Cytotoxicities and induction of metallothionein (MT) and metal regulatory element (MRE)-binding transcription factor-1 (MTF-1) messenger RNA levels in the zebrafish (Danio rerio) ZFL and SJD cell lines after exposure to various metal ions

Aquatic Toxicology

Volumn 89, Issue 2, 2008, Pages 103-112

  Cheuk, Wai Ka ^a   Chan, Patrick Chung Yiu ^a   Chan, King Ming ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Gene expression; In vitro toxicity; LC50 values of metal ions; Molecular mechanism; Real time PCR

Indexed keywords

ARSENIC; CADMIUM; CHROMIUM; COPPER ION; HEAVY METAL; MERCURY; MESSENGER RNA; METAL REGULATORY ELEMENT BINDING TRANSCRIPTION FACTOR 1; METALLOTHIONEIN; RNA; TRANSCRIPTION FACTOR; ZINC ION;

CONCENTRATION (COMPOSITION); CYPRINID; CYTOLOGY; GENE EXPRESSION; METALLOTHIONEIN; POLYMERASE CHAIN REACTION; RNA; TOXICITY TEST;

ANIMAL CELL; ARTICLE; CELL LINE; CONCENTRATION (PARAMETERS); CYTOTOXICITY; GENE INDUCTION; LC 50; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; ZEBRA FISH;

ANIMALS; CELL LINE; CELL SURVIVAL; DNA-BINDING PROTEINS; GENE EXPRESSION; METALLOTHIONEIN; METALS, HEAVY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 48549090813     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2008.06.006     Document Type: Article

References (82)

