Shaping mechanisms of metal specificity in a family of metazoan metallothioneins: Evolutionary differentiation of mollusc metallothioneins

BMC Biology

Volumn 9, Issue , 2011, Pages

  Palacios, Òscar ^a   Pagani, Ayelen ^b   Pérez Rafael, Sílvia ^a   Egg, Margit ^c   Höckner, Martina ^c   Brandstätter, Anita ^d   Capdevila, Mercè ^a   Atrian, Sílvia ^b   Dallinger, Reinhard ^c  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF INNSBRUCK   (Austria)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; EUKARYOTA; GASTROPODA; HELIX POMATIA; METAZOA; MOLLUSCA;

CADMIUM; COPPER; METALLOTHIONEIN; ZINC;

ANIMAL; ARTICLE; CIRCULAR DICHROISM; ELECTROSPRAY MASS SPECTROMETRY; ESCHERICHIA COLI; GENE DUPLICATION; GENETICS; HELIX (SNAIL); METABOLISM; MOLECULAR EVOLUTION; ULTRAVIOLET SPECTROPHOTOMETRY; YEAST;

ANIMALS; CADMIUM; CIRCULAR DICHROISM; COPPER; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE DUPLICATION; HELIX (SNAILS); METALLOTHIONEIN; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROPHOTOMETRY, ULTRAVIOLET; YEASTS; ZINC;

EID: 78651549431     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-9-4     Document Type: Article

References (71)

