The thermodynamics of protein interactions with essential first row transition metals

Biochimica et Biophysica Acta - General Subjects

Volumn 1860, Issue 5, 2016, Pages 879-891

  Bou Abdallah, Fadi ^a   Giffune, Thomas R ^a  

^a STATE UNIVERSITY OF NEW YORK AT POTSDAM   (United States)

Author keywords

Binding; Enthalpy entropy; Isothermal titration calorimetry (ITC); Proteins; Thermodynamics; Transitions metal ions

Indexed keywords

CALGRANULIN; CARBONATE DEHYDRATASE; CERULOPLASMIN; COBALT; COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C OXIDASE; DIOXYGENASE; DNA; FERRITIN; HYDROLASE; IRON; LIGASE; LYASE; MANGANESE; METAL ION; METALLOCHAPERONE; METALLOCHAPERONE ATOX1; NICKEL; OXIDOREDUCTASE; PROTEIN; RNA; SILVER; TRANSFERASE; TRANSFERRIN; TRANSITION ELEMENT; UNCLASSIFIED DRUG; VANADIUM; ZINC; ZINC FINGER PROTEIN; ADENOSINE TRIPHOSPHATASE; ATOX1 PROTEIN, HUMAN; CATION TRANSPORT PROTEIN; METAL; PROTEIN BINDING; SOD1 PROTEIN, HUMAN; SUPEROXIDE DISMUTASE; WILSON DISEASE PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ARCHAEON; ARTICLE; BACTERIUM; BINDING AFFINITY; BIOCHEMICAL ANALYSIS; CHEMICAL ANALYSIS; CHEMICAL BINDING; DIATOM; DISULFIDE BOND; ENTHALPY; ENTROPY; EQUILIBRIUM CONSTANT; HUMAN; IRON STORAGE; ISOTHERMAL TITRATION CALORIMETRY; METAL BINDING; MOLECULAR INTERACTION; NONHUMAN; PLANT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; THERMODYNAMICS; ANIMAL; BINDING SITE; BOVINE; CALORIMETRY; CHEMISTRY; KINETICS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BINDING SITES; CALORIMETRY; CARBONIC ANHYDRASES; CATION TRANSPORT PROTEINS; CATTLE; FERRITINS; HUMANS; KINETICS; METALLOCHAPERONES; METALS; PROTEIN BINDING; SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE-1; THERMODYNAMICS; TRANSFERRIN; TRANSITION ELEMENTS;

EID: 84960799950     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2015.11.005     Document Type: Review

References (81)

