Spectroscopic Properties of Ag(I), Cd(II), Cu(I), Hg(II), and Zn(II) Metallothioneins

  • Martin J. Stillman
Part of the NATO ASI Series book series (ASEN2, volume 26)


Metallothioneins (MT), a class of protein characterized by a high cysteine content, low molar mass, and lack of aromatic amino acid residues, have been isolated from mammals, yeasts, fungus, and crustaceans [1–3]. The 20 cysteines out of a total of 61 or 62 amino acids in rabbit liver MT bind a remarkably wide range of metals, including, significantly, cadmium, copper, and mercuiy. The binding constants for metal binding follow the order found for inorganic thiolates, Hg(II) > Ag(I) ≈ Cu(I) > Cd(II) > Zn(II). In mammalian Cd7-MT and Zn7-MT the metals arc tetrahedrally co-ordinated in two isolated domains with stoichiometries of M4Sn and M3S9. Optical spectra, in particular circular dichroism and luminescence spectra, have provided rich details of a complicated metal binding chemistry when metals arc added directly to the metal free- or zinc- containing protein. The absence of aromatic amino acids is important because spectral data can be measured for the thiolate to metal charge transfer transitions that occur between 220 and 350 nm, a region that would be completely masked by the presence of aromatic groups. The CD technique is sensitive to changes in the orientation of the peptide chain induced by changes in the metal binding site as a result of metal binding or metal exchange. In particular, the CD spectral changes are extensive when the metal co-ordination geometry changes, for example from the tetrahedral of Zn7-MT to accommodate metals like Cu(I) and Ag(I), metals that generally exhibit trigonal or digonal coordination geometries. Absorption, emission, MCD, and CD spectra provide considerable detail about the stoichiometries of complexes that form as metal are added to either apo-MT or the Zn(II) in Zn7-MT.

Cu(I) and Hg(II) bind strongly to the cysteinyl thiolates in metallothionein both in vivo and in vitro. Structural information about mercury-containing metallothioneins is currently limited to optical and x-ray absorption (XAS, XANES, XAFS) studies. Emission spectra in the 450-750 nm region have been reported for metallothioneins containing Ag(I), Au(I), Cu(I), and Pt(II), at both room temperature and cryogenic temperatures. Excitation in the 250-300 nm results in emission inteasity in the 500-700 nm region for Cu(I), Ag(I), and Au(I) metallothioneins. The most well known emission of the metallothioneins is the orange luminescence observed at room temperature for copper-containing metallothioneins. The emission is generally characterized by lifetimes of the order a few microseconds. Recently the complex function of the emission intensity at 600 nm on the Cu(I):MT ratio has been interpreted When Cu(I) binds to rabbit liver Z7-MT, Zn(II) is first displaced from both domains on a statistical basis at all temperatures. Over time, the Cu(I) redistributes into the β domain forming the domain specific product. As a result of an imbalance in quantum yields between the two domains, the redistribution of Cu(I) from the a domain to the β domain can be monitored in real time. The luminescence of Cu-MT can also be detected directly from mammalian and yeast cells. XAFS structural data on a number of metallothioneins have been reported. The availability of XAFS data from both the co-ordinating thiolate sullur and the bound metal provides information unavailable from other techniques.

Three structural motifs have been identified for rabbit liver metallothionein following analysis of spectroscopic data for protein containing Zn(II), Cu(I), Ag(I), Co(II), and Hg(II). In these species the peptide chain forms metal thiolate clusters with stoichiometries ofM7-S20, M12-S20, and M18-S20. The precise determination of the stoichiometric ratio between the bound metals and the number of accessible cysteinyl sulfurs is important in understanding the chemistry of these proteins. Because the formation of metal-thiolate clusters involving terminal and/or bridging cysteinyl thiolate groups characterizes all metallothioneins, the protein’s tertiary structure is dominated by the cross-linking imposed by these clusters. Key metal binding properties for metallothioneins isolated from all sources are (i) the metal to sulfur stoichiometry, (ii) the domain preference in the two-domain class 1 proteins, and (iii) the co-ordination geometry of the sulfur around the metal. In addition, for a protein that binds multiple metals, answers to a number of questions are needed. First, what is the form of the metal binding site with very few metals bound? Second, how does the clustering proceed? Third, how does metal exchange occur between different sites and different domains?


