Why zinc fingers prefer zinc: Ligand-field symmetry and the hidden thermodynamics of metal ion selectivity

Biochemistry

Volumn 43, Issue 44, 2004, Pages 13910-13925

  Lachenmann, Marcel J ^a,b   Ladbury, John E ^a,c   Dong, Jian ^a   Huang, Kun ^a   Carey, Paul ^a   Weiss, Michael A ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; DISEASE CONTROL; ENTHALPY; ENTROPY; HEALTH CARE; IONIZATION; METAL ANALYSIS; OPTIMIZATION; RAMAN SCATTERING; THERMODYNAMICS; TUMORS;

BINDING SITES; METAL ION SELECTIVITY; TUMOR SUPPRESSORS; ZINC FINGERS;

ZINC COMPOUNDS;

COBALT; METAL ION; TUMOR SUPPRESSOR PROTEIN; ZINC; ZINC FINGER PROTEIN;

ARTICLE; ENTHALPY; HUMAN; HYDRATION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; RAMAN SPECTROMETRY; THERMODYNAMICS; TOPOGRAPHY;

AMINO ACID SEQUENCE; BINDING SITES; CALORIMETRY; CATIONS, DIVALENT; COBALT; CONSENSUS SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HUMANS; LIGANDS; METALLOPROTEINS; MODELS, CHEMICAL; MODELS, MOLECULAR; MODELS, STATISTICAL; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN FOLDING; SPECTRUM ANALYSIS, RAMAN; THERMODYNAMICS; WT1 PROTEINS; ZINC; ZINC FINGERS;

EUKARYOTA;

EID: 8344241300     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0491999     Document Type: Article

References (98)