1. I. Bertini, H.B. Gary, S.J. Lippard, and J.S. Valentine Bioinorganic Chem 1994 University Science Books Mill Valley, CA
2. H. Gray Biological inorganic chemistry at the beginning of the 21st century Proc. Natl. Acad. Sci. U. S. A. 2003 3563 3568
3. S.J. Lippard, and J.M. Berg Principles of Bioinorganic Chemistry 1994 University Science Books Mill Valley, CA
4. H. Irving, and R. Williams Order of stability of metal complexes Nature 1948 746 747
5. K. McCall, and C. Fierke J. Biochem. 43 2004 3979 3986
6. M. Cláudio, A. Gomes, and P. Wittung-Stafshede C.M. Gomes, P. Wittung-Stafshede, Metal ions, protein folding, and conformational states, an introduction, chapter 1 in "Protein folding and metal ions: mechanisms, biology and disease 1st Edition 2011 CRC Press, Taylor and Francis Group
7. R.R. Crichton Biological Inorganic Chemistry, a new Introduction to Molecular Structure and Function 2nd Ed 2012 Elsevier
8. W. Kaim, B. Schwederski, and A. Klein Bioinorganic Chemistry, Inorganic Elements in the Chemistry of Life: An Introduction and Guide, 2nd Edition, John Wiley and Sons 2013
9. J. Emsley Nature's Building Blocks: An A-Z Guide to the Elements 2001 Oxford University Press USA.
10. W. Maret, and Y. Li Coordination dynamics of zinc in proteins Chem. Rev. 109 2009 4682 4707
11. W. Maret New perspectives of zinc coordination environments in proteins J. Inorg. Biochem. 111 2012 110 116
12. J. Font, and J.P. Mackay Beyond DNA: zinc finger domains as RNA-binding modules, engineered zinc finger proteins Meth Mol Biol 649 2010 479 491
13. A. Klug The discovery of zinc fingers and their development for practical applications in gene regulation and genome manipulation Q. Rev. Biophys. 2010 1 21
14. J. Burdach, M. O'Connell, J. Mackay, and M. Crossley Two-timing zinc finger transcription factors liaising with RNA Trends Biochem. Sci. 5 2012 199 205
15. J. Berg Proposed structure for the zinc-binding domains from transcription factor IIIA and related proteins Proc. Natl. Acad. Sci. U. S. A. 85 1988 99 102
16. E.H. Cox, and G.L. McLendon Zinc-dependent protein folding Curr. Opin. Chem. Biol. 4 2000 162 165
17. K.S. Smith, C. Jakubzick, T.S. Whittam, and J.G. Ferry Carbonic anhydrase is an ancient enzyme widespread in prokaryotes Proc. Natl. Acad. Sci. U. S. A. 96 1999 15184 15189
18. V.M. Krishnamurthy, G.K. Kaufman, A.R. Urbach, I. Gitlin, K.L. Gudiksen, D.B. Weibel, and G.M. Whitesides Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein-ligand binding Chem. Rev. 108 2008 946 1051
19. J. Miller, A.D. McLachlan, and A. Klug Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes EMBO J. 4 1985 1609 1614
20. J.M. Berg, and H.A. Godwin Lessons from zinc-binding peptides Annu. Rev. Biophys. Biomol. Struct. 26 1997 357 371
21. 4 transcription factor site J. Am. Chem. Soc. 134 2012 10405 10418
22. V. Alterio, A. Di Fiore, K. D'Ambrosio, C.T. Supuran, and G. De Simone Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem. Rev. 112 2012 4421 4468
23. J.A. Hunt, and C.A. Fierke Selection of carbonic anhydrase variants displayed on phage. Aromatic residues in zinc binding site enhance metal affinity and equilibration kinetics J. Biol. Chem. 272 1997 20364 20372
24. J.A. Hunt, M. Ahmed, and C.A. Fierke Metal binding specificity in carbonic anhydrase is influenced by conserved hydrophobic core residues Biochemistry 38 1999 9054 9062
25. H. Song, D.L. Wilson, E.R. Farquhar, E.A. Lewis, and J.P. Emerson Revisiting zinc coordination in human carbonic anhydrase II Inorg. Chem. 51 2012 11098 11105