1. Adams T.K., and Freedman J.H. Regulation of metallothionein transcription. In: Centeno J.A., Collery P., Vermet G., Finkelman R.B., Gibb H., and Etienne J.-C. (Eds). Metal Ions in Biology and Medicine (2000), John Libbey Eurotext, Montrouge 694-697
2. Adams T.K., Saydam N., Steiner F., Schaffner W., and Freedman J.H. Activation of gene expression by metal-responsive signal transduction pathways. Environ. Health Perspect. 110 Suppl 5 (2002) 813-817
3. Amiard J.C., Amiard-Triquet C., Barka S., Pellerin J., and Rainbow P.S. Metallothioneins in aquatic invertebrates: Their role in metal detoxification and their use as biomarkers. Aquat. Toxicol. 75 (2006) 160-202
4. Andrews G.K. Regulation of metallothionein gene expression. Prog. Food Nutr. Sci. 14 (1990) 193-225
5. Andrews G.K. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem. Pharmacol. 59 (2000) 95-104
6. Andrews G.K. Cellular zinc sensors: MTF-1 regulation of gene expression. Biometals 14 (2001) 223-237
7. 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
8. Auf der Maur A., Belser T., Wang Y., Günes C., Lichtlen P., Georgiev O., and Schaffner W. Characterization of the mouse gene for the heavy metal-responsive transcription factor MTF-1. Cell Stress Chaperones 5 (2000) 196-206
9. Bertin G., and Averbeck D. Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88 (2006) 1549-1559
10. Berg J.M. Zinc fingers and other metal-binding domains: elements for interactions between macromolecules. J. Biol. Chem. 265 (1990) 6513-6516
11. Bertolero F., Pozzi G., Sabbioni E., and Saffiotti U. Cellular uptake and metabolic reduction of penta-valent to trivalent arsenic as determinants of cytotoxicity and morphological transformation. Carcinogenesis 8 (1987) 803-808
12. 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
13. Bittel D.C., Smienova I.V., and Andrews G.K. Functional heterogeneity in the zinc fingers of metalloregulatory protein metal response element-binding transcription factor-1. J. Biol. Chem. 275 (2000) 37194-37201
14. Borgono J.M., Vicent P., Venturino H., and Infante A. Arsenic in the drinking water of the city of Antofagasta: epidemiological and clinical study before and after the installation of a treatment plant. Environ. Health Perspect. 19 (1977) 103-105
15. Bourdineaud J.-P., Baudrimont M., Gonzalez J., and Moreau L. Challenging the model for induction of metallothionein gene expression. Biochemie 88 (2006) 1787-1792
16. Brugnera E., Georgiev O., Radtke F., Heuchel R., Baker E., Sutherland G.R., and Schaffner W. Cloning, chromosomal mapping and characterization of the human metal-regulatory transcription factor MTF-1. Nucleic Acids Res. 22 (1994) 3167-3173
17. Carvan III M.J., Solis W.A., Gedamu L., and Nebert D.W. Activation of transcription factors in zebrafish cell cultures by environmental pollutants. Arch. Biochem. Biophys. 376 (2000) 320-327
18. Casadevall M., and Kortenkamp A. Chromium and cancer. In: Sarkar B. (Ed). Heavy Metals in the Environment (2002), Marcel Dekker, New York 271-309
19. Chan K.M., Davidson W.S., Hew C.L., and Fletcher G.L. Molecular cloning of metallothionein cDNA and analysis of metallothionein gene expression in winter flounder tissues. Can. J. Zool. 67 (1989) 2520-2527
20. Chan K.M. PCR-cloning of goldfish and tilapia metallothionein complementary DNAs. Biochem. Biophys. Res. Commun. 205 (1994) 368-374
21. Chan K.M. Metallothionein: potential biomarker for monitoring heavy metal pollution in fish around Hong Kong. Mar. Pollut. Bull. 31 (1995) 411-415
22. Chan K.M., Ku L.L., Chan P.C., and Cheuk W.K. Metallothionein gene expression in zebrafish embryo-larvae and ZFL cell-line exposed to heavy metal ions. Mar. Environ. Res. 62 Suppl. (2006) S83-S87
23. Chan W.L., and Chan K.M. Cloning and characterization of a tilapia (Oreochromis aureus) metallothionein gene promoter in Hepa-T1 cells following the administration of various heavy metal ions. Aquat. Toxicol. 86 (2008) 59-75
24. Chen C.J., Chen C.W., Wu M.M., and Kuo T.L. Cancer potential in liver, lung, bladder and kidney due to ingested inorganic arsenic in drinking water. Br. J. Cancer 66 (1992) 888-892
25. Chen W.Y., John J.A.C., Lin C.H., and Chang C.Y. Molecular cloning and developmental expression of zinc finger transcription factor MTF-1 gene in zebrafish, Danio rerio. Biochem. Biophys. Res. Commun. 291 (2002) 798-805
26. Chen W.Y., John J.A., Lin H.F., Wu S.C., Lin C.H., and Chang C.Y. Expression of metallothionein gene during embryonic and early larval development in zebrafish. Aquat. Toxicol. 69 (2004) 215-227
27. Chen W.Y., John J.A., Lin C.H., and Chang C.Y. Expression pattern of metallothionein, MTF-1 nuclear translocation, and its DNA-binding activity in zebrafish (Danio rerio) induced by zinc and cadmium. Environ. Toxicol. Chem. 26 (2007) 110-117
