Transcription of genes involved in glutathione biosynthesis in the solitary tunicate Ciona intestinalis exposed to metals

Aquatic Toxicology

Volumn 114-115, Issue , 2012, Pages 14-22

  Franchi, N ^a   Ferro, D ^a   Ballarin, L ^a   Santovito, G ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Ciona intestinalis; Glutathione; Metal induced oxidative stress; Tunicates

Indexed keywords

CADMIUM; COPPER; GAMMA GLUTAMYLCYSTEINE LIGASE CATALYTIC SUBUNIT; GAMMA GLUTAMYLCYSTEINE LIGASE MODIFIER SUBUNIT; GLUTATHIONE; GLUTATHIONE SYNTHASE; LIGASE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ZINC;

AMINO ACID; ENVIRONMENTAL STRESS; FILTER FEEDER; GENE EXPRESSION; METAL; MOLECULAR ANALYSIS;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CIONA INTESTINALIS; COMPUTER MODEL; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; IN VIVO STUDY; NONHUMAN; OXIDATIVE STRESS; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION;

ANIMALS; CIONA INTESTINALIS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION; GLUTATHIONE; METALS; OXIDATIVE STRESS; WATER POLLUTANTS, CHEMICAL;

CIONA INTESTINALIS; INVERTEBRATA; MAMMALIA; METAZOA; UROCHORDATA; VERTEBRATA;

EID: 84857943144     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.02.007     Document Type: Article

References (65)