26. R. Holm, P. Kennepohl, and E. Solomon Structural and functional aspects of metal sites in biology Chem. Rev. 96 1996 2239 2314
27. T.J. Lyons, A. Nersissian, H. Huang, H. Yeom, C.R. Nishida, J.A. Graden, E.B. Gralla, and J.S. Valentine The metal binding properties of the zinc site of yeast copper-zinc superoxide dismutase: implications for amyotrophic lateral sclerosis J. Biol. Inorg. Chem. 5 2000 189 203
28. P.L. Bounds, B. Sutter, and W.H. Koppenol Studies of metal-binding properties of Cu,Zn superoxide dismutase by isothermal titration calorimetry Meth Enzym, Superoxide Dismutase 349 2002 115 123
29. J.P. Crow, J. Sampson, Y.X. Zhuang, J.A. Thompson, and J.S. Beckman Decreased zinc affinity of amyotrophic lateral sclerosis-associated superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite Neurochem 69 1997 1936 1944
30. J.S. Valentine, and M.W. Pantoliano Protein-metal ion interactions in cuprozinc protein (superoxide dismutase) T.C. Spiro, Copper Proteins Wiley Interscience 1981 John Wiley and Sons, Inc New York 291 358
31. J. Hirose, M. Yamada, C. Hayakawa, H. Nagao, M. Noji, and Y. Kidani Selective binding behavior of zinc(II) and copper(II) ions to their native sites of apo-bovine superoxide dismutase Biochem. Int. 8 1984 401 408
32. J.A. Roe, R. Peoples, D.M. Scholler, and J.S. Valentine Silver-binding properties of bovine cuprozinc superoxide dismutase and the overall stability of selected metal-ion derivatives J. Am. Chem. Soc. 112 1990 1538 1545
33. S.Z. Potter, H. Zhu, B.F. Shaw, J.A. Rodriguez, P.A. Doucette, S.H. Sohn, A. Durazo, K.F. Faull, E.B. Gralla, A.M. Nersissian, and J.S. Valentine Binding of a single zinc ion to one subunit of copper-zinc superoxide dismutase apoprotein substantially influences the structure and stability of the entire homodimeric protein J. Am. Chem. Soc. 129 2007 4575 4583
34. J.W. Whittaker Metal uptake by manganese superoxide dismutase Biochim. Biophys. Acta 1804 2010 298 307
35. W.E. Karsten, and P.F. Cook An isothermal titration calorimetry study of the binding of substrates and ligands to the tartrate dehydrogenase from Pseudomonas putida reveals half-of-the-sites reactivity Biochemistry 45 2006 9000 9006
36. T.J. Lyons, A. Nersissian, H. Huang, H. Yeom, C.R. Nishida, J.A. Graden, E.B. Gralla, and J.S. Valentine The metal binding properties of the zinc site of yeast copper-zinc superoxide dismutase: implications for amyotrophic lateral sclerosis J. Biol. Inorg. Chem. 5 2000 189 203
37. A.K. Wernimont, L.A. Yatsunyk, and A.C. Rosenzweig Binding of copper(I) by the Wilson disease protein and its copper chaperone J. Biol. Chem. 279 2004 12269 12276
38. Z. Xiao, J. Brose, S. Schimo, S.M. Ackland, S. LaFontaine, and A.G. Wedd Unification of the copper(I) binding affinities of the metallo-chaperones Atx1, Atox1, and related proteins. Detection probes and affinity standards J.Biol. Chem. 286 2011 11047 11055
39. M.E. Palm-Espling, C.D. Andersson, E. Björn, A. Linusson, and P. Wittung-Stafshede Determinants for simultaneous binding of copper and platinum to human chaperone Atox1: hitchhiking not hijacking PLoS One 8 2013 e70473 10.1371/journal.pone.0070473
40. M.E. Palm-Espling, C. Lundin, E. Björn, P. Naredi, and P. Wittung-Stafshede Interaction between the anticancer drug Cisplatin and the copper chaperone Atox1 in human melanoma cells Protein Pept. Lett. 21 2014 63 68
41. L. Banci, I. Bertini, S. Ciofi-Baffoni, T. Kozyreva, K. Zovo, and P. Palumaa Affinity gradients drive copper to cellular destinations Nature 2010 645 648
42. L.A. Yatsunyk, and A.C. Rosenzweig Cu(I) binding and transfer by the N terminus of the Wilson disease protein J. Biol. Chem. 282 2007 8622 8631
