Use of 113Cd NMR to Probe the Native Metal Binding Sites in Metalloproteins: An Overview

  • Ian M. Armitage
  • Torbjörn Drakenberg
  • Brian Reilly
Part of the Metal Ions in Life Sciences book series (MILS, volume 11)

Abstract

Our laboratories have actively published in this area for several years and the objective of this chapter is to present as comprehensive an overview as possible. Following a brief review of the basic principles associated with 113Cd NMR methods, we will present the results from a thorough literature search for 113Cd chemical shifts from metalloproteins. The updated 113Cd chemical shift figure in this chapter will further illustrate the excellent correlation of the 113Cd chemical shift with the nature of the coordinating ligands (N, O, S) and coordination number/geometry, reaffirming how this method can be used not only to identify the nature of the protein ligands in uncharacterized cases but also the dynamics at the metal binding site. Specific examples will be drawn from studies on alkaline phosphatase, Ca2+ binding proteins, and metallothioneins.

In the case of Escherichia coli alkaline phosphatase, a dimeric zinc metalloenzyme where a total of six metal ions (three per monomer) are involved directly or indirectly in providing the enzyme with maximal catalytic activity and structural stability, 113Cd NMR, in conjunction with 13C and 31P NMR methods, were instrumental in separating out the function of each class of metal binding sites. Perhaps most importantly, these studies revealed the chemical basis for negative cooperativity that had been reported for this enzyme under metal deficient conditions. Also noteworthy was the fact that these NMR studies preceeded the availability of the X-ray crystal structure.

In the case of the calcium binding proteins, we will focus on two proteins: calbindin D9k and calmodulin. For calbindin D9k and its mutants, 113Cd NMR has been useful both to follow actual changes in the metal binding sites and the cooperativity in the metal binding. Ligand binding to calmodulin has been studied extensively with 113Cd NMR showing that the metal binding sites are not directly involved in the ligand binding. The 113Cd chemical shifts are, however, exquisitely sensitive to minute changes in the metal ion environment.

In the case of metallothionein, we will reflect upon how 113Cd substitution and the establishment of specific Cd to Cys residue connectivity by proton-detected heteronuclear 1H-113Cd multiple-quantum coherence methods (HMQC) was essential for the initial establishment of the 3D structure of metallothioneins, a protein family deficient in the regular secondary structural elements of α-helix and β-sheet and the first native protein identified with bound Cd. The 113Cd NMR studies also enabled the characterization of the affinity of the individual sites for 113Cd and, in competition experiments, for other divalent metal ions: Zn, Cu, and Hg.

Keywords

alkaline phosphatase calbindin calcium-binding proteins calmodulin metallothionein 113Cd NMR methods 113Cd NMR chemical shifts from metalloproteins 

Abbreviations

AP

alkaline phosphatase

AztR

aztR gene product

CadC

cad operon transcription regulating protein

CaM

calmodulin

CaMKI

calcium-calmodulin-dependent protein kinase I

cNOS

constitutive nitric oxide synthase

Com

bacteriophage MU com gene product

CSA

chemical shift anisotropy

D600

α[3-{[2-(3,4-dimethoxyphenyl)-ethyl]-methylamino}propyl]-3,4,5-trimethoxy-α-(1-methylethyl)-benzene-acetonitrile