28. Chen X., Agarwal A., and Giedroc D.P. Structural and functional heterogeneity among the zinc fingers of human MRE-binding transcription factor-1. Biochemistry 37 (1998) 11152-11161
29. Chen X., Chu M., and Giedroc D.P. 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 (1999) 12915-12925
30. Cherian M.G., and Clarkson T.W. Biochemical changes in rat kidney on exposure to elemental mercury vapor: effect on biosynthesis of metallothionein. Chem. Biol. Interact. 12 (1976) 109-120
31. Cheung, A.P.-L., 2003. Regulation of tilapia metallothionein (MT) gene expression. M.Phil. Thesis. Chinese University of Hong Kong, 251 pp.
32. Cheung A.P.-L., Lam T.H., and Chan K.M. Regulation of Tilapia metallothionein gene expression by heavy metal ions. Mar. Environ. Res. 58 (2004) 389-394
33. Cheung A.P.-L., Lam K.-L., and Chan K.M. Tilapia metallothionein genes: PCR-cloning and gene expression studies. Biochim. Biophys. Acta 1731 (2005) 191-201
34. Cousins R.T., and Lee-Ambrose L.M. Nuclear zinc uptake and interactions and metallotheionein gene expression are influenced by dietary zinc in rats. J. Nutr. 122 (1992) 56-64
35. Dalton T.P., Bittel D., and Andrews G.K. 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 (1997) 2781-2789
36. Dalton T.P., Solis W.A., Nebert D.W., and Carvan M.J. Characterization of the MTF-1 transcription factor from zebrafish and trout cells. Comp. Biochem. Physiol. (Biochem. Mol. Biol.) 126 (2000) 325-335
37. Daniels P.J., Bittel D., Smirnova I.V., Winge D.R., and Andrews G.K. 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 (2002) 3130-3140
38. 3+ exposure increase metallothionein mRNA and protein expression in juvenile winter flounder. Aquat. Toxicol. 42 4 (1998) 301-320
39. Forsberg C.W. Effects of heavy metals and other trace elements on the fermentative activity of the rumen microflora and growth of functionally important rumen bacteria. Can. J. Microbiol. 24 (1978) 298-306
40. Gonzalez P., Baudrimont M., Boudou A., and Bourdineaud J.P. Comparative effects of direct cadmium contamination on gene expression in gills, liver, skeletal muscles and brain of the zebrafish (Danio rerio). Biometals 19 (2006) 225-235
41. Gunnarsson D., Nordberg G., Lundgren P., and Selstam G. Cadmium-induced decrement of the LH receptor expression and cAMP levels in the testis of rats. Toxicology 183 (2003) 57-63
42. Heuchel R., Raotke 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
43. Hindmarsh J.T. Caveats in hair analysis in chronic arsenic poisoning. Clin. Biochem. 35 (2002) 1-11
44. Hogstrand C., and Haux C. Metallothionein as an indicator of heavy metal exposure in two subtropical fish species. J. Exp. Mar. Biol. Ecol. 138 (1990) 69-84
45. Jiang H., Daniels P.J., and Andrews G.K. 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 (2003) 30394-30402
46. Kägi J.H. Overview of metallothionein. Methods Enzymol. 205 (1991) 613-626
47. Koizumi S., Suzuki K., Ogra Y., Yamada H., and Otsuka F. Transcriptional activity and regulatory protein binding of metal-responsive elements of the human metallothionein-IIA gene. Eur. J. Biochem. 259 (1999) 635-642
48. Laity J.H., and Andrews G.K. Understanding the mechanisms of zinc-sensing by metal-response element binding transcription factor-1 (MTF-1). Arch. Biochem. Biophys. 463 (2007) 201-210
49. Langmade S.J., Ravindra R., Daniels P.J., and Andrews G.K. The transcription factor MTF-1 mediates metal regulation of the mouse ZnT1 gene. J. Biol. Chem. 275 (2000) 34803-34809
50. LaRochelle O., Gagné V., Charron J., Soh J.W., and Séguin C. Phosphorylation is involved in the activation of metal-regulatory transcription factor 1 in response to metal ions. J. Biol. Chem. 276 (2001) 41879-41888
51. Li Y., Kimura T., Laity J.H., and Andrews G.K. The zinc-sensing mechanism of mouse MTF-1 involves linker peptides between zinc fingers. Mol. Cell. Biol. 26 (2006) 5580-5587
52. Li W.H., Chan P.C., and Chan K.M. Metal uptake in zebrafish embryo-larvae exposed to metal-contaminated sediments. Mar. Environ. Res. 58 (2004) 829-832
53. Lichtlen P., and Schaffner W. Putting its fingers on stressful situations: the heavy metal-regulatory transcription factor MTF-1. BioEssays 23 (2001) 1010-1017
54. Majumder S., Ghoshal K., Summers D., Bai S., Datta J., and Jacob S.T. Chromium (VI) down regulates heavy metal induced metallothionein gene transcription by modifying transactivation potential of the key transcription factor, metal-responsive transcription factor 1. J. Biol. Chem. 278 (2003) 26216-26226
55. Marr II M.T., Isogai Y., Wright K.J., and Tjian R. Coactivator cross-talk specifies transcriptional output. Genes Dev. 20 (2006) 1458-1469