1. Sigel A, Sigel H, Sigel RKO. Metal ions in Life Sciences; v 5: Metallothioneins and Related Chelators 2009, 1-514. Cambridge: Royal Society of Chemistry.
2. Blindauer CA, Leszczyszyn OI. Metallothioneins: unparalleled diversity in structures and functions for metal ion homeostasis and more. Nat Prod Rep 2010, 27:720-741. 10.1039/b906685n, 20442962.
3. Klaassen CD, Liu J, Choudhuri S. Metallothionein: An intracellular protein to protect against cadmium toxicity. Ann Rev Pharmacol Toxicol 1999, 39:267-294.
4. Egli D, Yepiskoposyan H, Selvaraj A, Balamurugan K, Rajaram R, Simons A, Multhaup G, Mettler S, Vardanyan A, Georgiev O, Schaffner W. A family knockout of all four Drosophila metallothioneins reveals a central role in copper homeostasis and detoxification. Mol Cell Biol 2006, 26:2286-2296. 10.1128/MCB.26.6.2286-2296.2006, 1430275, 16508004.
5. Palmiter RD. The elusive function of metallothioneins. Proc Natl Acad Sci USA 1998, 95:8428-8430. 10.1073/pnas.95.15.8428, 33872, 9671693.
6. Davis SR, Cousins RJ. Metallothionein expression in animals: a physiological perspective on function. J Nutr 2000, 130:1085-1088.
7. Chen P, Muñoz A, Nettesheim D, Shaw CF-III, Petering DH. Stoichiometry and cluster specificity of copper binding to metallothionein: homogeneous metal clusters. Biochem J 1996, 317:395-402. 1217501, 8713064.
8. Egli D, Domenech J, Selvaraj A, Balamurugan K, Hua H, Capdevila M, Georgiev O, Schaffner W, Atrian S. The four members of the Drosophila metallothionein family exhibit distinct yet overlapping roles in heavy metal homeostasis and detoxification. Genes to Cells 2006, 11:647-658. 10.1111/j.1365-2443.2006.00971.x, 16716195.
9. Stillman MJ, Zelazowski AJ. Domain specificity of Cd2+ and Zn2+ binding to rabbit liver metallothionein2. Biochem J 1989, 262:181-188. 1133245, 2510714.
10. Li H, Otvos JD. 111Cd NMR studies of the domain specificity of Ag+ and Cu+ binding to metallothionein. Biochemistry 1996, 35:13929-13936. 10.1021/bi961401n, 8909290.
11. Tio L, Villarreal L, Atrian S, Capdevila M. Functional differentiation in the mammalian metallothionein gene family. Metal binding features of Mouse MT4 and comparison with its paralog MT1. J Biol Chem 2004, 279:24403-24413. 10.1074/jbc.M401346200, 15033980.
12. Kägi JHR, Kojima Y. Chemistry and biochemistry of metallothionein. Metallothionein II 1987, 25-61. Basel: Birkhäuser Verlag, Kägi JHR,Kojima Y, Exp Suppl 52..
13. Vasák M. Standard isolation procedure for metallothionein. Meth Enzymol 1991, 205:41-44.
14. Lerch K, Johnsen GF, Grushoff PS, Sternlieb I. Canine hepatic lysosomal copper protein: identification as metallothionein. Arch Biochem Biophys 1985, 243:108-114. 10.1016/0003-9861(85)90778-7, 4062298.
15. Overnell J. Occurrence of cadmium in crabs (Cancer pagurus) and the isolation and properties of cadmium metallothionein. Environ Hlth Perspect 1986, 65:101-105.
16. Waldron KJ, Robinson NJ. How do bacterial cells ensure that metalloproteins get the correct metal?. Nature Rev Microb 2010, 6:25-35.
17. Ponder W, Lindberg DR. Phylogeny and Evolution of the Mollusca 2008, 1-488. CA: University of California Press.
18. Dallinger R, Berger B, Hunziker PE, Birchler N, Hauer C, Kägi JHR. Purification and primary structure of snail metallothionein. Similarity of the N-terminal sequence with histones H4 and H2A. Eur J Biochem 1993, 216:739-746. 10.1111/j.1432-1033.1993.tb18193.x, 8404892.
19. Berger B, Dallinger R, Gehrig P, Hunziker PE. Primary structures of a copper-binding metallothionein from mantle tissue of the terrestrial gastropod Helix pomatia. L Biochem J 1997, 328:219-224.
20. Dallinger R, Berger B, Hunziker PE, Kägi JHR. Metallothionein in snail Cd and Cu metabolism. Nature 1997, 388:237-238. 10.1038/40785, 9230430.
21. Hispard F, Schuler D, deVaufleury A, Scheifler R, Badot PM, Dallinger R. Metal distribution and metallothionein induction after cadmium exposure in the terrestrial snail Helix aspersa (gastropoda, pulmonata). Environ Toxicol Chem 27:1533-1542. 208, 10.1897/07-232.1, 18384240.
22. Dallinger R, Wang Y, Berger B, Mackay EA, Kägi JHR. Spectroscopic characterization of metallothionein from the terrestrial snail, Helix pomatia. Eur J Biochem 2001, 268:4126-4133. 10.1046/j.1432-1327.2001.02318.x, 11488904.
23. Gehrig PM, You C, Dallinger R, Gruber C, Brouwer M, Kägi JHR, Hunziker PE. Electrospray ionization mass spectrometry of Zn, Cd and Cu metallothioneins: evidence for metal-binding cooperativity. Prot Sci 2000, 9:395-402.
24. Chabicovsky M, Niederstaetter H, Thaler R, Hödl E, Parson W, Rossmanith W, Dallinger R. Localization and quantification of Cd- and Cu-specific metallothionein isoform mRNA in cells and organs of the terrestrial gastropod Helix pomatia. Toxicol Appl Pharmacol 2003, 190:25-36. 10.1016/S0041-008X(03)00148-0, 12831780.