GIF

neuronal growth inhibitory factor

HCAB

human carbonic anhydrase

HMQC

heteronuclear multiple quantum correlation

M13

KRRWKKNFIAVSAANRFKKISSSGAL

MT

metallothionein

NMR

nuclear magnetic resonance

NOE

nuclear Overhauser enhancement

p7

HIV-1 nucleic acid binding protein

R1

spin-lattice relaxation rate

Rd

rubredoxin

RDC

residual dipolar coupling

SAXS

small angle X-ray scattering

skMLCK

skeletal myosin light chain kinase

TFP

trifluoperazine

TR1C

N-terminal half of calmodulin

TR2C

C-terminal half of calmodulin

References

  1. 1.
    I. M. Armitage, R. T. Pajer, A. J. M. Schoot Uiterkamp, J. F. Chlebowski, J. E. Coleman, J. Am. Chem. Soc. 1976, 98, 5710–5712.PubMedCrossRefGoogle Scholar
  2. 2.
    J. F. Chlebowski, I. M. Armitage, J. E. Coleman, J. Biol. Chem. 1977, 252, 7053–7061.Google Scholar
  3. 3.
    I. M. Armitage, A. J. M. Schoot Uiterkamp, J. F. Chlebowski, J. E. Coleman, J. Magn. Reson. 1978, 29, 375–392.Google Scholar
  4. 4.
    T. Drakenberg, B. Lindman, A. Cavé, J. Parello, FEBS Lett. 1978, 92, 346–350.PubMedCrossRefGoogle Scholar
  5. 5.
    R. J. Kostelnik, A. A. Bothner-By, J. Magn. Reson. 1974, 14, 141–151.Google Scholar
  6. 6.
    I. M. Armitage, J. D. Otvos, Biol. Magn. Res. 1982, 4, 79–144.Google Scholar
  7. 7.
    H. J. Vogel, T. Drakenberg, S. Forsén, NMR of Newly Accessible Nuclei, Ed P. Laszlo, Vol. 1, Academic Press, New York, 1983, pp. 157–192.Google Scholar
  8. 8.
    I. M. Armitage, Y. Boulanger, NMR of Newly Accessible Nuclei, Ed P. Laszlo, Vol. 2, Academic Press, New York, 1983, pp. 337–365.Google Scholar
  9. 9.
    M. F. Summers, Coord. Chem. Rev. 1988, 86, 43–134.CrossRefGoogle Scholar
  10. 10.
    C. Johansson, T. Drakenberg, Annu. Rep. NMR Spectrosc. 1990, 22, 1-59.CrossRefGoogle Scholar
  11. 11.
    G. Öz, D. L. Pountney, I. M. Armitage, Biochem. Cell Biol. 1998, 76, 223–234.Google Scholar
  12. 12.
    K. Zangger, I. M. Armitage, Handbook of Metalloproteins, Eds A. Messerschmidt, M. Cygler, W. Bode, John Wiley & Sons Ltd., Chichester, UK, 2004.Google Scholar
  13. 13.
    P. S. Marchetti, P. D. Ellis, R. G. Bryant, J. Am. Chem. Soc. 1985, 107, 8191–8196.CrossRefGoogle Scholar
  14. 14.
    M. Sola, Inorg. Chem. 1990, 29, 1113–1116.CrossRefGoogle Scholar
  15. 15.
    A. R. Palmer, D. B. Bailey, W. D. Benhke, A. D. Cardin, P. P. Yang, P. D. Ellis, Biochemistry 1980, 19, 5063–5070.PubMedCrossRefGoogle Scholar
  16. 16.
    K. M. Welsh, I. M. Armitage, B. S. Cooperman, Biochemistry 1983, 22, 1046–1054.PubMedCrossRefGoogle Scholar
  17. 17.
    H. R. Engeseth, D. R. McMillin, J. D. Otvos, J. Biol. Chem. 1984, 259, 4822.PubMedGoogle Scholar
  18. 18.
    F. A. Cotton, G. Wilkinson, Advanced Inorganic Chemistry, Wiley, New York, 1988.Google Scholar
  19. 19.
    J. M. Aramini, T. Hiraoki, Y. Ke, K. Nitta, H. J. Vogel, J. Biochem. 1995, 117, 623–628.PubMedGoogle Scholar
  20. 20.
    T. Drakenberg, The Biological Chemistry of Magnesium, Ed J. A. Cowan, VCH Publishers Inc., New York, Weinheim, Cambridge, 1995, 27–51.Google Scholar
  21. 21.
    G. E. Maciel, M. Borzo, J. Chem. Soc., Chem. Commun. 1973, 394a–394a.Google Scholar
  22. 22.
    A. D. Cardin, P. D. Ellis, J. D. Odom, J. W. Howard Jr, J. Am. Chem. Soc. 1975, 97, 1672–1679.CrossRefGoogle Scholar
  23. 23.
    M. Karplus, J. Chem. Phys. 1959, 30, 11–15.Google Scholar
  24. 24.
    O. Zerbe, D. L. Pountney, W. von Philipsborn, M. Vašák, J. Am. Chem. Soc. 1994, 116, 377–378.CrossRefGoogle Scholar
  25. 25.
    J. D. Otvos, I. M. Armitage, Biochemistry 1980, 19, 4031–4043.PubMedCrossRefGoogle Scholar
  26. 26.
    J. E. Coleman, I. M. Armitage, J. F. Chlebowski, J. D. Otvos, A. J. M. Schoot Uiterkamp, Biological Applications of Magnetic Resonance, Academic Press, London New York 1979, 345–395.Google Scholar
  27. 27.
    R. A. Dwek, Nuclear Magnetic Resonance (NMR) in Biochemistry: Applications to Enzyme Systems, Clarendon Press, Oxford, 1973.Google Scholar
  28. 28.
    E. Hsi, R. G. Bryant, J. Phys. Chem. 1977, 81, 462–465.Google Scholar
  29. 29.
    L. E. Kay, D. A. Torchia, A. Bax, Biochemistry 1989, 28, 8972–8979.PubMedCrossRefGoogle Scholar
  30. 30.
    L. Werbelow, J. Magn. Reson. 1984, 57, 136–139.Google Scholar
  31. 31.