Emission Intensity Metal Binding Peptide Chain Charge Transfer Band Metal Binding Site 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Kagi, J.H.R. and Nordberg, M. (eds.) (1979) Metallothionein, Birkhauser Verlag, Basel.Google Scholar
  2. 2.
    Kagi, J.H.R. and Kojima, Y. (eds.) (1987) Metallothionein II, Birkhauser Verlag, Basel.Google Scholar
  3. 3.
    Stillman, M.J., Shaw, C.F., and Suzuki, K.T (eds.) (1992) Metallothioneins, V.C.H. Publishers, New York.Google Scholar
  4. 4.
    Suzuki, K.T., Imura, N. and Kimura, M. (eds.) (1993) Metallothionein III, Birkhauser Verlag, Basel.Google Scholar
  5. 5.
    Riordan, J.F. and Vallee, B.L. (eds.) (1991) Metallobiochemistry Part B. Metallothionein and Related Molecules. Methods in Enzymology, vol. 205, Academic Press, New York.Google Scholar
  6. 6.
    Stillman, M. J. (1995) Metallothioneins, Coord. Chem. Review 144, 461–571.CrossRefGoogle Scholar
  7. 7.
    Robbins, A.H., McRee, D.E., Williamson, M., Collett, S.A., Xuong, N.H., Furey, W.F., Wang, B.C., and Stout, C.D., (1991) Refined crystal structure of Cd, Zn-metallothionein at 2.0 A resolution, J. Mol. Biol. 221, 1269–1293.Google Scholar
  8. 8.
    Robbins, A.H. and Stout, CD. (1992) Crystal structure of metallothioneins in M.J. Stillman, C.F. Shaw III, K.T. Suzuki (eds.), Metallothioneins, VCH Publishers, New York, pp. 31–54.Google Scholar
  9. 9.
    Zhu, Z., DeRose, E.F., Mullen, G.P., Petering, D.H., and Shaw, C.F. III (1994) Sequential proton resonance assignments and metal cluster topology of lobster metallothionein-1, Biochem. 33, 8858–8865CrossRefGoogle Scholar
  10. 10.
    Braun, W., Vasak, M., Robbins, A.H., Stout, C.D., Wagner, G., Kagi, J.H.R., and Wuthrich, K. (1992) Comparison of the NMR solution structure and the X-ray crystal structure of rat metallothionein-2. Proc. Natl. Acad. Sci. U.S.A. 89, 10124–10128.CrossRefGoogle Scholar
  11. 11.
    Otvos, J.D., Olafson, R.W., and Armitage, I.M. (1982) Structure of an invertebrate metallothionein from Scylla Serrata 113Cd NMR, J. Biol. Chem. 257, 2427–2431.Google Scholar
  12. 12.
    Hayashi, Y, and Winge, D.R. (1992) (γ-EC)n G peptides in M.J. Stillman, C.F. Shaw, and K.T. Suzuki (eds.) Metallothioneins, VCH Publishers, New York, pp. 271–283.Google Scholar
  13. 13.
    Savas, M.M., Shaw, CF. III, and Petering, D.H (1993) The oxidation of rabbit liver metallothionein-II by 5, 5′-dithiobis(2-nitrobenzoic acid) and gluthathione disulfide, J. Inorg. Biochem. 52, 235–249.CrossRefGoogle Scholar
  14. 14.
    George, G.N., Byrd, J., and Winge D.R (1988) X-ray absorption studies of yeast copper MT, J. Biol. Chem. 263, 8199–8203.Google Scholar
  15. 15.
    Kagi, J.H.R. (1993) Evolution, structure and chemical reactivity of class I metallothioneins: An overview in Suzuki, K.T., Imura, N., and Kimura, M. (eds.) Metallothionein III, Birkhauser Verlag, Basel, pp. 29–55.Google Scholar
  16. 16.
    Le Blanc, Y.J.C, Presta, A., Veinot, J., Gibson, D., Siu, K.W.M. and Stillman, M.J. (1996) submitted.Google Scholar
  17. 17.
    Jiang, D.T., Gui, Z.Q., Heald, S.M., Sham, T.K. and Stillman, M.J. (1995) XAFS of silver(I) metallothioneia Physica B 208/209, 729–730.Google Scholar
  18. 18.