25. Chabicovsky M, Klepal W, Dallinger R. Mechanisms of cadmium toxicity in terrestrial pulmonates: programmed cell death and metallothionein overload. Environ Toxicol Chem 2004, 23:648-655. 10.1897/02-617, 15285358.
26. Manzl C, Krumschnabel G, Schwarzbaum PJ, Dallinger R. Acute toxicity of cadmium and copper in hepatopancreas cells from the Roman snail (Helix pomatia). Comp Biochem Physiol C 2004, 138:45-52.
27. Dallinger R, Chabicovsky M, Hödl E, Prem C, Hunziker P, Manzl C. Copper in Helix pomatia (Gastropoda) is regulated by one single cell type: differently responsive metal pools in rhogocytes. Am J Physiol 189:R1185-R1195. 205.
28. Vasák M, Kägi JHR, Hill HAO. Zinc(II), cadmium(II) and mercury(II) thiolate transitions in metallothionein. Biochemistry 1981, 20:2852-2856.
29. Willner H, Vasák M, Kägi JHR. Cadmium-thiolate clusters in metallothionein: spectrometric and spectropolarimetric features. Biochemistry 1987, 26:6287-6292. 10.1021/bi00393a049, 3689776.
30. Willner H, Bernhard WR, Kägi JHR. Optical properties of metallothioneins. Origin of the optical properties of mammalian metallothioneins. Metallothioneins, Synthesis, Structure and Properties of Metallothioneins, Phytochelatins and Metal-Thiolate Complexes 1992, 128-143. New York: VCH Publishers, Stillman MJ, Shaw CF, Suzuki KT.
31. Presta A, Rae Green A, Zelazowski A, Stillman MJ. Copper binding to rabbit liver metallothionein: formation of a continuum of Copper(I)-thiolate stoichiometric species. Eur J Biochem 1885, 227:226-240.
32. Pagani A, Villarreal L, Capdevila M, Atrian S. The Saccharomyces cerevisiae Crs5 metallothionein metal-binding abilities and its role in the response to zinc overload. Mol Microbiol 2007, 63:256-269. 10.1111/j.1365-2958.2006.05510.x, 17163970.
33. Capdevila M, Domènech J, Pagani A, Tío L, Villarreal L, Atrian S. Zn- and Cd-metallothionein recombinant species from the most diverse phyla may contain sulfide (S2-) ligands. Angew Chem Int Ed Engl 2005, 44:4618-4622. 10.1002/anie.200501183, 15991200.
34. Bofill R, Capdevila M, Atrian S. Independent metal-binding features of recombinant metallothioneins convergently draw a step gradation between Zn- and Cu-thioneins. Metallomics 2009, 1:229-234.
35. Orihuela R, Monteiro F, Pagani A, Capdevila M, Atrian S. Evidence of native metal-(S2-)-MT complexes confirmed by the analysis of Cup1 divalent metal ion binding properties. Chem A Eur J 16:12363-12372. 210.
36. Egg M, Höckner M, Brandstätter A, Schuler D, Dallinger R. Structural and bioinformatic analysis of the Roman snail Cd-Metallothionein gene uncovers molecular adaptation towards plasticity in coping with multifarious environmental stress. Mol Ecol 2009, 18:2426-2443. 10.1111/j.1365-294X.2009.04191.x, 19457198.
37. Nielson KB, Atkin CL, Winge DR. Distinc Metal-binding Configurations in Metallothioneins. J Biol Chem 1985, 260:5342-5350.
38. Stillman MJ, Rae Green A, Gui Z, Fowle D, Presta PA. Circular dichroism, emission, and exafs studies of Ag(I), Cd(II), Cu(I), and Hg(II) binding to metallothioneins and modelling the metal binding site. Metallothionein 1999, 23-35. Basel: Birkhäuser Verlag, Klaassen C, Vol IV.
39. Otvos JD, Engeseth HR, Nettesheim DG, Hilt CR. Interprotein metal exchange reactions of metallothionein. Experientia Suppl 1987, 52:171-178.
40. Maroni G, Wise J, Young JE, Otto E. Metallothionein gene duplications and metal tolerance in natural populations of Drosophila melanogaster. Genetics 1987, 117:739-744. 1203245, 2828157.
41. Tanguy A, Moraga D. Cloning and characterization of a gene coding for a novel metallothionein in the Pacific Oyster Crassostrea gigas (CgMT2): a case of adaptive response to metal-induced stress?. Gene 2001, 273:123-130. 10.1016/S0378-1119(01)00577-7, 11483368.
42. Kondrashov FA, Kondrashov AS. Role of selection in fixation of gene duplications. J Theoret Biol 2006, 239:141-151.
43. Haszprunar G. The molluscan rhogocyte (pore-cell, Blasenzelle, cellule nucale), and its significance for ideas on nephridial evolution. J Mollus Stud 1996, 62:185-211.
44. Albrecht U, Keller H, Gebauer W, Markl J. Rhogocytes (pore cells) as the site of hemocyanin biosynthesis in the marine gastropod Haliotis tuberculata. Cell Tissue Res 2001, 304:455-462. 10.1007/s004410100368, 11456421.
45. Brouwer M, Whaling P, Engel DW. Copper-Metallothioneins in the American Lobster, Homarus americanus: Potential role as Cu(I) donors to apohemocyanin. Environ Hlth Persp 1986, 65:93-100.
46. Narula SS, Brouwer M, Hua Y, Armitage IM. Three-dimensional solution structure of Callinectes sapidus metallothionein-1 determined by homonuclear and heteronuclear magnetic resonance spectroscopy. Biochemistry 1995, 34:620-631. 10.1021/bi00002a029, 7819257.