43. C. Abajian, L.A. Yatsunyk, B.E. Ramirez, and A.C. Rosenzweig Yeast Cox17 solution structure and copper(I) binding J. Biol. Chem. 279 2004 53584 53592
44. D.L. Huffman, and T.V. O'Halloran Energetics of copper trafficking between the Atx1 metallochaperone and the intracellular copper transporter, Ccc2 J. Biol. Chem. 275 2000 18611 18614
45. R.R. Crichton Iron Metabolism: From Molecular Mechanisms to Clinical Consequences 3rd Ed. 2009 John Wiley & Sons New York
46. 2 + binding to human serum transferrin J. Inorg. Biochem. 136 2014 24 32
47. F. Bou-Abdallah, and T.R. Terpstra The thermodynamic and binding properties of the transferrins as studied by isothermal titration calorimetry Biochim. Biophys. Acta 1820 2012 318 325
48. F. Bou-Abdallah The iron redox and hydrolysis chemistry of the ferritins Biochim. Biophys. Acta 1800 2010 719 731
49. E.C. Theil Ferritin: The protein nanocage and iron biomineral in health and in disease Inorg. Chem. 52 2013 12223 12233
50. K.H. Ebrahimi, P.L. Hagedoorn, and W.R. Hagen Unity in the biochemistry of the iron-storage proteins ferritin and bacterioferritin Chem. Rev. 115 2015 295 326
51. F. Bou-Abdallah, H. Yang, A. Awomolo, B. Cooper, M.R. Woodhall, S.C. Andrews, and N.D. Chasteen Functionality of the three-site ferroxidase center of Escherichia coli bacterial ferritin (EcFtnA) Biochemistry 53 2014 483 495
52. J.M. Bradley, G.R. Moore, and N.E. Le Brun Mechanisms of iron mineralization in ferritins: one size does not fit all J. Biol. Inorg. Chem. 19 2014 775 785
53. E.C. Theil Ferritin and its role in iron homeostasis, Chap 13 in "Binding, transport and storage of metal ions in biological cells" W. Maret, A. Wedd, The Royal Society of Chemistry 2014 Thomas Graham House, Science Park, Milton Road, Cambridge CB4 OWF UK
54. F. Bou-Abdallah, M.R. Woodhall, A.V. Campoy, S.C. Andrews, and N.D. Chasteen Thermodynamic analysis of ferrous ion binding to Escherichia coli ferritin EcFtnA Biochemistry 44 2005 13837 13846
55. F. Bou-Abdallah, P. Arosio, P. Santambrogio, X. Yang, C. Janus-Chandler, and N.D. Chasteen Ferrous ion binding to recombinant human H-chain ferritin. An isothermal titration calorimetry study Biochemistry 41 2002 11184 11191
56. F. Bou-Abdallah, P. Arosio, S. Levi, C. Janus-Chandler, and D. Chasteen Defining metal ion inhibitor interactions with recombinant human H- and L-chain ferritins and site-directed variants: An isothermal titration calorimetry study J. Biol. Inorg. Chem. 8 2003 489 497
57. K.M. Papp-Wallace, and M.E. Maguire Manganese transport and the role of manganese in virulence Annu. Rev. Microbiol. 60 2006 187 209
58. T.E. Kehl-Fie, S. Chitayat, M.I. Hood, S. Damo, N. Restrepo, C. Garcia, K.A. Munro, W.J. Chazin, and E.P. Skaar Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus Cell Host Microbe 10 2011 158 164
59. J.A. Hayden, M.B. Brophy, L.S. Cunden, and E.M. Nolan High-affinity manganese coordination by human calprotectin is calcium-dependent and requires the histidine-rich site formed at the dimer interface J. Am. Chem. Soc. 135 2013 775 787
60. S.M. Damo, T.E. Kehl-Fie, N. Sugitani, M.E. Holt, S. Rathi, W.J. Murphy, Y. Zhang, C. Betz, L. Hench, G. Fritz, E.P. Skaar, and W.J. Chazin Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens Proc. Natl. Acad. Sci. U. S. A. 110 2013 3841 3846
61. D.M. Gagnon, M.B. Brophy, S.E.J. Bowman, T.A. Stich, C.L. Drennan, R.D. Britt, and E.M. Nolan Manganese binding properties of human calprotectin under conditions of high and low calcium: x-ray crystallographic and advanced electron paramagnetic resonance spectroscopic analysis J. Am. Chem. Soc. 137 2015 3004 3016