1. Maret, W., and Vallee, B. L. (1993) Cobalt as probe and label of proteins, Methods Enzymol. 226, 52-71.
2. Klug, A., and Rhodes, D. (1987) Zinc fingers a novel protein motif for nucleic acid recognition, Trends Biochem. Sci. 12, 464-469.
3. Pavletich, N. P., and Pabo, C. O. (1991) Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 Å, Science 252, 809-817.
4. Luisi, B. F., Xu, W., Otwinowski, Z., Freedman, L. P., Yamamoto, K. R., and Sigler, P. B. (1991) Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA, Nature 352, 497-505.
5. Berg, J. M., and Shi, Y. (1996) The galvanization of biology: a growing appreciation of the role of zinc, Science 271, 1081-1085.
6. Frankel, A. D., Berg, J. M., and Pabo, C. O. (1987) Metal-dependent folding of a single zinc finger from transcription factor IIIA, Proc. Natl. Acad. Sci. U.S.A. 84, 4841-4845.
7. Parraga, G., Horvath, S. J., Eisen, A., Taylor, W. E., Hood, L., Young, E. T., and Klevit, R. E. (1988) Zinc-dependent structure of a single-finger domain of yeast ADR1, Science 241, 1489-1492.
8. Lee, M. S., Gippert, G. P., Soman, K. V., Case, D. A., and Wright, P. E. (1989) Three-dimensional solution structure of a single zinc finger DNA-binding domain, Science 245, 635-637.
9. Berg, J. M., and Merkle, D. L. (1989) On the metal ion specificity of "Zn finger" proteins, J. Am. Chem. Soc. 111, 3779-3781.
10. Fraústro da Silva, J. J. R., and Williams, R. J. P. (2001) The biological chemistry of the elements. The inorganic chemistry of life, 2nd ed., Oxford University Press, Oxford.
11. Lippard, S. J., and Berg, J. M. (1994) Principles of Bioinorganic Chemistry, University Science Books, Mill Valley, CA.
12. Call, K. M., Glaser, T., Ito, C. Y., Buckler, A. J., Pelletier, J., Haber, D. A., Rose, E. A., Kral, A., Yeger, H., Lewis, W. H., Jones, C., and Houseman, D. E. (1990) Isolation and characterization of a zinc finger polypeptide gene at the human chromsome 11 Wilms' tumor locus, Cell 60, 509-520.
13. Bruening, W., Bardeesy, N., Silverman, B. L., Cohn, R. A., Machin, G. A., Aronson, A. J., Houseman, D., and Pelletier, J. (1992) Germline intronic and exonic mutations in the Wilms' tumour gene (WT1) affecting urogenital development, Nat. Genet. 1, 144-148.
14. Blasie, C. A., and Berg, J. M. (2002) Structure-based thermodynamic analysis of a coupled metal binding-protein folding reaction involving a zinc finger peptide, Biochemistry 41, 15068-15073.
15. Danil de Namor, A. F. (1988) Linear correlation between entropies of complexation of cryptand 222 with metal ions in non-aqueous solvents and entropies of solvation of these ions in these solvents, J. Chem. Soc., Faraday Trans. 1 84, 2441-2444.
16. DiTusa, C. A., McCall, K. A., Christensen, T., Mahapatro, M., Fierke, C. A., and Toone, E. J. (2001) Thermodynamics of metal ion binding. 2. Metal ion binding by carbonic anhydrase variants, Biochemistry 40, 5345-5351.
17. DiTusa, C. A., Christensen, T., McCall, K. A., Fierke, C. A., and Toone, E. J. (2001) Thermodynamics of metal ion binding. 1. Metal ion binding by wild-type carbonic anhydrase, Biochemistry 40, 5338-5344.
18. Christensen, T., Gooden, D. M., Kung, J. E., and Toone, E. J. (2003) Additivity and the physical basis of multivalency effects: a thermodynamic investigation of the calcium EDTA interaction, J. Am. Chem. Soc. 125, 7357-7366.
19. Sharp, K. (2001) Entropy-enthalpy compensation: fact or artifact? Protein Sci. 10, 661-667.
20. Liu, L., and Guo, Q. X. (2001) Isokinetic relationship, isoequilibrium relationship, and enthalpy-entropy compensation, Chem. Rev. 101, 673-695.
21. Dunitz, J. D. (1995) Win some, lose some: enthalpy-entropy compensation in weak intermolecular interactions, Chem. Biol. 2, 709-712.
22. Searle, M. S., Westwell, M. S., and Williams, D. H. (1995) Application of a generalised enthalpy-entropy relationship to binding co-operativity and weak associations in solution, J. Chem. Soc., Perkin Trans. 2, 141-151.
23. Lumry, R., and Rajender, S. (1970) Enthalpy-entropy compensation phenomena in water solutions of proteins and small molecules: a ubiquitous property of water, Biopolymers 9, 1125-1227.
