Spectroscopic determination of the thermodynamics of cobalt and zinc binding to GATA proteins

Biochemistry

Volumn 43, Issue 26, 2004, Pages 8346-8355

  Ghering, Amy B ^a   Shokes, Jacob E ^b   Scott, Robert A ^b,c   Omichinski, James G ^b,c,d   Godwin, Hilary A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c Université de Montréal ^*  (United States)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; EQUILIBRIUM CONSTANTS; FINGER DOMAINS; X RAY ABSORPTION SPECTROSCOPY;

COBALT COMPOUNDS; DNA; PROTEINS; SPECTROSCOPIC ANALYSIS; TITRATION; X RAY ANALYSIS; ZINC COMPOUNDS;

THERMODYNAMICS;

COBALT; DNA; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR GATA 1; ZINC FINGER PROTEIN; ZINC ION;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; DNA BINDING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; METAL BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; ROENTGEN SPECTROSCOPY; SPECTROSCOPY; STOICHIOMETRY; THERMODYNAMICS; TRANSCRIPTION REGULATION; X RAY ABSORPTION SPECTROSCOPY;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CHICKENS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COBALT; DNA; DNA-BINDING PROTEINS; ERYTHROID-SPECIFIC DNA-BINDING FACTORS; GATA1 TRANSCRIPTION FACTOR; HUMANS; HYDROGEN-ION CONCENTRATION; IONS; KINETICS; METALS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SPECTROPHOTOMETRY; TEMPERATURE; THERMODYNAMICS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; ZINC;

GALLUS GALLUS; VERTEBRATA;

EID: 3142615316     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035673j     Document Type: Article

References (80)