47. Engel DW, Brouwer M. Metal regulation and molting in the blue crab, Callinectes sapidus: Metallothionein function in metal metabolism. Biol Bull 1987, 173:239-251.
48. Engel DW, Brouwer M. Short-term metallothionein and copper changes in blue crabs at ecdysis. Biol Bull 1991, 180:447-452.
49. Butt TR, Sternberg EJ, Gorman JA, Clark P, Hamer D, Rosenberg M, Crooke ST. Copper Metallothionein of yeast, structure of the gene, and regulation of expression. Proc Natl Acad Sci USA 1984, 81:3332-3336. 10.1073/pnas.81.11.3332, 345501, 6374656.
50. Münger K, Lerch K. Copper Metallothionein from the fungus Agaricus bisporus: chemical and spectroscopic properties. Biochemistry 1985, 24:6751-6756.
51. Beltramini M, Lerch K. Primary structure and spectroscopic studies of Neurospora copper Metallothionein. Environ Hlth Persp 1986, 65:21-27.
52. Lerch K. Copper metallothionein, a copper-binding protein from Neurospora crassa. Nature 1980, 284:368-370. 10.1038/284368a0, 6444697.
53. Dallinger R, Berger B, Bauer-Hilty A. Purification of cadmium-binding proteins from related species of terrestrial helicidae (Gastropoda, Mollusca): a comparative study. Mol Cell Biochem 1989, 85:135-145. 10.1007/BF00577109, 2725484.
54. Münger K, Lerch K, Tschierpe HJ. Metal accumulation in Agaricus bisporus: Influence of Cd and Cu on growth and tyrosinase activity. Cell Mol Life Sci 1982, 38:1039-1041.
55. Brouwer M, Bonaventura C, Bonaventura J. Metal ion interactions with Limulus polyphemus and Callinectes sapidus hemocyanins: stoichiometry and structural and functional consequences of calcium(II), cadmium(II), zinc(II), and mercury(II) binding. Biochemistry 1983, 22:4713-4723. 10.1021/bi00289a016, 6626526.
56. Bubacco L, Rocco GP, Salvato B, Beltramini M. The binding of Cd(II) to the hemocyanin of the Mediterranean crab Carcinus maenas. Arch Biochem Biphys 1993, 302:78-84.
57. Ngo HTT, Gerstmann S, Frank H. Subchronic effects of environment-like cadmium levels on the bivalve Anodonta anatina (Linnaeus 1758): III. Effects on carbonic anhydrase activity in relation to calcium metabolism. Toxicol Environ Chem 2010, 92(10):1029-0486.
58. Vasak M, Kägi JHR. Spectroscopic properties of metallothionein. Metal Ions in Biological Systems 1983, 213-273. New York: Marcel Dekker, Sigel H, Vol 15.
59. Haq F, Mahoney M, Koropatnick J. Signalling events for metallothionein induction. Mutat Res 2003, 533:211-226.
60. Dallinger R, Chabicovsky M, Berger B. Isoform-specific quantification of metallothionein in the terrestrial gastropod Helix pomatia I. Molecular, biochemical, and methodical background. Environ Toxicol Chem 2004, 23:890-901. 10.1897/03-100, 15095884.
61. Cols N, Romero-Isart N, Capdevila M, Oliva B, Gonzàlez-Duarte P, Gonzàlez-Duarte R, Atrian S. Binding of excess cadmium(II) to Cd7-metallothionein from recombinant mouse Zn7-metallothionein 1. UV-VIS absorption and circular dichroism studies and theoretical location approach by surface accessibility analysis. J Inorg Biochem 1997, 68:157-166. 10.1016/S0162-0134(97)00085-8, 9352652.
62. Bongers J, Walton CD, Richardson DE, Bell JU. Micromolar protein concentrations and metalloprotein stoichiometries obtained by inductively coupled plasma. Atomic emission spectrometric determination of sulphur. Anal Chem 1988, 60:2683-2686. 10.1021/ac00175a008, 3245594.
63. Fabris D, Zaia J, Hathout Y, Fenselau C. Retention of thiol protons in two classes of protein zinc ion coordination centers. J Am Chem Soc 1996, 118:12242-12243.
64. Capdevila M, Cols N, Romero-Isart N, González-Duarte R, Atrian S, González-Duarte P. Recombinant synthesis of mouse Zn3-α and Zn4-α metallothionein 1 domains and characterization of their cadmium(II) binding capacity. Cell Mol Life Sci 1997, 53:681-688. 10.1007/s000180050088, 9351472.
65. Bofill R, Palacios O, Capdevila M, Cols N, González-Duarte R, Atrian S, González-Duarte P. A new insight into the Ag+ and Cu+ binding sites in the metallothionein β domain. J Inorg Biochem 1999, 73:57-64. 10.1016/S0162-0134(98)10091-0, 10212995.
66. Longo VD, Gralla EB, Valentine JS. Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. J Biol Chem 1996, 271:12275-12280. 10.1074/jbc.271.21.12275, 8647826.
67. Mumberg D, Müller R, Funk M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 1995, 156:119-122. 10.1016/0378-1119(95)00037-7, 7737504.
68. Stearns T, Ma H, Botstein D. Manipulating yeast genome using plasmid vectors. Methods Enzymol 1990, 185:280-297. full_text, 2199782.
69. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948. 10.1093/bioinformatics/btm404, 17846036.
70. Saitou N, Nei M. The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4:406-425.
71. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.