1. Abbott J.J., Pei J., Ford J.L., Qi Y., Grishin V.N., Pitcher L.A., Phillips M.A., Grishin N.V. Structure prediction and active site analysis of the metal binding determinants in gamma-glutamylcysteine synthetase. J. Biol. Chem. 2001, 276:42099-42107.
2. Atli G., Canli M. Responses of metallothionein and reduced glutathione in a freshwater fish Oreochromis niloticus following metal exposures. Environ. Toxicol. Pharmacol. 2008, 25:33-38.
3. Bertin G., Averbeck D. Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences. Biochimie 2006, 88:1549-1559.
4. Boldrin F., Santovito G., Irato P., Piccinni E. Metal interaction and regulation of Tetrahymena pigmentosa metallothionein genes. Protist 2002, 153:283-291.
5. Casalino E., Calzaretti G., Sblano C., Landriscina C. Molecular inhibitory mechanisms of antioxidant enzymes in rat liver and kidney by cadmium. Toxicology 2002, 179:37-50.
6. Cook J.A., Pass H.I., Russo A., Iype S., Mitchell J.B. Use of monochlorobimane for glutathione measurements in hamster and human tumor cell line 1989, Int. J. Radiat. Oncol. Biol. Phys. 15, 1321-1324.
7. Cookson M.R., Slamon N.D., Pentreath V.W. Glutathione modifies the toxicity of triethyltin and trimethyltin in C6 glioma cells. Arch. Toxicol. 1998, 72:197-202.
8. Dehal P., Satou Y., Campbell R.K., Chapman J., Degnan B., De Tomaso A., Davidson B., Di Gregorio A., Gelpke M., Goodstein D.M., Harafuji N., Hastings K.E., Ho I., Hotta K., Huang W., Kawashima T., Lemaire P., Martinez D., Meinertzhagen I.A., Necula S., Nonaka M., Putnam N., Rash S., Saiga H., Satake M., Terry A., Yamada L., Wang H.G., Awazu S., Azumi K., Boore J., Branno M., Chin-Bow S., DeSantis R., Doyle S., Francino P., Keys D.N., Haga S., Hayashi H., Hino K., Imai K.S., Inaba K., Kano S., Kobayashi K., Kobayashi M., Lee B.I., Makabe K.W., Manohar C., Matassi G., Medina M., Mochizuki Y., Mount S., Morishita T., Miura S., Nakayama A., Nishizaka S., Nomoto H., Ohta F., Oishi K., Rigoutsos I., Sano M., Sasaki A., Sasakura Y., Shoguchi E., Shin-I.T., Spagnuolo A., Stainier D., Suzuki M.M., Tassy O., Takatori N., Tokuoka M., Yagi K., Yoshizaki F., Wada S., Zhang C., Hyatt P.D., Larimer F., Detter C., Doggett N., Glavina T., Hawkins T., Richardson P., Lucas S., Kohara Y., Levine M., Satoh N., Rokhsar D.S. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 2002, 298:2157-2167.
9. Delsuc F., Brinkmann H., Chourrout D., Philippe H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 2006, 439:965-968.
10. Díaz D., Krejsa C.M., White C.C., Keener C.L., Farin F.M., Kavanagh T.J. Tissue specific changes in the expression of glutamate-cysteine ligase mRNAs in mice exposed to methylmercury. Toxicol. Lett. 2001, 122:119-129.
11. Dickinson D.A., Levonen A.L., Moellering D.R., Arnold E.K., Zhang H., Darley-Usmar V.M., Forman H.J. Human glutamate cysteine ligase gene regulation through the electrophile response element. Free Radic. Biol. Med. 2004, 37:1152-1159.
12. Dickinson D.A., Forman H.J. Cellular glutathione and thiol metabolism. Biochem. Pharmacol. 2002, 64:1019-1026.
13. Dodd Mooz E., Meister A. Tripeptide (glutathione) synthetase. Purification, properties, and mechanism of action. Biochemistry 1967, 6:1722-1734.
14. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
15. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
16. Franchi N., Boldrin F., Ballarin L., Piccinni E. CiMT-1, an unusual chordate metallothionein gene in Ciona intestinalis genome: structure and expression studies. J. Exp. Zool. 2011, 315:90-100.
17. Franklin C.C., Backos D.S., Mohar I., White C.C., Forman H.J., Kavanagh T.J. Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase. Mol. Aspects Med. 2009, 30:86-98.
18. Ghoshal K., Jacob S.T. Regulation of metallothionein gene expression. Prog. Nucleic Acid Res. Mol. Biol. 2001, 66:357-384.
19. Gogos A., Shapiro L. Large conformational changes in the catalytic cycle of glutathione synthase. Structure 2002, 10:1669-1676.
20. Griffith O.W. Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic. Biol. Med. 1999, 27:922-935.