56. Murphy B.J., Andrews G.K., Bittel D., Discher D.J., McCue J., Green C.J., Yanovsky M., Giaccia A., Sutherland R.M., Laderoute K.R., and Webster K.A. Activation of Metallothionein gene expression by hypoxia involves metal response elements and metal transcription factor-1. Cancer Res. 59 (1999) 1315-1322
57. Nebes V.L., DeFranco D., and Morris Jr. S.M. Cyclic AMP induces metallothionein gene expression in rat hepatocytes but not in rat kidney. Biochem. J. 255 (1988) 741-743
58. Olsson P.-E., Kling P., Erkell L.J., and Kille P. Structural and functional analysis of the rainbow trout (Oncorhyncus mykiss) metallothionein-A gene. Eur. J. Biochem. 230 (1995) 344-349
59. Olsson P.-E., Kling P., and Hogstrand C. Mechanisms of heavy metal accumulation and toxicity in fish. In: Langston W.J., and Bebianno M.J. (Eds). Metal Metabolism in Aquatic Environments (1998), Chapman and Hall, London 321-350
60. Otsuka F., Iwamatsu A., Suzuki K., Ohsawa M., Hamer D.H., and Koizumi S. 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
61. Palmiter R.D. 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. U.S.A. 91 (1994) 1219-1223
62. Palmiter R.D. The elusive function of metallothioneins. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 8428-8430
63. Pramanik R., Ishido M., and Kunimoto M. Effects of cadmium chloride on neurite outgrowth and gene expression in human neuroblastoma NB-1 cells. J. Health Sci. 46 (2001) 478-482
64. Radtke F., Heuchel R., Georgiev O., Hergersberg M., Gariglio M., Dembic Z., and Schaffner W. Cloned transcription factor MTF-1 activates the mouse metallothionein I promoter. EMBO J. 12 (1993) 1355-1362
65. Ramana V.V., and Sastry K.S. Chromium toxicity in Neurospora crassa. J. Inorg. Biochem. 56 (1994) 87-95
66. Samson S.L., and Gedamu L. Metal-responsive elements of the rainbow trout metallothionein-B gene function for basal and metal-induced activity. J. Biol. Chem. 270 (1995) 6864-6871
67. 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
68. Searle P.F., Davison B.L., Stuart G.W., Wilikie T.M., Norstedt G., and Palmiter R.D. Regulation, linkage, and sequence of mouse metallothionein I and II genes. Mol. Cell Biol. 4 (1984) 1221-1230
69. Searle P.E., Stuart G.W., and Palmiter R.D. Metal regulatory elements of the mouse metallothionein-I gene. Exp. Suppl. 52 (1987) 407-414
70. Smirnova I.V., Bittel D.C., Ravindra R., Jinag H., and Andrews G.K. Zinc and cadmium can promote rapid nuclear translocation of metal response element-binding transcription factor-1. J. Biol. Chem. 275 (2000) 9377-9384
71. Stuart G.W., Searle P.F., Chen H.Y., Brinster R.L., and Palmiter R.D. 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. U.S.A. 81 (1984) 7318-7322
72. Stuart G.W., Searle P.F., and Palmiter R.D. Identification of multiple metal regulatory elements in mouse metallothionein-I promoter by assaying synthetic sequences. Nature 317 (1985) 828-831
73. Thirumoorthy N., Manisenthil Kumar K.T., Shyam Sundar A., Panayappan L., and Chatterjee M. Metallothionein: an overview. World J. Gastroenterol. 13 (2007) 993-996
74. Tom M., and Auslander M. Transcript and protein environmental biomarkers in fish-a review. Chemosphere 59 (2005) 155-162
75. Uetani M., Kobayashi E., Suwazono Y., Honda R., Nishijo M., Nakagawa H., Kido T., and Nogawa K. Tissue cadmium (Cd) concentrations of people living in a Cd polluted area, Japan. Biometals 19 (2006) 521-525
76. Wang Y., Wimmer U., Lichtlen P., Inderbitzin D., Stieger B., Meier P.J., Hunziker L., Stallmach T., Forrer R., Rulicke T., Georgiev O., and Schaffner W. Metal-responsive transcription factor-1 (MTF-1) is essential for embryonic liver development and heavy metal detoxification in the adult liver. FASEB J. 18 (2004) 1071-1079
77. Wimmer U., Wang Y., Georgiev O., and Schaffner W. Two major branches of anti-cadmium defense in the mouse: MTF1/metallothioneins and glutathione. Nucleic Acids Res. 33 (2005) 5715-5727
78. Westin G., and Schaffner W. A zinc-responsive factor interacts with a metal-regulated enhancer element (MRE) of the mouse metallothionein-I gene. EMBO J. 7 (1988) 3763-3770
79. Yan C.H., and Chan K.M. Characterization of zebrafish metallothionein gene promoter in a zebrafish caudal fin cell-line, SJD. 1. Mar. Environ. Res. 54 (2002) 335-339
80. Yan C.H., and Chan K.M. Cloning of zebrafish metallothionein gene and characterization of its gene promoter region in HepG2 cell line. Biochem. Biophys. Acta 1679 (2004) 47-58
81. Yu C.W., Chen J.H., and Lin L.Y. Metal-induced metallothionein gene expression can be inactivated by protein kinase C inhibitor. FEBS Lett. 420 (1997) 69-73
82. 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