62. I.P. Korndörfer, F. Brueckner, and A. Skerra The crystal structure of the human (S100A8/S100A9)2 heterotetramer, calprotectin, illustrates how conformational changes of interacting alpha-helices can determine specific association of two EF hand proteins J. Mol. Biol. 370 2007 887 898
63. Y. Li, and D.B. Zamble Nickel homeostasis and nickel regulation: An overview Chem. Rev. 109 2009 4617 4643
64. 2 + binding to the urease metallochaperone UreE Biochemistry 46 2007 10506 10516
65. D.E. Wilcox Isothermal titration calorimetry of metal ions binding to proteins: An overview of recent studies Inorg. Chim. Acta 361 2008 857 867
66. W.R. Harris, and C.J. Carrano Binding of vanadate to human serum transferrin J. Inorg. Biochem. 22 1984 201 218
67. N.D. Chasteen, J.K. Grady, and C.E. Holloway Characterization of the binding, kinetics, and redox stability of vanadium(IV) and vanadium(V) protein complexes in serum Inorg. Chem. 25 1986 2754 2760
68. T. Kiss, E. Kiss, E. Garribba, and H. Sakurai Speciation of insulin-mimetic VO(IV)-containing drugs in blood serum J. Inorg. Biochem. 80 2000 65 73
69. B.D. Liboiron, K.H. Thompson, G.R. Hanson, E. Lam, N. Aebischer, and C. Orvig New insights into the interactions of serum proteins with bis(maltolato)oxovanadium(IV): transport and biotransformation of insulin-enhancing vanadium pharmaceuticals J. Am. Chem. Soc. 127 2005 5104 5115
70. A. Dörnyei, A. Marcão, J. Pessoa, T. Jakusch, and T. Kiss Interactions of insulin-mimetic vanadium complexes with the cell constituents ATP and glutathione Eur. J. Inorg. Chem. 18 2006 3614 3621
71. T. Kiss, T. Jakusch, D. Hollender, A. Dörnyei, E.A. Enyedy, J.C. Pessoa, H. Sakurai, and A. Sanz-Medel Biospeciation of antidiabetic VO(IV) complexes Coord. Chem. Rev. 252 2008 1153 1162
72. A.K. Bordbar, A.L. Creagh, F. Mohammadi, C.A. Haynes, and C. Orvig Calorimetric studies of the interaction between the insulin-enhancing drug candidate bis(maltolato)oxovanadium(IV) (BMOV) and human serum apo-transferrin J. Inorg. Biochem. 103 2009 643 647
73. Biocalorimetry, Methods 76 (2015), Edited by J.B. Chaires, L.D. Hansen, S. Keller, C.A. Brautigam, H. Zhao and P. Schuck, 1-200
74. SEDPHAT, A platform for global ITC analysis and global multi-method analysis of molecular interactions, H. Zhao, G. Piszczek, and P. Schuck Methods 76 2015 137 148
75. A unified framework based on the binding polynomial for characterizing biological systems by isothermal titration calorimetry, S. Vega, O. Abian, and A. Velazquez-Campoy Methods 76 2015 99 115
76. M.J. Todd, and J. Gomez Enzyme kinetics determined using calorimetry: A general assay for enzyme activity? Anal. Biochem. 296 2001 179 187
77. M. Lucia Bianconi Calorimetry of enzyme-catalyzed reactions Biophys. Chem. 126 2007 59 64
78. S.N. Olsen Applications of isothermal titration calorimetry to measure enzyme kinetics and activity in complex solutions Thermochim. Acta 448 2006 12 18
79. D. Burnouf, E. Ennifar, S. Guedich, B. Puffer, G. Hoffmann, G. Bec, F. Disdier, M. Baltzinger, and P. Dumas KinITC: A new method for obtaining joint thermodynamic and kinetic data by isothermal titration calorimetry J. Am. Chem. Soc. 134 2012 559 565
80. M.K. Transtruma, L.D. Hansen, and C. Quinn Enzyme kinetics determined by single-injection isothermal titration calorimetry Methods 76 2015 194 200
81. M.W. Freyer, and E.A. Lewis Isothermal titration calorimetry: experimental design, data analysis, and probing macromolecule/ligand binding and kinetic interactions Methods Cell Biol. 84 2008 79 113 chap 4