    Fowle, D.A. and Stillman, M.J. (1996) Comparison of the structures of the metal-thiolate binding sites in Zn(II)7, Cd(II)7, and Hg(II)7-metallothioneins using molecular modeling techniques, J. Biomol. Struct. Dyn. 00, in press.Google Scholar
  19. 19.
    Gui, Z, Green, A.R., Kasrai, M., Bancroft, G.M. and Stillman, M.J. (1996) Sulfur K-edge EXAFS studies of cadmium, zinc, copper, and silver rabbit liver metallothioneins, Inorganic Chemistry, 35, (Oct. issue).Google Scholar
  20. 20.
    Green, A.R. and Stillman, M.J. (1996) Mobility of copper in binding sites in rabbit liver metallothionein 2, Inorg. Chan. 35, 2799–2807.CrossRefGoogle Scholar
  21. 21.
    Presta, A., Green, A.R., Zelazowski, A.J. and Stillman, M.J. (1995) Copper binding to rabbit liver metallothionein. Fomation of a continuum of copper(I)-thiolate stoichiometric species, Eur. J. Biochem. 227, 226–240.CrossRefGoogle Scholar
  22. 22.
    Presta, A., Green, A.R., and Stillman, M.J. (1996) Cu(I) binding to apo-MT. A circular dichroism study, submitted.Google Scholar
  23. 23.
    Stillman, M.J., Presta, A., Gui, Z. and Jiang, D.T. (1994) Spectroscopic studies of copper, silver and gold-metallothioneins, Metal-Based Drugs 1, 375–393.CrossRefGoogle Scholar
  24. 24.
    Green, A.R., and Stillman, M.J. (1994) Oxidative quenching of luminescence from copper metallothioneia Inorg. Chim. Acta 226, 275–283.CrossRefGoogle Scholar
  25. 25.
    Jiang, D.T., Heald, S.M., Sham, T.K. and Stillman, M.J. (1994) Structures of the cadmium, mercury, and zinc thiolate clusters in metallothionein: XAFS study of Zn7-MT, Cd7-MT, Hg7-MT and Hgl8-MT formed from rabbit liver metallothionein, J. Am. Chem. Soc. 116, 11004–11013.CrossRefGoogle Scholar
  26. 26.
    Green, A.R., Presta, A, Gasyna, Z and Stillman, M.J. (1994) Luminescent probe of copper-thiolate cluster formation within mammalian metallothionein, Inorg Chem. 33, 4159–4168.CrossRefGoogle Scholar
  27. 27.
    Presta, A. and Stillman, M.J. (1994) Chiral copper(I)-thiolate clusters in metallothionein and glutathione, Chirality 6, 521–530.CrossRefGoogle Scholar
  28. 28.
    Lu, W. and Stillman, M.J. (1993) Mercury-thiolate clusters in metallothioneins. Analysis of circular dichroism spectra of complexes formed between α-metallothionein, apometallothionein, zinc metallothionein, and cadmium metallothionein and Hg2+, J. Am. Chem. Soc 115, 3291–3299.CrossRefGoogle Scholar
  29. 29.
    Lu, W. Zelazowski, A.J. and Stillman, M.J. (1993) Mercury binding to metallothioneins: Formation of Hg18-MT, Inorg. Chem. 32, 919–926.CrossRefGoogle Scholar
  30. 30.
    Zelazowski, A.J. and Stillman, M.J. (1992) Ag(I) binding to metallothionein. CD study of silver-thiolate cluster formation formation with Zn-MT and Zn-α and Zn-β MT, Inorg Chem. 31, 3363–3370.CrossRefGoogle Scholar
  31. 31.
    Shaw, C.F. III, Stillman, M.J., and Suzuki, K.J. Metallothioneins in M.J. Stillman, C.F. Shaw III, and K.T. Suzuki (eds.), Metallothioneins, VCH Publishers, New York, pp. 1–13 (1992).Google Scholar
  32. 32.
    Stillman, M.J. Optical spectroscopy of metallothioneins in M.J. Stillman, C.F. Shaw III, and K.T. Suzuki (eds.), Metallothioneins, VCH Publishers, New York, pp. 55–127 (1992).Google Scholar
  33. 33.