21. Hara T., Kato H., Katsube Y., Oda J. A Pseudo-Michaelis quaternary complex in the reverse reaction of a ligase: structure of Escherichia coli B glutathione synthetase complexed with ADP, glutathione, and sulfate at 2.0Å resolution. Biochemistry 1996, 35:11967-11974.
22. Herrera K., Cahoon R.E., Kumaran S., Jez J. Reaction mechanism of glutathione synthetase from Arabidopsis thaliana: site-directed mutagenesis of active site residues. J. Biol. Chem. 2007, 282:17157-17165.
23. Hibi T., Nii H., Nakatsu T., Kimura A., Kato H., Hiratake J., Oda J. Crystal structure of gamma-glutamylcysteine synthetase: insights into the mechanism of catalysis by a key enzyme for glutathione homeostasis. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:15052-15057.
24. Hothorn M., Wachter A., Gromes R., Stuwe T., Rausch T., Scheffzek K. Structural basis for the redox control of plant glutamate cysteine ligase. J. Biol. Chem. 2006, 281:27557-27565.
25. Huang C.S., Chang L.S., Anderson M.E., Meister A. Catalytic and regulatory properties of the heavy subunit of rat kidney γ-glutamylcysteine synthetase. J. Biol. Chem. 1993, 268:19675-19680.
26. Jez J.M., Cahoon R.E., Chen S. Arabidopsis thaliana glutamate-cysteine ligase functional properies, kinetic mechanism, and regulation of activity. Biol. Chem. 2004, 279:42726-42731.
27. Kille P., Kay J., Sweeney G.E. Analysis of regulatory elements flanking metallothionein genes in Cd-tolerant fish (pike and stone loach). Biochem. Biophys. Acta 1993, 1216:55-64.
28. Krzywanski D.M., Dickinson D.A., Iles K.E., Wigley A.F., Franklin C.C., Liu R.M., Kavanagh T.J., Forman H.J. Variable regulation of glutamate cysteine ligase subunit proteins affects glutathione biosynthesis in response to oxidative stress. Arch. Biochem. Biophys. 2004, 423:116-125.
29. Liu R.M., Gaston Pravia K.A. Oxidative stress and glutathione in TGF-beta-mediated fibrogenesis. Free Radic. Biol. Med. 2010, 48:1-15.
30. Meister A. Selective modification of glutathione metabolism. Science 1983, 220:472-477.
31. Nava G.M., Lee D.Y., Ospina J.H., Cai S.Y., Gaskins H.R. Genomic analyses reveal a conserved glutathione homeostasis pathway in the invertebrate chordate Ciona intestinalis. Physiol. Genomics 2009, 39:183-194.
32. Nei M., Kumar S. Molecular Evolution and Phylogenetics 2000, Oxford University Press, New York.
33. Olsson P.E., Kling P., Erkell L.J., Kille P. Structural and functional analysis of the rainbow trout (Oncorhyncus mykiss) metallothionein-a gene. Eur. J. Biochem. 1995, 230:344-349.
34. Peña M.M., Koch K.A., Thiele D.J. Dynamic regulation of copper uptake and detoxification genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 1998, 18:2514-2523.
35. Polekhina G., Board P.G., Gali R.R., Rossjohn J., Parker M.W. Molecular basis of glutathione synthetase deficiency and a rare gene permutation event. EMBO J. 1999, 18:3204-3213.
36. Rahman I., MacNee W. Oxidative stress and regulation of glutathione in lung inflammation. Eur. Respir. J. 2000, 16:534-554.
37. Rico D., Martín-Gonzáles A., Díaz S., de Lucas P., Gutiérrez J.-C. Heavy metals generate reactive oxygen species in terrestrial and aquatic ciliated protozoa. Comp. Biochem. Physiol. 2009, 149C:90-96.
38. Rzhetsky A., Nei M. A simple method for estimating and testing minimum evolution trees. Mol. Biol. Evol. 1992, 9:945-967.
39. Sadhu C., Gedamu L. Metal-specific posttranscriptional control of human metallothionein genes. Mol. Cell. Biol. 1989, 9:5738-5741.
40. Saitou N., Imanishi M. Relative efficiencies of the Fitch-Margoliash, maximumparsimony, maximum-likelihood, minimum-evolution, and neighbor-joining methods of phylogenetic tree construction in obtaining the correct tree. Mol. Biol. Evol. 1989, 6:514-525.
41. Samson S.L.A., Gedamu L. Molecular analyses of metallothionein gene regulation. Prog. Nucleic Acid Res. Mol. Biol. 1998, 59:257-288.
42. Sandrini J.Z., Regoli F., Fattorini D., Notti A., Inácio A.F., Linde-Arias A.R., Laurino J., Bainy A.C., Marins L.F., Monserrat J.M. Short-term responses to cadmium exposure in the estuarine polychaete Laeonereis acuta (Polychaeta Nereididae): subcellular distribution and oxidative stress generation. Environ. Toxicol. Chem. 2006, 25:1337-1344.