    L. G. Werbelow, J. Chem. Soc., Faraday Trans. 2 1987, 83, 897–904.Google Scholar
  32. 32.
    I. Morishima, M. Kurono, Y. Shiro, J. Biol. Chem. 1986, 261, 9391–9399.Google Scholar
  33. 33.
    H. J. Vogel, T. Drakenberg, S. Forsén, J. D. J. O'Neil, T. Hofmann, Biochemistry 1985, 24, 3870–3876.PubMedCrossRefGoogle Scholar
  34. 34.
    S. Linse, P. Brodin, T. Drakenberg, E. Thulin, P. Sellers, K. Elmdén, T. Grundström, S. Forsén, Biochemistry 1987, 26, 6723–6735.PubMedCrossRefGoogle Scholar
  35. 35.
    P. Brodin, C. Johansson, S. Forsén, T. Drakenberg, T. Grundström, J. Biol. Chem. 1990, 265, 11125–11130.Google Scholar
  36. 36.
    C. Johansson, P. Brodin, T. Grundström, E. Thulin, S. Forsén, T. Drakenberg, Eur. J. Biochem. 1990, 187, 455–460.PubMedCrossRefGoogle Scholar
  37. 37.
    C. Johansson, P. Brodin, T. Grundström, S. Forsén, T. Drakenberg, Eur. J. Biochem. 1991, 202, 1283–1290.PubMedCrossRefGoogle Scholar
  38. 38.
    S. Linse, C. Johansson, P. Brodin, T. Grundstroem, T. Drakenberg, S. Forsén, Biochemistry 1991, 30, 154–162.PubMedCrossRefGoogle Scholar
  39. 39.
    J. Kördel, C. Johansson, T. Drakenberg, J. Magn. Reson. 1992, 100, 581–587.Google Scholar
  40. 40.
    S. Linse, E. Thulin, P. Sellers, Protein Sci. 1993, 2, 985–1000.PubMedCrossRefGoogle Scholar
  41. 41.
    S. Linse, N. R. Bylsma, T. Drakenberg, P. Sellers, S. Forsén, E. Thulin, L. A. Svensson, I. Zajtzeva, V. Zajtsev, J. Marek, Biochemistry 1994, 33, 12478–12486.PubMedCrossRefGoogle Scholar
  42. 42.
    N. Bylsma, T. Drakenberg, I. Andersson, P. F. Leadlay, S. Forsén, FEBS Lett. 1992, 299, 44–47.PubMedCrossRefGoogle Scholar
  43. 43.
    S. Forsén, E. Thulin, H. Lilja, FEBS Lett. 1979, 104, 123–126.PubMedCrossRefGoogle Scholar
  44. 44.
    O. Teleman, T. Drakenberg, S. Forsén, E. Thulin, Eur. J. Biochem. 1983, 134, 453–457.PubMedCrossRefGoogle Scholar
  45. 45.
    P. D. Ellis, P. Strang, J. D. Potter, J. Biol. Chem. 1984, 259, 10348–10356.Google Scholar
  46. 46.
    T. Drakenberg, S. Forsén, E. Thulin, H. J. Vogel, J. Biol. Chem. 1987, 262, 672–678.Google Scholar
  47. 47.
    P. D. Ellis, P. S. Marchetti, P. Strang, J. D. Potter, J. Biol. Chem. 1988, 263, 10284–10288.Google Scholar
  48. 48.
    S. Forsén, E. Thulin, T. Drakenberg, J. Krebs, K. Seamon, FEBS Lett. 1980, 117, 189–194.PubMedCrossRefGoogle Scholar
  49. 49.
    S. L. Boström, B. Ljung, S. Mårdh, S. Forsén, E. Thulin, Nature 1981, 292, 777–778.PubMedCrossRefGoogle Scholar
  50. 50.
    T. Andersson, T. Drakenberg, S. Forsén, E. Thulin, Eur. J. Biochem. 1982, 126, 501–505.PubMedCrossRefGoogle Scholar
  51. 51.
    A. Andersson, S. Forsén, E. Thulin, H. J. Vogel, Biochemistry 1983, 22, 2309–2313.PubMedCrossRefGoogle Scholar
  52. 52.
    A. Andersson, T. Drakenberg, E. Thulin, S. Forsén, Eur. J. Biochem. 1983, 134, 459–465.PubMedCrossRefGoogle Scholar
  53. 53.
    E. Thulin, A. Andersson, T. Drakenberg, S. Forsén, H. J. Vogel, Biochemistry 1984, 23, 1862–1870.PubMedCrossRefGoogle Scholar
  54. 54.
    S. Linse, T. Drakenberg, S. Forsén, FEBS Lett. 1986, 199, 28–32.PubMedCrossRefGoogle Scholar
  55. 55.
    M. Ikura, N. Hasegawa, S. Aimoto, M. Yazawa, K. Yagi, K. Hikichi, Biochem. Biophys. Res. Commun. 1989, 161, 1233–1238.PubMedCrossRefGoogle Scholar
  56. 56.
    S. Ohki, U. Iwamoto, S. Aimoto, M. Yazawa, K. Hikichi, J. Biol. Chem. 1993, 268, 12388–12392.Google Scholar
  57. 57.
    M. Zhang, T. Yuan, J. M. Aramini, H. J. Vogel, J. Biol. Chem. 1995, 270, 20901–20907.Google Scholar
  58. 58.
    R. D. Brokx, H. J. Vogel, Protein Sci. 2000, 9, 964–975.PubMedCrossRefGoogle Scholar
  59. 59.
    T. Yuan, A. V. Gomes, J. A. Barnes, H. N. Hunter, H. J. Vogel, Arch. Biochem. Biophys. 2004, 421, 192–206.PubMedCrossRefGoogle Scholar
  60. 60.
    L. T. Kakalis, M. Kennedy, R. Sikkink, F. Rusnak, I. M. Armitage, FEBS Lett. 1995, 362, 55–58.PubMedCrossRefGoogle Scholar
  61. 61.
    A. Cavé, J. Parello, T. Drakenberg, E. Thulin, B. Lindman, FEBS Lett. 1979, 100, 148–152.PubMedCrossRefGoogle Scholar
  62. 62.
    A. Cavé, A. Saint-Yves, J. Parello, M. Swärd, E. Thulin, B. Lindman, Mol. Cell. Biochem. 1982, 44, 161–172.PubMedCrossRefGoogle Scholar
  63. 63.
    L. Lee, B. D. Sykes, Biochemistry 1983, 22, 4366–4373.PubMedCrossRefGoogle Scholar
  64. 64.