24. Grunwald, E., and Steel, C. (1995) Solvent reorganization and thermodynamic enthalpy-entropy compensation, J. Am. Chem. Soc. 117, 5687-5692.
25. Lachenmann, M. J., Ladbury, J. E., Phillips, N. B., Narayana, N., Qian, X., and Weiss, M. A. (2002) The hidden thermodynamics of a zinc finger, J. Mol. Biol. 316, 969-989.
26. Lachenmann, M. J., Ladbury, J. E., Qian, X., Huang, K., Singh, R., and Weiss, M. A. (2004) The hidden thermodynamics of a zinc finger probed by non-standard repair of a protein crevice, Protein Sci. (in press).
27. Lindskog, S., and Nyman, P. O. (1964) Metal-binding properties of human erythrocyte carbonic anhydrase, Biochim. Biophys. Acta 85, 462-474.
28. Discenza, M. T., and Pelletier, J. (2004) Insights into the physiological role of WT1 from studies of genetically modified mice, Physiol. Genomics 16, 287-300.
29. 2O and its applications to proteins, J. Magn. Reson. 81, 212-216.
30. Dong, J., Wan, Z., Popov, M., Carey, P. R., and Weiss, M. A. (2003) Insulin assembly damps conformational fluctuations: Raman analysis of amide I line widths in native states and fibrils, J. Mol. Biol. 330, 431-442.
31. Irving, H., and Willimas, R. J. P. (1953) The stability of transition-metal complexes, J. Chem. Soc. 3192-3210.
32. Onuchic, J. N., Luthey-Schulten, Z., and Wolynes, P. G. (1997) Theory of protein folding: the energy landscape perspective, Annu. Rev. Phys. Chem. 48, 545-600.
33. Pande, V. S., Grosberg, A., Tanaka, T., and Rokhsar, D. S. (1998) Pathways for protein folding: is a new view needed? Curr. Opin. Struct. Biol. 8, 68-79.
34. Lazaridis, T., and Karplus, M. (2003) Thermodynamics of protein folding: a microscopic view, Biophys. Chem. 100, 367-395.
35. Merrifield, B. (1986) Solid phase synthesis, Science 232, 341-347.
36. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter, Anal. Biochem. 179, 131-137.
37. Ladbury, J. E., and Chowdhry, B. Z. (1996) Sensing the heat: the application of isothermal titration calorimetry to thermodynamic studies of biomolecular interactions, Chem. Biol. 3, 791-801.
38. Dong, J., Dinankarpandian, D., and Carey, P. R. (1998) Extending the Raman analysis of biological samples to the 100 micromolar concentration cange, Appl. Spectrosc. 52, 1117-1122.
39. Kochoyan, M., Havel, T. F., Nguyen, D. T., Dahl, C. E., Keutmann, H. T., and Weiss, M. A. (1991) Alternating zinc fingers in the human male associated protein ZFY: 2D NMR structure of an even finger and implications for "jumping-linker" DNA recognition, Biochemistry 30, 3371-3386.
40. Smallcombe, S. H. (1993) Solvent suppression with symmetrically-shifted pulses, J. Am. Chem. Soc. 115, 4776-4785.
41. Laskowski, R. A. (1995) SURFNET: a program for visualizing molecular surfaces, cavities and intermolecular interactions, J. Mol. Graphics 13, 323-330.
42. Lee, B., and Richards, F. M. (1971) The interpretation of protein structure: estimation of static accessibility, J. Mol. Biol. 55, 379-400.
43. Lee, J. D. (1991) Concise Inorganic Chemistry, 4th ed., Chapman & Hall, London.
44. Schubert, J., Lind, E. L., Westfall, W. M., Pfleger, R., and Li, N. C. (1958) Ion-exchange and solvent-extraction studies on Co(II) and Zn(II) complexes of soem organic acids, J. Am. Chem. Soc. 80, 4799-4802.
45. Li, N. C., and Manning, R. A. (1955) Some metal complexes of sulfur-containing amino acids, J. Am. Chem. Soc. 77, 5225-5227.
46. Martell, A. E. (1964) Stability Constants of Metal-Ion Complexes, The Chemical Society, London.
47. Silber, H. B., and Murguia, M. A. (1985) Spectrophotometric investigations of the ocathedral-tetrahedral equilibria in cobalt-(II)- thiocynate systems in aqueous methanol, Inorg. Chem. 24, 3794-3802.
48. Laity, J. H., Dyson, H. J., and Wright, P. E. (2000) Molecular basis for modulation of biological function by alternate splicing of the Wilms' tumor suppressor protein, Proc. Natl. Acad. Sci. U.S.A. 97, 11932-11935.