43. Santovito G., Irato P., Piccinni E. Regulation of metallothionein in a: induction of MT mRNA and protein by cadmium exposure. Eur. J. Protistol. 2000, 36:437-442.
44. Sayeed.I., Parvez S., Pandey S., Bin-Hafeez.B., Haque R., Raisuddin S. Oxidative stress biomarkers of exposure to deltamethrin in freshwater fish, Channa punctatus (Bloch). Ecotoxicol. Environ. Saf. 2003, 56:295-301.
45. Shaw G., Kamen R. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 1986, 46:659-667.
46. Shida K., Terajima D., Uchino R., Ikawa S., Ikeda M., Asano K., Watanabe T., Azumi K., Nonaka M., Satou Y., Satoh N., Satake M., Kawazoe Y., Kasuya A. Hemocytes of Ciona intestinalis express multiple genes involved in innate immune host defense. Biochem. Biophys. Res. Commun. 2003, 302:207-218.
47. Sneath P.H.A., Sokal R.R. Numerical Taxonomy 1973, Freeman, San Francisco.
48. Soares S.S., Martins H., Duarte R.O., Moura J.J.G., Coucelo J., GutiérrezMerino C., Aureliano M. Vanadium distribution, lipid peroxidation and oxidative stress markers upon decavanadate in vivo administration. J. Inorg. Biochem. 2007, 101:80-88.
49. Stach T., Braband A., Podsiadlowski L. Erosion of phylogenetic signal in tunicate mitochondrial genomes on different levels of analysis. Mol. Phylogenet. Evol. 2010, 55:860-870.
50. Storey K.B. Oxidative stress: animal adaptations in nature. Braz. J. Med. Biol. Res. 1996, 29:1715-1733.
51. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
52. Tanaka T., Kato H., Nishioka T., Oda J. Mutational and proteolytic studies on a flexible loop in glutathione synthetase from Escherichia coli B: the loop and arginine 233 are critical for the catalytic reaction. Biochemistry 1992, 31:2259-2265.
53. Tang R.S. The return of copy-choice in DNA recombination. Bioessays 1994, 16:785-788.
54. Ternay A.L., Sorokin V. Redox, radicals, and antioxidants. Oxidants, Antioxidants, and Free Radicals 1997, 1-21. Taylor Francis, Washington, D.C. S.I. Baskin, H. Salem (Eds.).
55. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
56. Thompson S.A., White C.C., Krejsa C.M., Diaz D., Woods J.S., Eaton D.L., Kavanagh T.J. Induction of glutamate-cysteine ligase (γ-glutamylcysteine synthetase) in the brains of adult female mice subchronically exposed to methylmercury. Toxicol. Lett. 1999, 110:1-9.
57. Townsend D.M. S-Glutathionylation: indicator of cell stress and regulator of the unfolded protein response. Mol. Interv. 2007, 7:313-324.
58. Tu Z., Anders M.W. Identification of an important cysteine residue in human glutamate-cysteine ligase catalytic subunit by site-directed mutagenesis. Biochem. J. 1998, 336:675-680.
59. Vasconcelos M.H., Tam S.C., Beattie J.H., Hesketh J.E. Evidence for differences in the post-transcriptional regulation of rat metallothionein isoforms. Biochem. J. 1996, 315:665-671.
60. Wan G., Cheuk W.K., Chan K.M. Differential regulation of zebrafish metallothionein-II (zMT-II) gene transcription in ZFL and SJD cell lines by metal ions. Aquat. Toxicol. 2009, 91:33-43.
61. Wild A.C., Mulcahy R.T. Regulation of gamma-glutamylcysteine synthetase subunit gene expression: insights into transcriptional control of antioxidant defenses. Free Radic. Res. 2000, 32:281-301.
62. Winterbourn C.C. Superoxide ad an intracellular radical sink. Free Radic. Biol. Med. 1993, 14:85-90.
63. Wu G., Fang Y.Z., Yang S., Lupton J.R., Turner N.D. Glutathione metabolism and its implications for health. J. Nutr. 2004, 134:489-492.
64. Yamane Y., Furuichi M., Song R., Van N.T., Mulcahy T., Ishikaw a T., Kuo M.T. Expression of multidrug resistance protein/GS-X pump and γ-glutamylcysteine synthetase genes is regulated by oxidative stress. J. Biol.Chem. 1998, 273:31075-31085.
65. Zuckerkandl E., Pauling L. Evolutionary divergence and convergence in proteins. Evolving Genes and Proteins 1965, 97-166. Academic Press, New York. V. Bryson, H.J. Vogel (Eds.).