    T. Drakenberg, M. Swärd, A. Cavé, J. Parello, Biochem. J. 1985, 227, 711–717.PubMedGoogle Scholar
  65. 65.
    M. E. Bjornson, D. C. Corson, B. D. Sykes, J. Inorg. Biochem. 1985, 25, 141–149.Google Scholar
  66. 66.
    M. Svärd, T. Drakenberg, Acta Chem. Scand. B: Org. Chem. Biochem. 1986, 40, 689–693.CrossRefGoogle Scholar
  67. 67.
    C. Zhang, D. J. Nelson, J. Alloys Compd. 1992, 180, 349–356.CrossRefGoogle Scholar
  68. 68.
    L. J. Berliner, P. D. Ellis, K. Murakami, Biochemistry 1983, 22, 5061–5063.PubMedCrossRefGoogle Scholar
  69. 69.
    L. Bhattacharyya, P. S. Marchetti, P. D. Ellis, C. F. Brewer, J. Biol. Chem. 1987, 262, 5616–5621.Google Scholar
  70. 70.
    D. B. Bailey, P. D. Ellis, A. D. Cardin, W. D. Behnke, J. Am. Chem. Soc. 1978, 100, 5236–5237.CrossRefGoogle Scholar
  71. 71.
    E. Chiancone, T. Drakenberg, O. Teleman, S. Forsén, J. Mol. Biol. 1985, 185, 201–207.Google Scholar
  72. 72.
    F. Adebodun, F. Jordan, Biochemistry 1989, 28, 7524–7531.PubMedCrossRefGoogle Scholar
  73. 73.
    J. L. Sudmeier, S. J. Bell, M. C. Storm, M. F. Dunn, Science 1981, 212, 560–562.PubMedCrossRefGoogle Scholar
  74. 74.
    K. M. Welsh, B. S. Cooperman, Biochemistry 1984, 23, 4947–4955.PubMedCrossRefGoogle Scholar
  75. 75.
    R. S. Ehrlich, R. F. Colman, Biochemistry 1989, 28, 2058–2065.PubMedCrossRefGoogle Scholar
  76. 76.
    R. S. Ehrlich, R. F. Colman, Biochim. Biophys. Acta-Protein Struct. Mol. Enzym. 1995, 1246, 135–141.CrossRefGoogle Scholar
  77. 77.
    P. B. Kingsley-Hickman, G. L. Nelsestuen, K. Ugurbil, Biochemistry 1986, 25, 3352–3355.PubMedCrossRefGoogle Scholar
  78. 78.
    G. I. Rhyu, W. J. Ray Jr, J. L. Markley, Biochemistry 1985, 24, 2536–2541.PubMedCrossRefGoogle Scholar
  79. 79.
    W. J. Ray Jr, C. B. Post, Y. Liu, G. I. Rhyu, Biochemistry 1993, 32, 48–57.PubMedCrossRefGoogle Scholar
  80. 80.
    J. D. Otvos, J. R. Alger, J. E. Coleman, I. M. Armitage, J. Biol. Chem. 1979, 254, 1778–1780.Google Scholar
  81. 81.
    J. D. Otvos, I. M. Armitage, J. F. Chlebowski, J. E. Coleman, J. Biol. Chem. 1979, 254, 4707–4713.Google Scholar
  82. 82.
    J. D. Otvos, I. M. Armitage, Biochemistry 1980, 19, 4021–4030.PubMedCrossRefGoogle Scholar
  83. 83.
    P. Gettins, J. E. Coleman, J. Biol. Chem. 1983, 258, 396–407.Google Scholar
  84. 84.
    P. Gettins, J. E. Coleman, J. Biol. Chem. 1984, 259, 4987–4990.Google Scholar
  85. 85.
    P. Gettins, J. E. Coleman, J. Biol. Chem. 1984, 259, 4991–4997.Google Scholar
  86. 86.
    P. Gettins, J. E. Coleman, J. Biol. Chem. 1984, 259, 11036–11040.Google Scholar
  87. 87.
    J. Afflitto, K. A. Smith, M. Patel, A. Esposito, E. Jensen, A. Gaffar, Pharm. Res. 1991, 8, 1384–1388.PubMedCrossRefGoogle Scholar
  88. 88.
    E. O. Martins, T. Drakenberg, Inorg. Chim. Acta 1982, 67, 71–74.Google Scholar
  89. 89.
    W. Göumakos, J. P. Laussac, B. Sarkar, Biochem. Cell Biol. 1991, 69, 809–820.Google Scholar
  90. 90.
    P. J. Sadler, J. H. Viles, Inorg. Chem. 1996, 35, 4490–4496.PubMedCrossRefGoogle Scholar
  91. 91.
    K. Aalmo, J. Krane, C. Little, C. S. Storm, Biochem. Soc. Trans. 1982, 10, 367–368.Google Scholar
  92. 92.
    K. Aalmo, L. Hansen, E. Hough, K. Jynge, J. Krane, C. Little, C. B. Storm, Biochem. Int. 1984, 8, 27–33.PubMedGoogle Scholar
  93. 93.
    K. Kanaori, N. Uodome, A. Nagai, D. Ohta, A. Ogawa, G. Iwasaki, A. Y. Nosaka, Biochemistry 1996, 35, 5949–5954.PubMedCrossRefGoogle Scholar
  94. 94.
    K. Kanaori, D. Ohta, A. Y. Nosaka, FEBS Lett. 1997, 412, 301–304.PubMedCrossRefGoogle Scholar
  95. 95.
    P. Gettins, J. Biol. Chem. 1986, 261, 15513–15518.Google Scholar
  96. 96.
    P. D. Ellis, J. Biol. Chem. 1989, 264, 3108–3110.Google Scholar
  97. 97.
    J. Matysik, G. Alia, G. Nachtegaal, H. J. van Gorkom, A. J. Hoff, H. J. M. de Groot, Biochemistry 2000, 39, 6751–6755.PubMedCrossRefGoogle Scholar
  98. 98.
    G. A. Omburo, J. M. Kuo, L. S. Mullins, F. M. Raushel, J. Biol. Chem. 1992, 267, 13278–13283.Google Scholar
  99. 99.
    G. A. Omburo, L. S. Mullins, F. M. Raushel, Biochemistry 1993, 32, 9148–9155.PubMedCrossRefGoogle Scholar
  100. 100.
    C. Damblon, C. Prosperi, L. Y. Lian, I. Barsukov, R. P. Soto, M. Galleni, J. M. Frère, G. C. K. Roberts, J. Am. Chem. Soc. 1999, 121, 11575–11576.CrossRefGoogle Scholar