    Stillman, M.J. and Gasyna, Z. (1991) Luminescence spectroscopy of metallothioneins in B. Vallee and J.F. Riordan (eds.), Methods in Enzymology, Metallobiochemistry part B, Metallothionein and Related Molecules, Academic Press, New York, vol. 205 pp. 540–555.CrossRefGoogle Scholar
  34. 34.
    Lu, W, Kasrai, M., Bancroft, G.M, Stillman, M.J, and Tan, K.H. (1990) S L-edge XANES study of Zn, Cd, and Hg containing metallothionein and model compounds MT, Inorg. Chem. 29, 2561–2563.CrossRefGoogle Scholar
  35. 35.
    Green, A.R. (1995) Ph.D. Thesis. University of Western Ontario, London, Canada.Google Scholar
  36. 36.
    Stillman, M.J., Gasyna, Z, and Zelazowski, A.J. (1989) A luminescence probe for MT in liver tissue: emission intensity measured directly from Cu(I)-MT induced in rat liver, FEBS Letters 257, 283–286.CrossRefGoogle Scholar
  37. 37.
    Zelazowski, A.J., Gasyna, Z, and Stillman, M.J. (1989) Ag binding to rabbit liver MT. CD and emission study of Ag-thiolate cluster formation with apoMT and the alpha and beta fragments, J. Biol. Chem. 264, 17091–17099.Google Scholar
  38. 38.
    Stillman, M.J., Zelazowski, A.J., Szymanska, J., and Gasyna, Z. (1989) Luminescent metallothioneins: Emission properties of copper, silver, gold and platinum complexes of MT, Inorg. Chim. Acta. 161, 275–279.CrossRefGoogle Scholar
  39. 39.
    Stillman, M.J. and Zelazowski, A.J. (1989) Domain specificty of cadmium and zinc binding to rabbit liver metallothionein 2. Metal ion mobility in the formation of Cd4-a MT, Biochem. J 262, 181–188.Google Scholar
  40. 40.
    Stillman, M.J, Zelazowski, A.J., and Gasyna, Z. (1988) Luminescent Ag-metallothionein: Dependence of emission intensity on silver-thiolate cluster formation, FEBS Lett. 240, 159–162.CrossRefGoogle Scholar
  41. 41.
    Cai, W. and Stillman, M.J. (1988) Hg18-metallothionein. J. Am. Chem. Soc. 110, 7872–7873.CrossRefGoogle Scholar
  42. 42.
    Gasyna, Z, Zelazowski, A.J., Green, A.R., Ough, E, and Stillman, M.J. (1988) Luminescence decay from copper(I) complexes of metallothionein, Inorg. Chim. Acta 153, 115–118.CrossRefGoogle Scholar
  43. 43.
    Cai, W. and Stillman, M.J. (1988) Metal binding to MT: Competition for cadmium and zinc between Chelex-100 and metal binding sites in MT, Inorg. Chim. Acta 152, 111–115.CrossRefGoogle Scholar
  44. 44.
    Stillman, M. J., Cai, W., and Zelazowski, A. J. (1987) Cadmium binding to metallothioneins domain specificity in reactions of α and β fragments, apometallothionein, and zinc metallothionein with Cd, J. Biol. Chem. 262, 4538–4548.Google Scholar
  45. 45.
    Stillman, M.J. and Zelazowski, A.J. (1988) Domain specificity in metal binding to metallothionein. A CD and MCD study of Cd and Zn binding at temperature extremes, J. Biol. Chem. 263, 6128–6133.Google Scholar
  46. 46.
    Otvos J.D. and Armitage, I.M. (1980) Structure of the metal clusters in rabbit liver metallothionein MT, 113Cd NMR, Proc. Natl. Acad. Sci. USA 77, 7094–7098.CrossRefGoogle Scholar
  47. 47.
    Messerle, B. A., Schaffer, A., Vasak, M., Kagi, J.H.R., and Wuthrich, K. (1992) Comparison of the solution conformations of human [Zn7]-metallothionein-2 and [Cd7J-metallothionein-2 using NMR spectroscopy, J. Mol. Biol. 225, 433–443.CrossRefGoogle Scholar
  48. 48.