1. Berg, J. M., and Shi, Y. (1996) The galvanization of biology: a growing appreciation for the roles of zinc, Science 271, 1081-1085.
2. Krishna, S. S., Majumdar, I., and Grishin, N. V. (2003) Structural classification of zinc fingers: survey and summary, Nucleic Acids Res. 31, 532-550.
3. Tzfati, Y., Abeliovich, H., Avrahami, D., and Shlomai, J. (1995) Universal minicircle sequence binding protein, a CCHC-type zinc finger protein that binds the universal minicircle sequence of trypanosomatids, J. Biol. Chem. 270, 21339-21345.
4. Michelotti, E. F., Tomonaga, T., Krutzsch, H., and Levens, D. (1995) Cellular nucleic acid binding protein regulates the CT element of the human c-myc protooncogene, J. Biol. Chem. 270, 9494-9499.
5. Chen, X., Chu, M., and Giedroc, D. P. (2000) Spectroscopic characterization of Co(II)-, Ni(II)-, and Cd(II)-substituted wild-type and non-native retroviral-type zinc finger peptides, J. Biol. Inorg. Chem. 5, 93-101.
6. Bochkareva, E., Korolev, S., Lees-Miller, S. P., and Bochkarev, A. (2002) Structure of the RPA trimerization core and its role in the multistep DNA-binding mechanism of RPA, EMBO J. 21, 1855-1863.
7. Cheng, B., Zhu, C. X., Ji, C., Ahumada, A., and Tse-Dinh, Y. C. (2003) Direct interaction between Escherichia coli RNA polymerase and the zinc ribbon domains of DNA topoisomerase I, J. Biol. Chem. 278, 30705-30710.
8. Chen, H.-T., and Hahn, S. (2003) Binding of TFIIB to RNA polymerase II: Mapping the binding site for the TFIIB zinc ribbon domain within the preinitiation complex, Mol. Cell 12.
9. Saurin, A. J., Borden, K. L. B., Boddy, M. N., and Freemont, P. S. (1996) Does this have a familiar RING?, Trends Biochem. Sci. 21, 208-214.
10. Patient, R. K., and McGhee, J. D. (2002) The GATA family (vertebrates and invertebrates), Curr. Opin. Genet. Dev. 12, 416-422.
11. Molkentin, J. D. (2000) The zinc finger-containing transcription factors GATA-4, -5, and -6. Ubiquitously expressed regulators of tissue-specific gene expression, J. Biol. Chem. 275, 38949-38952.
12. Clarke, N. D., and Berg, J. M. (1998) Zinc fingers in Caenorhabditis elegans: finding families and probing pathways, Science 282, 2018-2022.
13. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., et al. (2001) Initial sequencing and analysis of the human genome, Nature 409, 860-921.
14. Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., Sutton, G. G., Smith, H. O., Yandell, M., Evans, C. A., Holt, R. A., et al. (2001) The sequence of the human genome, Science 291, 1304-1351.
15. Magyar, J. S. (2002) Study of Coordination Chemistry, Thermodynamics, and Kinetics of Metal Binding to Zinc-Binding Peptides, Ph.D. Thesis, Northwestern University, Evanston, IL.
16. McLendon, G., Hull, H., Larkin, K., and Chang, W. (1999) Metal binding to the HIV nucleocapsid peptide, J. Biol. Inorg. Chem. 4, 171-174.
17. Berg, J. M., and Merkle, D. L. (1989) On the metal ion specificity of "zinc finger" proteins, J. Am. Chem. Soc. 111, 3759-3761.
18. Krizek, B. A., Amann, B. T., Kilfoil, V. J., Merkle, D. L., and Berg, J. M. (1991) A consensus zinc finger peptide: design, high-affinity metal-binding, a pH-dependent structure, and a His to Cys sequence variant, J. Am. Chem. Soc. 113, 4518-4523.
19. 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.
20. Green, L. M., and Berg, J. M. (1990) Retroviral nucleocapsid protein-metal ion interactions: folding and sequence variants, Proc. Natl. Acad. Sci. U.S.A. 87, 6403-6407.
21. Green, L. M., and Berg, J. M. (1989) A retroviral Cys-Xaa2-Cys-Xaa4-His- Xaa4-Cys peptide binds metal ions: spectroscopic studies and a proposed three-dimensional structure, Proc. Natl. Acad. Sci. U.S.A. 86, 4047-4051.
22. Kowalski, K., Czolij, R., King, G. F., Crossley, M., and Mackay, J. P. (1999) The solution structure of the N-terminal zinc finger of GATA-1 reveals a specific binding face for the transcriptional co-factor FOG, J. Biomol. NMR 13, 249-262.
23. Omichinski, J. G., Clore, G. M., Schaad, O., Felsenfeld, G., Trainor, C., Appella, E., Stahl, S. J., and Gronenbom, A. M. (1993) NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1, Science 261, 438-446.
24. Roehm, P. C., and Berg, J. M. (1997) Sequential metal binding by the RING finger domain of BRCA1, Biochemistry 36, 10240-10245.
25. Lai, Z., Freedman, D. A., Levine, A. J., and McLendon, G. L. (1998) Metal and RNA binding properties of the hdm2 RING finger domain, Biochemistry 37, 17005-17015.
