS Lett. 380 (1996) 33-38
93. Culotta V.C., Howard W.R., and Liu X.F. CRS5 encodes a metallothionein-like protein in Saccharomyces cerevisiae. J. Biol. Chem. 269 (1994) 25295-25302
94. Jensen L.T., Howard W.R., Strain J.J., Winge D.R., and Culotta V.C. Enhanced effectiveness of copper ion buffering by CUP1 metallothionein compared with CRS5 metallothionein in Saccharomyces cerevisiae. J Biol. Chem. 271 (1996) 18514-18519
95. Pena M.M., Koch K.A., and Thiele D.J. Dynamic regulation of copper uptake and detoxification genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 18 (1998) 2514-2523
96. Lastowski-Perry D., Otto E., and Maroni G. Nucleotide sequence and expression of a Drosophila metallothionein. J. Biol. Chem. 260 (1985) 1527-1530
97. Maroni G., Otto E., and Lastowski-Perry D. Molecular and cytogenetic characterization of a metallothionein gene of Drosophila. Genetics 112 (1986) 493-504
98. Silar P., Theodore L., Mokdad R., Erraiss N.E., Cadic A., and Wegnez M. Metallothionein Mto gene of Drosophila melanogaster: structure and regulation. J. Mol. Biol. 215 (1990) 217-224
99. Egli D., Yepiskoposyan H., Selvaraj A., Balamurugan K., Rajaram R., Simons A., Multhaup G., Mettler S., Vardanyan A., Georgiev O., and Schaffner W. A family knockout of all four Drosophila metallothioneins reveals a central role in copper homeostasis and detoxification. Mol. Cell. Biol. 26 (2006) 2286-2296
100. Filshie B.K., Poulson D.F., and Waterhouse D.F. Ultrastructure of the copper-accumulating region of the Drosophila larval midgut. Tissue Cell 3 (1971) 77-102
101. Lauverjat S., Ballan-Dufrancais C., and Wegnez M. Detoxification of cadmium. Ultrastructural study and electron-probe microanalysis of the midgut in a cadmium-resistant strain of Drosophila melanogaster. Biol. Met. 2 (1989) 97-107
102. Egli D., Domenech J., Selvaraj A., Balamurugan K., Hua H., Capdevila M., Georgiev O., Schaffner W., and Atrian S. The four members of the Drosophila metallothionein family exhibit distinct yet overlapping roles in heavy metal homeostasis and detoxification. Genes Cells 11 (2006) 647-648
103. Durnam D.M., and Palmiter R.D. Analysis of the detoxification of heavy metal ions by mouse metallothionein. Experientia, Suppl. 52 (1987) 457-463
104. Aschner M., Cherian M.G., Klaassen C.D., Palmiter R.D., Erickson J.C., and Bush A.I. Metallothioneins in brain-The role in physiology and pathology. Toxicol. Appl. Pharmacol. 142 (1997) 229-242
105. Quaife C.J., Findley S.D., Erickson J.C., Froelick G.J., Kelly E.J., Zambrowicz B.P., and Palmiter R.D. Induction of a new metallothionein isoform (MT-IV) occurs during differentiation of stratified squamous epithelia. Biochemistry 33 (1994) 7250-7259
106. Doz F., Roosen N., and Rosenblum M.L. Metallothionein and anticancer agents: the role of metallothionein in cancer chemotherapy. J. Neurooncol. 17 (1993) 123-129
107. Lichtlen P., and Schaffner W. Putting its fingers on stressful situations: the heavy metal-regulatory transcription factor MTF-1. BioEssays 23 (2001) 1010-1017
108. Thiele D.J. ACE1 regulates expression of the Saccharomyces cerevisiae metallothionein gene. Mol. Cell. Biol. 8 (1988) 2745-2752
109. Zhu Z., and Thiele D.J. Toxic metal-responsive gene transcription. EXS 77 (1996) 307-320
110. Jensen LT., Posewitz M.C., Srinivasan C., and Winge D.R. Mapping of the DNA binding domain of the copper-responsive transcription factor Mac1 from Saccharomyces cerevisiae. J. Biol. Chem. 273 (1998) 23805-23811
111. Winge D.R. Copper-regulatory domain involved in gene expression. Prog. Nucleic Acid Res. Mol. Biol. 58 (1998) 165-195
112. Keller G., Bird A., and Winge D.R. Independent metalloregulation of Ace1 and Mac1 in Saccharomyces cerevisiae. Eukaryot. Cell 4 (2005) 1863-1871
113. Beaudoin J., Mercier A., Langlois R., and Labbé S. The Schizosaccharomyces pombe cuf1 is composed of functional modules from two distinct classes of copper metalloregulatory transcription factors. J. Biol. Chem. 278 (2003) . 14565-14577
114. Heuchel R., Radtke F., Georgiev O., Stark G., Aguet M., and Schaffner W. The transcription factor MTF-1 is essential for basal and heavy metal-induced metallothionein gene expression. EMBO J. 13 (1994) 2870-2875
115. Auf der Maur A., Belser T., Elgar G., Georgiev O., and Schaffner W. Characterization of the transcription factor MTF-1 from the Japanese pufferfish (Fugu rubripes) reveals evolutionary conservation of heavy metal stress response. Biol. Chem. 380 (1999) 175-185
116. Zhang B., Egli D., Georgiev O., and Schaffner W. The Drosophila homolog of mammalian zinc finger factor MTF-1 activates transcription in response to heavy metals. Mol. Cell. Biol. 21 (2001) 4505-4514
117. Giedroc D.P., Chen X., and Apuy J.L. Metal response element (MRE)-binding transcription factor-1 (MTF-1): structure, function and regulation. Antioxid. Redox Signal. 3 (2001) 577-596
118. 2 in vitro is modulated by metallothionein. Mol. Cell. Biol. 23 (2003) 8471-8485
119. Bittel D., Dalton T., Samson S.L., Gedamu L., and Andrews G.K. 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 (1998) 7127-7133
120. Saydam N., Georgiev O., Nakano M.Y., Greber U.F., and Schaffner W. Nucleo-cytoplasmic trafficking of metal-regulatory transcription factor 1 is regulated by diverse stress signals. J. Biol. Chem. 276 (2001) 25487-25495
121. Saydam N., Adams T.K., Steiner F., Schaffner W., and Freedman J.H. 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
122. Radtke F., Georgiev O., Müller H.P., Brugnera E., and Schaffner W. Functional domains of the heavy metal-responsive transcription regulator MTF-1. Nucleic Acids Res. 23 (1995) 2277-2286
123. Balamurugan K., Egli D., Selvaraj A., Zhang B., Georgiev O., and Schaffner W. 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
124. Ciriolo M.R., Desideri A., Paci M., and Rotilio G. Reconstitution of Cu,Zn-superoxide dismutase by the Cu(I).glutathione complex. J. Biol. Chem. 265 (1990) 11030-11034