  101. 101.
    L. Hemmingsen, C. Damblon, J. Antony, M. Jensen, H. W. Adolph, S. Wommer, G. C. K. Roberts, R. Bauer, J. Am. Chem. Soc. 2001, 123, 10329–10335.PubMedCrossRefGoogle Scholar
  102. 102.
    C. Damblon, M. Jensen, A. Ababou, I. Barsukov, C. Papamicael, C. J. Schofield, L. Olsen, R. Bauer, G. C. K. Roberts, J. Biol. Chem. 2003, 278, 29240–29251.Google Scholar
  103. 103.
    J. D. Otvos, W. E. Antholine, S. Wehrli, D. H. Petering, Biochemistry 1996, 35, 1458–1465.PubMedCrossRefGoogle Scholar
  104. 104.
    J. L. Sudmeier, S. J. Bell, J. Am. Chem. Soc. 1977, 99, 4499–4500.PubMedCrossRefGoogle Scholar
  105. 105.
    A. J. M. Schoot Uiterkamp, I. M. Armitage, J. E. Coleman, J. Biol. Chem. 1980, 255, 3911–3917.Google Scholar
  106. 106.
    N. B. Jonsson, L. A. Tibell, J. L. Evelhoch, S. J. Bell, J. L. Sudmeier, Proc. Natl. Acad. Sci. USA 1980, 77, 3269–3272.CrossRefGoogle Scholar
  107. 107.
    J. L. Evelhoch, D. F. Bocian, J. L. Sudmeier, Biochemistry 1981, 20, 4951–4954.PubMedCrossRefGoogle Scholar
  108. 108.
    D. B. Bailey, P. D. Ellis, J. A. Fee, Biochemistry 1980, 19, 591–596.PubMedCrossRefGoogle Scholar
  109. 109.
    P. Kofod, R. Bauer, E. Danielsen, E. Larsen, M. J. Bjerrum, Eur. J. Biochem. 1991, 198, 607–611.PubMedCrossRefGoogle Scholar
  110. 110.
    M. A. Kennedy, P. D. Ellis, J. Am. Chem. Soc. 1989, 111, 3195–3203.CrossRefGoogle Scholar
  111. 111.
    Y. Wang, L. Hemmingsen, D. P. Giedroc, Biochemistry 2005, 44, 8976–8988.PubMedCrossRefGoogle Scholar
  112. 112.
    B. R. Bobsein, R. J. Myers, J. Am. Chem. Soc. 1980, 102, 2454–2455.CrossRefGoogle Scholar
  113. 113.
    B. R. Bobsein, R. J. Myers, J. Biol. Chem. 1981, 256, 5313–5316.Google Scholar
  114. 114.
    D. Krepkiy, F. H. Försterling, D. H. Petering, Chem. Res. Toxicol. 2004, 17, 863–870.PubMedCrossRefGoogle Scholar
  115. 115.
    A. J. Bird, S. Swierczek, W. Qiao, D. J. Eide, D. R. Winge, J. Biol. Chem. 2006, 281, 25326–25335.Google Scholar
  116. 116.
    T. Liu, J. W. Golden, D. P. Giedroc, Biochemistry 2005, 44, 8673–8683.PubMedCrossRefGoogle Scholar
  117. 117.
    Z. Xiao, M. J. Lavery, M. Ayhan, S. D. B. Scrofani, M. C. J. Wilce, J. M. Guss, P. A. Tregloan, G. N. George, A. G. Wedd, J. Am. Chem. Soc. 1998, 120, 4135–4150.CrossRefGoogle Scholar
  118. 118.
    L. S. Busenlehner, N. J. Cosper, R. A. Scott, B. P. Rosen, M. D. Wong, D. P. Giedroc, Biochemistry 2001, 40, 4426–4436.PubMedCrossRefGoogle Scholar
  119. 119.
    L. S. Busenlehner, T. C. Weng, J. E. Penner-Hahn, D. P. Giedroc, J. Mol. Biol. 2002, 319, 685–701.Google Scholar
  120. 120.
    D. P. Giedroc, B. A. Johnson, I. M. Armitage, J. E. Coleman, Biochemistry 1989, 28, 2410–2418.PubMedCrossRefGoogle Scholar
  121. 121.
    D. P. Giedroc, H. Qiu, R. Khan, G. C. King, K. Chen, Biochemistry 1992, 31, 765–774.PubMedCrossRefGoogle Scholar
  122. 122.
    D. W. Fitzgerald, J. E. Coleman, Biochemistry 1991, 30, 5195–5201.PubMedCrossRefGoogle Scholar
  123. 123.
    W. J. Roberts, T. Pan, J. I. Elliott, J. E. Coleman, K. R. Williams, Biochemistry 1989, 28, 10043–10047.PubMedCrossRefGoogle Scholar
  124. 124.
    X. Chen, M. Chu, D. P. Giedroc, J. Biol. Inorg. Chem. 2000, 5, 93–101.PubMedGoogle Scholar
  125. 125.
    T. Pan, J. E. Coleman, Proc. Natl. Acad. Sci. USA 1989, 86, 3145–3149.CrossRefGoogle Scholar
  126. 126.
    T. Pan, J. E. Coleman, Proc. Natl. Acad. Sci. USA 1990, 87, 2077–2081.CrossRefGoogle Scholar
  127. 127.
    T. Pan, J. E. Coleman, Biochemistry 1990, 29, 3023–3029.CrossRefGoogle Scholar
  128. 128.
    K. H. Gardner, T. Pan, S. Narula, E. Rivera, J. E. Coleman, Biochemistry 1991, 30, 11292–11302.PubMedCrossRefGoogle Scholar
  129. 129.
    D. W. Hasler, P. Faller, M. Vašák, Biochemistry 1998, 37, 14966–14973.PubMedCrossRefGoogle Scholar
  130. 130.
    P. Faller, D. W. Hasler, O. Zerbe, S. Klauser, D. R. Winge, M. Vašák, Biochemistry 1999, 38, 10158–10167.PubMedCrossRefGoogle Scholar
  131. 131.
    M. Vašák, D. W. Hasler, P. Faller, J. Inorg. Biochem. 2000, 79, 7–10.Google Scholar
  132. 132.
    J. D. Otvos, I. M. Armitage, J. Am. Chem. Soc. 1979, 101, 7734–7736.CrossRefGoogle Scholar
  133. 133.
    J. D. Otvos, I. M. Armitage, Proc. Natl. Acad. Sci. USA 1980, 77, 7094–7098.CrossRefGoogle Scholar