49. Harper, L. V., Amann, B. T., Vinson, V. K., and Berg, J. M. (1993) NMR studies of a cobalt-substituted zinc finger peptide, J. Am. Chem. Soc. 115, 2577-2580.
50. Qian, X., and Weiss, M. A. (1992) Two-dimensional NMR studies of the zinc finger motif: solution structures and dynamics of mutant ZFY domains containing aromatic substitutions in the hydrophobic core, Biochemistry 31, 7463-7476.
51. Narayan, V. A., Kriwacki, R. W., and Caradonna, J. P. (1997) Structures of zinc finger domains from transcription factor Sp1. Insights into sequence-specific protein-DNA recognition, J. Biol. Chem. 272, 7801-7809.
52. Miura, T., Satoh, T., and Takeuchi, H. (1998) Role of metal-ligand coordination in the folding pathway of zinc finger peptides, Biochim. Biophys. Acta 1384, 171-179.
53. Pavletich, N. P., and Pabo, C. O. (1993) Crystal structure of a five-finger GLI-DNA complex: new perspectives on zinc fingers, Science 261, 1701-1707.
54. Eriksson, A. E., Jones, T. A., and Liljas, A. (1988) Refined structure of human carbonic anhydrase II at 2.0 Å resolution, Proteins: Struct., Funct., Genet. 4, 274-282.
55. Gomez, J., and Freire, E. (1995) Thermodynamic mapping of the inhibitor site of the aspartic protease endothiapepsin, J. Mol. Biol. 252, 337-350.
56. Schwarzenbach, G. (1952) Der Chelateffekt, Helv. Chim. Acta 35, 2344-2359.
57. Williams, R. J. P. (1954) The stability of complex ions with special reference to hydration, J. Phys. Chem. 58, 121-126.
58. Hanas, J. S., Hazuda, D. J., Bogenhagen, D. F., Wu, F. Y., and Wu, C. W. (1983) Xenopus transcription factor A requires zinc for binding to the 5 S RNA gene, J. Biol. Chem. 258, 14120-14125.
59. Berg, J. M. (1988) Proposed structure for the zinc-binding domains from transcription factor TFIIIA and related proteins, Proc. Natl. Acad. Sci. U.S.A. 85, 99-102.
60. Rees, D. C. (2002) Great metalloclusters in enzymology, Annu. Reu. Biochem. 71, 221-246.
61. Berkner, I. V., and Marshall, L. C. (1965) On the origin and rise of oxygen concentration in the earth's atmosphere, J. Atmos.. Sci. 22, 225-261.
62. Canfield, D. E., Habicht, K. S., and Thamdrup, B. (2000) The Archean sulfur cycle and the early history of atmospheric oxygen, Science 288, 658-661.
63. 12: reminiscences and after-thoughts, Ciba Found. Symp. 180, 309-329.
64. Anbar, A. D., and Knoll, A. H. (2002) Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297, 1137-1142.
65. Liljas, A., Kannan, K. K., Bergsten, P.-C., Waara, I., Fridborg, K., Strandberg, B., Carlbom, U., Jarup, L., Lovgren, S., and Petef, M. (1972) Crystal structure of human carbonic anhydrase C, Nat. New Biol. 235, 131-137.
66. Forsman, C., Behravan, G., Osterman, A., and Jonsson, B. H. (1988) Production of active human carbonic anhydrase II in E. coli, Acta Chem. Scand., B 42, 314-318.
67. Hakansson, K., Carlsson, M., Svensson, L. A., and Liljas, A. (1992) Structure of native and apo carbonic anhydrase II and structure of some of its anion-ligand complexes, J. Mol. Biol. 227, 1192-1204.
68. Hakansson, K., and Wehnert, A. (1992) Structure of cobalt carbonic anhydrase complexed with bicarbonate, J. Mol. Biol. 228, 1212-1218.
69. Blundell, T. L., Cutfield, J. F., Cutfield, S. M., Dodson, E. J., Dodson, G. G., Hodgkin, D. C., Mercola, D. A., and Vijayan, M. (1971) Atomic positions in rhombohedral 2-zinc insulin crystals, Nature 231, 506-511.
70. 3f human insulin: temperature or pressure induced? Acta Crystallogr. D57, 1091-1100.
71. McGraw, S. E., and Lindenbaum, S. (1990) The use of micro-calorimetry to measure thermodynamic parameters of the binding of ligands to insulin, Pharm. Res. 7, 606-611.
72. 2+ binding to proteins, J. Biol. Chem. 267, 24297-24301.
73. Searle, M. S., and Williams, D. H. (1992) The cost of conformational order: entropy changes in molecular associations, J. Am. Chem. Soc. 114, 10690-10697.
74. Yang, D., Mok, Y. K., Forman-Kay, J. D., Farrow, N. A., and Kay, L. E. (1997) Contributions to protein entropy and heat capacity from bond vector motions measured by NMR spin relaxation, J. Mol. Biol. 272, 790-804.