    Worgotter, E., Wagner, G., Vasak, M., Kagi, J. H. R., and Wuthnch, K (1987) Sequence specific H NMR assignments in rat liver MT. Eur. J. Biochem. 167, 457–466.CrossRefGoogle Scholar
  49. 49.
    Frey, M., Wagner, G., Vasak, M., Sorensen, O., Neuhaus, D., Worgotter, E., Kagi, J.H.R., Ernst, R. R., and Wuthrich, K. (1985) Polypeptide-metal cluster connectivities in MT 2 by novel 1H-ll3Cd heteronuclear two-dimensional NMR experiments, J. Am. Chem. Soc. 107, 6847–6851.CrossRefGoogle Scholar
  50. 50.
    Petering, D.H., Quesada, A., Dughish, M., Krull, S., Gan, T., Lemkuil, D., Pattanaik, A., Byrnes, R.W., Savas, M., Whelan, H., and Shaw, C.F. (1993) Metallothionein in tumor and host: Intersections of zinc metabolism, the stress response, and tumor therapy in Suzuki, K.T., Imura, N. and Kimura, M. (eds.) Metallothionein III, Birkhauser Verlag, Basel, pp. 329–346.Google Scholar
  51. 51.
    Hamer, D.H. (1993) Molecular genetics of metallothionein: An overview in Suzuki, K.T., Imura, N. and Kimura, M. (eds.) (1993) Metallothionein III, Birkhauser Verlag, Basel, pp. 347–350.Google Scholar
  52. 52.
    Suzuki, K. T. (1992) Preparation of metallothioneins in M. J. Stillman, C. F. Shaw III, and K. T. Suzuki (eds.), Metallothioneins, VCH Publishers, New York, pp. 14–30.Google Scholar
  53. 53.
    Beattie, J. H. and Richards, M. P. (1994) Separation of metallothionein isoforms by micellar electrokinetic capillary chromatography, J. Chromat. A 664, 129–134CrossRefGoogle Scholar
  54. 54.
    Mann, M., Meng, C. K., and Fenn, J.B. (1989) Interpreting mass spectra of multiply charged ions, Anal. Chem. 61, 1702–1708.CrossRefGoogle Scholar
  55. 55.
    Yu, X., Wojciechowski, M., and Fenselau, C. (1993) Assessment of metals in reconstituted metallothioneins by electrospray mass spectrometry, Anal. Chem. 65, 1355–1359CrossRefGoogle Scholar
  56. 56.
    Le Blanc, J.C.Y., Siu, K.W.M., and Guevremont, R. (1994) Electrospray mass spectrometnc study of protein-ketone equilibria in solution, Anal. Chem. 66, 3289–3296CrossRefGoogle Scholar
  57. 57.
    Winge, D.H. and Dameron, C.T. (1993) The metallothionein structural motif involved in metalloregulation in Suzuki, K.T., Imura, N. and Kimura, M. (eds.) Metallothionein III, Birkhauser Verlag, Basel, pp. 381–397.Google Scholar
  58. 58.
    Presta, P.A., Fowle, D.A., and Stillman, M.J. (1996) Structural model of mammalian copper metallothionein, submitted.Google Scholar
  59. 59.
    George, G.N., Winge, D.R., Stout, CD. and Cramer, S.P. (1986) X-ray absorption studies of the copper-beta domain of rat liver metallothionein, J. Inorg. Biochem. 27, 213–220.CrossRefGoogle Scholar
  60. 60.
    Abrahams, I.L, Bremner, I., Diakun, G.P., Garner, CD., Hasnain, S.S., Ross, I., and Vasak, M. (1986) Structural study of the copper and zinc sites in MTs by using extended X-ray-absorption fine structure, Biochem. J., 236, 585–589.Google Scholar
  61. 61.
    Smith, T.A., Lerch, K., and Hodgson, K.O. (1986) Structural study of the Cu sites in metallothionein from Neurospora crassa, Inorg. Chem. 25, 4677–4680.CrossRefGoogle Scholar
  62. 62.
    Nakagawa, K.H., Inouye, C., Hedman, B., Kann, M., Tullius, T.D., and Hodgson, K.O. (1991) Evidence from EXAFS for a copper cluster in the metalloregulatory protein CUP2 from yeast, J. Am. Chem. Soc 113, 3621–3623.CrossRefGoogle Scholar
  63. 63.