  134. 134.
    J. D. Otvos, I. M. Armitage, Biochemical Structure Determination by NMR, Marcel Dekker, New York, 1982, pp. 65.Google Scholar
  135. 135.
    I. M. Armitage, J. D. Otvos, R. W. Briggs, Y. Boulanger, Fed. Proc. 1982, 41, 68–74.Google Scholar
  136. 136.
    Y. Boulanger, I. M. Armitage, J. Inorg. Biochem. 1982, 17, 147–153.Google Scholar
  137. 137.
    Y. Boulanger, I. M. Armitage, K. A. Miklossy, D. R. Winge, J. Biol. Chem. 1982, 257, 13717–13719.Google Scholar
  138. 138.
    R. W. Briggs, I. M. Armitage, J. Biol. Chem. 1982, 257, 1259–1262.Google Scholar
  139. 139.
    J. D. Otvos, R. W. Olafson, I. M. Armitage, J. Biol. Chem. 1982, 257, 2427–2431.Google Scholar
  140. 140.
    D. Neuhaus, G. Wagner, M. Vašák, J. H. R. Kägi, K. Wüthrich, Eur. J. Biochem. 1984, 143, 659–667.PubMedCrossRefGoogle Scholar
  141. 141.
    M. Vašák, G. E. Hawkes, J. K. Nicholson, P. J. Sadler, Biochemistry 1985, 24, 740–747.PubMedCrossRefGoogle Scholar
  142. 142.
    D. Live, I. M. Armitage, D. C. Dalgarno, D. Cowburn, J. Am. Chem. Soc. 1985, 107, 1775–1777.CrossRefGoogle Scholar
  143. 143.
    J. D. Otvos, H. R. Engeseth, S. Wehrli, Biochemistry 1985, 24, 6735–6740.PubMedCrossRefGoogle Scholar
  144. 144.
    E. Wörgötter, G. Wagner, M. Vašák, J. H. R. Kägi, K. Wüthrich, J. Am. Chem. Soc. 1988, 110, 2388–2393.CrossRefGoogle Scholar
  145. 145.
    M. Good, R. Hollenstein, P. J. Sadler, M. Vašák, Biochemistry 1988, 27, 7163–7166.PubMedCrossRefGoogle Scholar
  146. 146.
    F. Vazquez, M. Vašák, Biochem. J. 1988, 253, 611–614.PubMedGoogle Scholar
  147. 147.
    M. J. Cismowski, S. S. Narula, I. M. Armitage, M. L. Chernaik, P. C. Huang, J. Biol. Chem. 1991, 266, 24390–24397.Google Scholar
  148. 148.
    P. Palumaa, O. Zerbe, M. Vašák, Biochemistry 1993, 32, 2874–2879.PubMedCrossRefGoogle Scholar
  149. 149.
    S. S. Narula, I. M. Armitage, M. Brouwer, J. J. Enghild, Magn. Reson. Chem. 1993, 31, S96–S103.CrossRefGoogle Scholar
  150. 150.
    P. K. Pan, F. Y. Hou, C. W. Cody, P. C. Huang, Biochem. Biophys. Res. Commun. 1994, 202, 621–628.PubMedCrossRefGoogle Scholar
  151. 151.
    S. S. Narula, M. Brouwer, Y. Hua, I. M. Armitage, Biochemistry 1995, 34, 620–631.PubMedCrossRefGoogle Scholar
  152. 152.
    Y. Wang, E. A. Mackay, O. Zerbe, D. Hess, P. E. Hunziker, M. Vašák, J. H. R. Kägi, Biochemistry 1995, 34, 7460–7467.PubMedCrossRefGoogle Scholar
  153. 153.
    M. Vašák, Biodegradation 1998, 9, 501–512.PubMedCrossRefGoogle Scholar
  154. 154.
    K. Zangger, G. Öz, I. M. Armitage, J. D. Otvos, Protein Sci. 1999, 8, 2630–2638.PubMedCrossRefGoogle Scholar
  155. 155.
    C. You, E. A. Mackay, P. M. Gehrig, P. E. Hunziker, J. H. R. Kägi, Arch. Biochem. Biophys. 1999, 372, 44–52.PubMedCrossRefGoogle Scholar
  156. 156.
    R. Riek, B. Prêcheur, Y. Wang, E. A. Mackay, G. Wider, P. Güntert, A. Liu, J. H. R. Kägi, K. Wüthrich, J. Mol. Biol. 1999, 291, 417–428.Google Scholar
  157. 157.
    J. Mendieta, M. S. Diaz–Cruz, A. Monjonell, R. Tauler, M. Esteban, Anal. Chim. Acta 1999, 390, 15–25.Google Scholar
  158. 158.
    D. W. Hasler, L. T. Jensen, O. Zerbe, D. R. Winge, M. Vašák, Biochemistry 2000, 39, 14567–14575.PubMedCrossRefGoogle Scholar
  159. 159.
    K. Zangger, G. Shen, G. Öz, J. D. Otvos, I. M. Armitage, Biochem. J. 2001, 359, 353–360.PubMedCrossRefGoogle Scholar
  160. 160.
    M. Vaher, N. Romero-Isart, M. Vašák, P. Palumaa, J. Inorg. Biochem. 2001, 83, 1–6.Google Scholar
  161. 161.
    A. Munoz, H. F. Försterling, F. C. Shaw, D. H. Petering, J. Biol. Inorg. Chem. 2002, 7, 713–724.PubMedCrossRefGoogle Scholar
  162. 162.
    C. Capasso, V. Carginale, O. Crescenzi, D. Di Maro, E. Parisi, R. Spadaccini, P. A. Temussi, Structure 2003, 11, 435–443.PubMedCrossRefGoogle Scholar
  163. 163.
    K. E. Rigby Duncan, C. W. Kirby, M. J. Stillman, FEBS J. 2008, 275, 2227–2239.PubMedCrossRefGoogle Scholar
  164. 164.
    H. Wang, H. Li, B. Cai, Z. X. Huang, H. Sun, J. Biol. Inorg. Chem. 2008, 13, 411–419.PubMedCrossRefGoogle Scholar
  165. 165.
    G. Digilio, C. Bracco, L. Vergani, M. Botta, D. Osella, A. Viarengo, J. Biol. Inorg. Chem. 2009, 14, 167–178.PubMedCrossRefGoogle Scholar
  166. 166.
    D. E. K. Sutherland, M. J. Willans, M. J. Stillman, Biochemistry, 49, 3593–3601.Google Scholar