75. Gallicchio, E., Kubo, M. M., and Levy, R. M. (1998) Entropy-enthalpy compensation in solvation and ligand binding revisited, J. Am. Chem. Soc. 120, 4526-4527.
76. Yu, H.-A., and Karplus, M. (1988) A thermodynamic analysis of solvation, J. Chem. Phys. 89, 2366-2379.
77. Chervenak, M., and Toone, E. J. (1994) A direct measure of the contribution of solvent reorganization to the enthalpy of ligand binding, J. Am. Chem. Soc. 116, 10534-10539.
78. Eftink, M. R., Anusiem, A. C., and Biltonen, R. T. (1983) Enthalpy-entropy compensation and heat capacity changes for protein-ligand interactions: general thermodynamic models and data for the binding of nucleotides to ribonuclease A, Biochemistry 22, 3884-3896.
79. Qian, H., and Hopfield, J. J. (1996) Entropy-enthalpy compensation: perturbation and relaxation in thermodynamic systems, J. Chem. Phys. 105, 9292-9298.
80. Qian, H. (1998) Entropy-enthalpy compensation: conformational fluctuation and induced-fit, J. Chem. Phys. 109, 10015-10017.
81. Marcus, Y. (1994) A simple empirical model describing the thermodynamics of hydration of ions of widely varying charges, sizes, and shapes, Biophys. Chem. 51, 111-127.
82. Krizek, B. A., Merkle, D. L., and Berg, J. M. (1993) Ligand variation and metal-ion binding specificity in zinc finger peptides, Inorg. Chem. 32, 937-940.
83. 4-Cys peptide binds metal ions: spectroscopic studies and a proposed three-dimensional structure, Proc. Natl. Acad. Sci. U.S.A. 86, 4047-4051.
84. Magyar, J. S., and Godwin, H. A. (2003) Spectropotentiometric analysis of metal binding to structural zinc-binding sites: accounting quantitatively for pH and metal ion buffering effects, Anal. Biochem. 320, 39-54.
85. Payne, J. C., Rous, B. W., Tenderholt, A. L., and Godwin, H. A. (2003) Spectroscopic Determination of the Binding Affinity of Zinc to the DNA-Binding Domains of Nuclear Hormone Receptors, Biochemistry 42, 14214-14224.
86. McLendon, G., Hull, H., Larkin, K., and Chang, W. (1999) Metal binding to the HIV nucleocapsid peptide, J. Biol. Inorg. Chem. 4, 171-174.
87. Berkovits, H. J., and Berg, J. M. (1999) Metal and DNA binding properties of a two-domain fragment of neural zinc finger factor 1, a CCHC-type zinc binding protein. Biochemistry 38, 16826-16830.
88. Maiti, N. C., Apetri, M. M., Zagorski, M. G., Carey, P. R., and Anderson, V. E. (2004) Spectroscopic characterization of secondary structure in natively unfolded proteins: alpha-synuclein, J. Am. Chem. Soc. 126, 2399-2408.
89. Sane, S. U., Cramer, S. M., and Przybycien, T. M. (1999) A holistic approach to protein secondary structure characterization using amide I band Raman spectroscopy, Anal. Biochem. 269, 255-272.
90. Peticolas, W. L. (1995) Raman spectroscopy of DNA and proteins, Methods Enzymol. 246, 389-416.
91. Berjot, M., Marx, J., and Alix, A. J. P. (1987) Determination of the secondary structure of proteins from the Raman amide I band: the reference intensity profile method, J. Raman Spectrosc. 18, 289-300.
92. Krizek, B. A., Zawadzke, L. E., and Berg, J. M. (1993) Independence of metal binding between tandme Cys2His2 zinc finger domains, Protein Sci. 2, 1313-1319.
93. Eriksson, A. E., Baase, W. A., and Matthews, B. (1993) Similar hydrophobic replacements of Leu99 amd Phe153 within the core of T4 lysozyme have different structural and thermodynamic consequences, J. Mol. Biol. 229, 747-769.
94. Gao, J., Kuczera, K., Tidor, B., and Karplus, M. (1989) Hidden thermodynamics of mutant proteins: a molecular dynamics analysis, Science 244, 1069-1072.
95. 2 centre in transcription factor IIIA (cys=cysteine; his=histidine), J. Chem. Soc., Chem. Commun. 966-967.
96. Tripp, B. C., Bell, C. B. r., Cruz, F., Krebs, C., and Ferry, J. G. (2004) A role for iron in an ancient carbonic anhydrase, J. Biol. Chem. 279, 6683-6687.
97. Atkins, P. W. (1990) Physical Chemistry, 4th ed., Oxford University Press, Oxford.
98. Derewenda, U., Derewenda, Z., Dodson, E. J., Dodson, G. G., Reynolds, C. D., Smith, G. D., Sparks, C., and Swenson, D. (1989) Phenol stabilizes more helix in a new symmetrical zinc insulin hexamer, Nature 338, 594-596.