    Nielson, K.B. and Winge, D.R. (1985) Independence of the domains of MT in metal binding, J. Biol. Chem. 260, 8698–8701.Google Scholar
  64. 64.
    Byrd, J. and Winge, D.R. (1986) Cooperative cluster formation in metallothionein, Arch. Biochem. Biophys. 250, 233–237CrossRefGoogle Scholar
  65. 65.
    Winge, D. R. (1991) Copper coordination in metallothionein in B. Vallee and J.F. Riordan (eds.), Methods in Enzymology, Metallobiochemistry part B, Metallothionein and Related Molecules, Academic Press, New York, vol. 205, pp 458–469.CrossRefGoogle Scholar
  66. 66.
    Dance, I., Fisher, K., and Lee, G. (1992) Metal thiolate compounds in M.J. Stillman, C.F. Shaw III, and KT. Suzuki (eds.), Metallothioneins, VCH Publishers, New York, pp. 284–345.Google Scholar
  67. 67.
    Margoshes, M. and Vallee, B.L. (1957) A Cd(II) protein from equine kidney cortex, J. Am Chem. Soc. 79, 4813–4814.CrossRefGoogle Scholar
  68. 68.
    Kagi, J.H.R. and Vallee, B.L. (1960) Metallothionein: a cadmium and zinc-containing protein from equine renal cortex., J. Biol. Chem. 235, 3460.Google Scholar
  69. 69.
    Kagi, J.H.R. and Vallee, B.L. (1961) Metallothionein: a cadmium and zinc-containing protein from equine renal cortex., J. Biol. Chem. 236, 2435.Google Scholar
  70. 70.
    Good, M. and Vasak, M. (1986) Spectroscopic properties of the cobalt(ii)-substituted α-fragment of rabbit liver metallothionein, Biochem. 25, 3328–3334.CrossRefGoogle Scholar
  71. 71.
    Beltramini, M. and Lerch, K. (1981) Luminescence properties of Neurospora Cu(I)-MT, FEBS Lett. 127, 201–203.CrossRefGoogle Scholar
  72. 72.
    Beltramini, M. and Lerch, K. (1982) Copper transfer between Neurospora Cu(I)-MT and type 3 copper apoproteins, FEBS Lett. 142, 219–222.CrossRefGoogle Scholar
  73. 73.
    Beltramini, M. and Lerch, K. (1983) Spectroscopic studies on Neurospora copper metallothionein, Biochem. 22, 2043–2048.CrossRefGoogle Scholar
  74. 74.
    Beltramini, M., Munger, K., Germann, U.A. and Lerch, K. (1987) Luminescence emission from the Cu(I)-thiolate complex in metallothioneins, in J.H.R Kagi and Y. Kojima (eds.) Metallothionein II, Birkhauser Verlag, Basel, pp. 237–241.Google Scholar
  75. 75.
    Presta, P.A. and Stillman, M.J. (1996) Incorporation of copper into the yeast Saccharomyces cerevisiae. Identification of Cu(I)MT in intact yeast cells, J. Inorg. Biochem., in press.Google Scholar
  76. 76.
    Green, A.R., Presta, P.A., and Stillman, M.J. (1996) Copper binding to metallothionein at low pH, submitted.Google Scholar
  77. 77.
    Suzuki, K.T., Yamamoto, K., Kanno, S., Aoki, Y., and Takeichi, N. (1993) Selective removal copper bound to metallothionein in the liver of LEC rats by tetrathiomolybdate, Toxicol. 83, 149–158.CrossRefGoogle Scholar
  78. 78.
    Winge, D.R. and Miklossy, K.A. (1982) Domain nature of metallothionein. J. Biol. Chem. 257, 3471–3476.Google Scholar
  79. 79.
    Dean, P.A.W. and Vittal, J.J. (1992) Adamantane-like cages in M.J. Stillman, C. F. Shaw III, and K. T. Suzuki (eds.), Metallothioneins, VCH Publishers, New York, pp. 346–386.Google Scholar
  80. 80.
    Hasnain, S.S., Diakun, G.P., Abrahams, I., Ross, I., Garner, C.D, Bremner, I., and Vasak, M. (1987) EXAFS studies of metallothioniens in J.H.R. Kagi, and Y. Kojima (eds.) Metallothionein II, Birkhauser Verlag, Basel, pp. 227–236.Google Scholar
  81. 81.