  167. 167.
    T. L. South, B. Kim, M. F. Summers, J. Am. Chem. Soc. 1989, 111, 395–396.CrossRefGoogle Scholar
  168. 168.
    R. A. Farrell, J. L. Thorvaldsen, D. R. Winge, Biochemistry 1996, 35, 1571–1580.PubMedCrossRefGoogle Scholar
  169. 169.
    J. W. Michelsen, K. L. Schmeichel, M. C. Beckerle, D. R. Winge, Proc. Natl. Acad. Sci. USA 1993, 90, 4404–4408.CrossRefGoogle Scholar
  170. 170.
    J. L. Kosa, J. W. Michelsen, H. A. Louis, J. I. Olsen, D. R. Davis, M. C. Beckerle, D. R. Winge, Biochemistry 1994, 33, 468–477.PubMedCrossRefGoogle Scholar
  171. 171.
    J. W. Michelsen, A. K. Sewell, H. A. Louis, J. I. Olsen, D. R. Davis, D. R. Winge, M. C. Beckerle, J. Biol. Chem. 1994, 269, 11108–11113.Google Scholar
  172. 172.
    Y. Iko, T. S. Kodama, N. Kasai, T. Oyama, E. H. Morita, T. Muto, M. Okumura, R. Fujii, T. Takumi, S. Tate, J. Biol. Chem. 2004, 279, 44834–44840.Google Scholar
  173. 173.
    L. C. Myers, M. P. Terranova, A. E. Ferentz, G. Wagner, G. L. Verdine, Science 1993, 261, 1164–1167.PubMedCrossRefGoogle Scholar
  174. 174.
    E. H. Morita, T. Ohkubo, I. Kuraoka, M. Shirakawa, K. Tanaka, K. Morikawa, Genes Cells 1996, 1, 437–442.PubMedCrossRefGoogle Scholar
  175. 175.
    J. Timmerman, A. L. Vuidepot, F. Bontems, J. Y. Lallemand, M. Gervais, E. Shechter, B. Guiard, J. Mol. Biol. 1996, 259, 792–804.Google Scholar
  176. 176.
    H. Hanzawa, M. J. de Ruwe, T. K. Albert, P. C. van der Vliet, H. T. M. Timmers, R. Boelens, J. Biol. Chem. 2001, 276, 10185–10190.Google Scholar
  177. 177.
    T. Pan, Y. D. Halvorsen, R. C. Dickson, J. E. Coleman, J. Biol. Chem. 1990, 265, 21427–21429.Google Scholar
  178. 178.
    R. M. A. Knegtel, R. Boelens, M. L. Ganadu, A. V. E. George, P. T. Vandersaag, R. Kaptein, Biochem. Biophys. Res. Commun. 1993, 192, 492–498.PubMedCrossRefGoogle Scholar
  179. 179.
    T. Pan, L. P. Freedman, J. E. Coleman, Biochemistry 1990, 29, 9218–9225.PubMedCrossRefGoogle Scholar
  180. 180.
    E. Kellenbach, B. A. Maler, K. R. Yamamoto, R. Boelens, R. Kaptein, FEBS Lett. 1991, 291, 367–370.PubMedCrossRefGoogle Scholar
  181. 181.
    C. J. Henehan, D. L. Pountney, M. Vašák, O. Zerbe, Protein Sci. 1993, 2, 1756–1764.PubMedCrossRefGoogle Scholar
  182. 182.
    H. J. Lee, L. Y. Lian, N. S. Scrutton, Biochem. J. 1997, 328, 131–136.PubMedGoogle Scholar
  183. 183.
    R. T. Witkowski, S. Hattman, L. Newman, K. Clark, D. L. Tierney, J. Penner-Hahn, G. McLendon, J. Mol. Biol. 1995, 247, 753–764.Google Scholar
  184. 184.
    W. Xia, H. Li, K. H. Sze, H. Sun, J. Am. Chem. Soc. 2009, 131, 10031–10040.PubMedCrossRefGoogle Scholar
  185. 185.
    F. Rusnak, C. Czaja, L. T. Kakalis, I. M. Armitage, Inorg. Chem. 1995, 34, 3833–3834.CrossRefGoogle Scholar
  186. 186.
    B. J. Goodfellow, I. Moura, J. J. G. Moura, F. Rusnak, T. Domke, Protein Sci. 1998, 7, 928–937.PubMedCrossRefGoogle Scholar
  187. 187.
    B. Xu, G. A. Krudy, P. R. Rosevear, J. Biol. Chem. 1993, 268, 16259–16264.Google Scholar
  188. 188.
    W. Bode, P. Schwager, J. Mol. Biol. 1975, 98, 693–717.Google Scholar
  189. 189.
    C. P. Hill, Z. Dauter, E. J. Dodson, G. G. Dodson, M. F. Dunn, Biochemistry 1991, 30, 917–924.PubMedCrossRefGoogle Scholar
  190. 190.
    K. Ravi Acharya, J. Ren, D. I. Stuart, D. C. Phillips, R. E. Fenna, J. Mol. Biol. 1991, 221, 571–581.Google Scholar
  191. 191.
    K. Inaka, R. Kuroki, M. Kikuchi, M. Matsushima, J. Biol. Chem. 1991, 266, 20666–20671.Google Scholar
  192. 192.
    M. Gajhede, D. J. Schuller, A. Henriksen, A. T. Smith, T. L. Poulos, Nat. Struct. Mol. Biol. 1997, 4, 1032–1038.CrossRefGoogle Scholar
  193. 193.
    P. C. Moews, R. H. Kretsinger, J. Mol. Biol. 1975, 91, 229–232.Google Scholar
  194. 194.
    A. L. Swain, R. H. Kretsinger, E. L. Amma, J. Biol. Chem. 1989, 264, 16620–16628.Google Scholar
  195. 195.
    D. M. Szebenyi, K. Moffat, J. Biol. Chem. 1986, 261, 8761–8777.Google Scholar
  196. 196.
    K. A. Satyshur, S. T. Rao, D. Pyzalska, W. Drendel, M. Greaser, M. Sundaralingam, J. Biol. Chem. 1988, 263, 1628–1647.Google Scholar
  197. 197.
    O. Herzberg, M. N. G. James, Nature 1985, 313, 653–659.PubMedCrossRefGoogle Scholar
  198. 198.
    Y. S. Babu, J. S. Sack, T. J. Greenhough, C. E. Bugg, A. R. Means, W. J. Cook, Nature 1985, 315, 37–40.PubMedCrossRefGoogle Scholar