    Winge, D.R., Dameron, C.T., and Mehra, R.K. (1992) Metal-sulfide quantum crytalhtes in yeast. In M.J. Stillman, C.F. Shaw III, and K.T. Suzuki (eds.) Metallothioneins, VCH Publishers, New York, pp. 257–270.Google Scholar
  82. 82.
    Pickering, I.J., George, G.N., Dameron, C.T., Kurz, B., Winge, D.R., and Dance, I.G. (1993) X-ray absorption spectroscopy of cuprous-thiolate clusters in proteins and model systems. J. Am. Chem. Soc. 115, 9498–9505.CrossRefGoogle Scholar
  83. 83.
    Dance I.G., Bowmaker, G.A., Clark, G.R., and Seadon, J.K. (1983) The formation and crystal and molecular structures of hexa(-organothiolato)tetracuprate(I) cage dianions: bis-(tetramethylammonium) hexa-(-methanethiolato)tetracuprate(I) and two polymorphs, Polyhedron 2, 10, 1031–1043CrossRefGoogle Scholar
  84. 84.
    Allinger, N.L (1977) Conformational Analysis. 130. MM2. A hydrocarbon force field utilizing V1 and V2 torsional terms, J. Am. Chem. Soc. 99, 8127–8134.CrossRefGoogle Scholar
  85. 85.
    Munger, K., Germann, U.A., Beltramini, M., Niedermann, D., Baitella-Eberle, G., Kagi, J.H.R., and Lerch, K (1985) (Cu, Zn)-Metallothioneins from fetal bovine liver, J. Biol. Chem. 260, 10032–10038.Google Scholar
  86. 86.
    Szymanska, J.A., Zelazowski, A.J., and Stillman, M.J. (1983) Spectroscopic characterization of rat kidney Hg, Cu-MT, Biochem. Biophys. Res. Commun. 115, 167–173.CrossRefGoogle Scholar
  87. 87.
    Oikawa, T., Esaki, N., Tanaka, H., and Soda, K. (1991) Metalloselenonein, the selenium analogue of metallothionein: synthesis and characterization of its complex with copper ions, Proc. Natl. Acad. Sci. USA 88, 3058–3059.CrossRefGoogle Scholar
  88. 88.
    Byrd, J., Berger, R.M., McMillin, D.R., Wright, C.F., Hamer, D., and Winge, D.R. (1988) Characterization of the copper-thiolate cluster in yeast MT and 2 truncated mutants, J. Biol. Chem. 263, 6688–6694.Google Scholar
  89. 89.
    Thrower, A.R., Byrd, J., Tarbett, E.B., Mehra, R.R., Hamer, D.H., and Winge, D.R. (1988) Effect of mutation of cysteinyl residues in yeast Cu(I)-MT, J. Biol. Chem. 263, 7037–7042.Google Scholar
  90. 90.
    Felix, K., Hartmann, H-J., and Weser, U. (1989) Cu(I>thionein release from Cu-loaded yeast cells, Biol. Metals 2, 50–54.CrossRefGoogle Scholar
  91. 91.
    Narula, S.S., Mehra, R.K., Winge, D.R., and Armitage, I.M. (1991), Establishment of the metal-to-cysteine connectivities in silver-substituted yeast metallothionein, J. Am. Chem. Soc. 113, 9354–9358.CrossRefGoogle Scholar
  92. 92.
    Stephan, D.W. and Hitchcock, A.P. (1987) EXAFS Studies of [N(C2H5)4]2[M(SC6H5)4] and [N(C2H5)4]2[M4(SC6H5)10](M = Zn, Cd): Model Compounds for Zn and CdMT, Inorg. Chim. Acta 136, L1-L5.Google Scholar
  93. 93.
    Johnson, B.A. and Armitage, I.M. (1987) Equilibrium and kinetic analysis of the interaction of Hg(II) with Cd(II) MT, Inorg. Chem. 26, 3139–3145.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1997

Authors and Affiliations

  • Martin J. Stillman
    • 1
  1. 1.Department of ChemistryThe University of Western OntarioLondonCanada

Personalised recommendations