  199. 199.
    R. H. Kretsinger, S. E. Rudnick, L. J. Weissman, J. Inorg. Biochem. 1986, 28, 289–302.Google Scholar
  200. 200.
    Y. S. Babu, C. E. Bugg, W. J. Cook, J. Mol. Biol. 1988, 204, 191–204.Google Scholar
  201. 201.
    J. D. Otvos, D. T. Browne, Biochemistry 1980, 19, 4011–4021.PubMedCrossRefGoogle Scholar
  202. 202.
    E. E. Kim, H. W. Wyckoff, Clin. Chim. Acta 1990, 186, 175–187.CrossRefGoogle Scholar
  203. 203.
    E. E. Kim, H. W. Wyckoff, J. Mol. Biol. 1991, 218, 449–464.Google Scholar
  204. 204.
    K. L. Yap, J. Kim, K. Truong, M. Sherman, T. Yuan, M. Ikura, J. Struct. Funct. Genomics 2000, 1, 8–14.Google Scholar
  205. 205.
    D. B. Heidorn, J. Trewhella, Biochemistry 1988, 27, 909–915.PubMedCrossRefGoogle Scholar
  206. 206.
    G. Barbato, M. Ikura, L. E. Kay, R. W. Pastor, A. Bax, Biochemistry 1992, 31, 5269–5278.PubMedCrossRefGoogle Scholar
  207. 207.
    M. Zhang, T. Tanaka, M. Ikura, Nat. Struct. Mol. Biol. 1995, 2, 758–767.CrossRefGoogle Scholar
  208. 208.
    H. Kuboniwa, N. Tjandra, S. Grzesiek, H. Ren, C. B. Klee, A. Bax, Nat. Struct. Mol. Biol. 1995, 2, 768–776.CrossRefGoogle Scholar
  209. 209.
    B. E. Finn, J. Evenäs, T. Drakenberg, J. P. Waltho, E. Thulin, S. Forsén, Nat. Struct. Mol. Biol. 1995, 2, 777–783.CrossRefGoogle Scholar
  210. 210.
    J. Evenäs, A. Malmendal, M. Akke, Structure 2001, 9, 185–195.PubMedCrossRefGoogle Scholar
  211. 211.
    M. Ikura, G. M. Clore, A. M. Gronenborn, G. Zhu, C. B. Klee, A. Bax, Science 1992, 256, 632–638.PubMedCrossRefGoogle Scholar
  212. 212.
    W. E. Meador, A. R. Means, F. A. Quiocho, Science 1992, 257, 1251–1255.PubMedCrossRefGoogle Scholar
  213. 213.
    W. E. Meador, A. R. Means, F. A. Quiocho, Science 1993, 262, 1718–1721.PubMedCrossRefGoogle Scholar
  214. 214.
    N. Matsushima, Y. Izumi, T. Matsuo, H. Yoshino, T. Ueki, Y. Miyake, J. Biochem. 1989, 105, 883–887.PubMedGoogle Scholar
  215. 215.
    J. H. R. Kägi, M. Nordberg, Metallothionein I, Birkhäuser, Boston, 1979.Google Scholar
  216. 216.
    J. H. R. Kägi, Y. Kojima, Metallothionein II: Proceedings of the Second International Meeting on Metallothionein and Other Low Molecular Weight Metal-binding Proteins: Zürich, August 21–24, 1985, Birkhäuser Verlag, Boston, 1987.Google Scholar
  217. 217.
    K. T. Suzuki, N. Imura, M. Kimura, Metallothionein III: Biological Roles and Medical Implications, Birkhäuser Verlag Boston, 1993.Google Scholar
  218. 218.
    C. D. Klaassen, Metallothionein IV, Birkhäuser Verlag Boston, 1999.Google Scholar
  219. 219.
    G. Öz, K. Zangger, I. M. Armitage, Biochemistry 2001, 40, 11433–11441.PubMedCrossRefGoogle Scholar
  220. 220.
    W. Braun, G. Wagner, E. Wörgötter, M. Vašák, J. H. R. Kägi, K. Wüthrich, J. Mol. Biol. 1986, 187, 125–129.Google Scholar
  221. 221.
    P. Schultze, E. Wörgötter, W. Braun, G. Wagner, M. Vašák, J. H. R. Kägi, K. Wüthrich, J. Mol. Biol. 1988, 203, 251–268.Google Scholar
  222. 222.
    B. A. Messerle, A. Schäffer, M. Vašák, J. H. R. Kägi, K. Wüthrich, J. Mol. Biol. 1990, 214, 765–779.Google Scholar
  223. 223.
    A. H. Robbins, D. E. McRee, M. Williamson, S. A. Collett, N. H. Xuong, W. F. Furey, B. C. Wang, C. D. Stout, J. Mol. Biol. 1991, 221, 1269–1293.Google Scholar
  224. 224.
    W. Braun, M. Vašák, A. H. Robbins, C. D. Stout, G. Wagner, J. H. R. Kägi, K. Wüthrich, Proc. Natl. Acad. Sci. USA 1992, 89, 10124–10128.CrossRefGoogle Scholar
  225. 225.
    K. Zangger, I. M. Armitage, J. Inorg. Biochem. 2002, 88, 135–143.Google Scholar
  226. 226.
    K. Wüthrich, NMR of Proteins and Nucleic Acids, Wiley, New York, 1986.Google Scholar
  227. 227.
    J. R. Tolman, H. M. Al-Hashimi, L. E. Kay, J. H. Prestegard, J. Am. Chem. Soc. 2001, 123, 1416–1424.PubMedCrossRefGoogle Scholar
  228. 228.
    P. A. Cobine, R. T. McKay, K. Zangger, C. T. Dameron, I. M. Armitage, Eur. J. Biochem. 2004, 271, 4213–4221.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Ian M. Armitage
    • 1
  • Torbjörn Drakenberg
    • 2
  • Brian Reilly
    • 1
  1. 1.Department of Biochemistry, Molecular Biology, and BiophysicsUniversity of MinnesotaMinneapolisUSA
  2. 2.Department of Biophysical ChemistryLund UniversityLundSweden

Personalised recommendations