26. Payne, J. C. (2002) Spectroscopic Analysis of the Interactions Between Lead and Structural Zinc-Binding Domains, Ph.D. Thesis, Northwestern University, Evanston, IL.
27. 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.
28. 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.
29. Michel, S. L. J., Guerrerio, A. L., and Berg, J. M. (2003) Selective RNA binding by a single CCCH zinc-binding domain from Nup475, Biochemistry 42, 4626-4630.
30. Worthington, M. T., Amann, B. T., Nathans, D., and Berg, J. M. (1996) Metal binding properties and secondary structure of the zinc-binding domain of Nup475, Proc. Natl. Acad. Sci. U.S.A. 93, 13754-13759.
31. Yang, H. Y., and Evans, T. (1992) Distinct roles for the two cGATA-1 finger domains, Mol. Cell. Biol. 12, 4562-4570.
32. Omichinski, J. G., Trainor, C., Evans, T., Gronenborn, A. M., Clore, G. M., and Felsenfeld, G. (1993) A small single-finger peptide from the erythroid transcription factor GATA-1 binds specifically to DNA as a zinc or iron complex, Proc. Natl. Acad. Sci. U.S.A. 90, 1676-1680.
33. Martin, D. I., and Orkin, S. H. (1990) Transcriptional activation and DNA binding by the erythroid factor GF-1/NF-E1/Eryf 1, Genes Dev. 4, 1886-1898.
34. Tsang, A. P., Visvader, J. E., Turner, C. A., Fujiwara, Y., Yu, C., Weiss, M. J., Crossley, M., and Orkin, S. H. (1997) FOG, a multitype zinc finger protein, acts as a cofactor for transcription factor GATA-1 in erythroid and megakaryocytic differentiation, Cell 90, 109-119.
35. Newton, A., Mackay, J., and Crossley, M. (2001) The N-terminal zinc finger of the erythroid transcription factor GATA-1 binds GATC motifs in DNA, J. Biol. Chem. 276, 35794-35801.
36. Trainor, C. D., Omichinski, J. G., Vandergon, T. L., Gronenbom, A. M., Clore, G. M., and Felsenfeld, G. (1996) A palindromic regulatory site within vertebrate GATA-1 promoters requires both zinc fingers of the GATA-1 DNA-binding domain for high-affinity interaction, Mol. Cell. Biol. 16, 2238-2247.
37. Trainor, C. D., Ghirlando, R., and Simpson, M. A. (2000) GATA zinc finger interactions modulate DNA binding and transactivation, J. Biol. Chem. 275, 28157-28166.
38. Mackay, J. P., Kowalski, K., Fox, A. H., Czolij, R., King, G. F., and Crossley, M. (1998) Involvement of the N-finger in the self-association of GATA-1, J. Biol. Chem. 273, 30560-30567.
39. Kudla, B., Caddick, M., Langdon, T., Martinez-Rossi, N., Bennett, C., Sibley, S., Davies, R., and Arst, H., Jr. (1990) The regulatory gene areA mediating nitrogen metabolite repression in Aspergillus nidulans. Mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger, EMBO J. 9, 1355-1364.
40. Abel, T., Michelson, A. M., and Maniatis, T. (1993) A Drosophila GATA family member that binds to Adh regulatory sequences is expressed in the developing fat body, Development 119, 623-633.
41. Tsai, S. F., Martin, D. I., Zon, L. I., D'Andrea, A. D., Wong, G. G., and Orkin, S. H. (1989) Cloning of cDNA for the major DNA-binding protein of the erythroid lineage through expression in mammalian cells, Nature 339, 446-451.
42. Yamamoto, M., Ko, L. J., Leonard, M. W., Beug, H., Orkin, S. H., and Engel, J. D. (1990) Activity and tissue-specific expression of the transcription factor NF-E1 multigene family, Genes Dev. 4, 1650-1662.
43. Laverriere, A. C., MacNeill, C., Mueller, C., Poelmann, R. E., Burch, J. B., and Evans, T. (1994) GATA-4/5/6, a subfamily of three transcription factors transcribed in developing heart and gut, J. Biol. Chem. 269, 23177-23184.
44. Arceci, R. J., King, A. A., Simon, M. C., Orkin, S. H., and Wilson, D. B. (1993) Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart, Mol. Cell. Biol. 13, 2235-2246.
45. Evans, T., and Felsenfeld, G. (1989) The erythroid-specific transcription factor Eryf1: a new finger protein, Cell 58, 877-885.
46. Tsai, F. Y., Keller, G., Kuo, F. C., Weiss, M., Chen, J., Rosenblatt, M., Alt, F. W., and Orkin, S. H. (1994) An early haematopoietic defect in mice lacking the transcription factor GATA-2, Nature 371, 221-226.
47. Labastie, M. C., Catala, M., Gregoire, J. M., and Peault, B. (1995) The GATA-3 gene is expressed during human kidney embryogenesis, Kidney Int. 47, 1597-1603.
48. Debacker, C., Catala, M., and Labastie, M. C. (1999) Embryonic expression of the human GATA-3 gene, Mech. Dev. 85, 183-187.
49. Nardelli, J., Thiesson, D., Fujiwara, Y., Tsai, F. Y., and Orkin, S. H. (1999) Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system, Dev. Biol. 210, 305-321.
50. Kelley, C., Blumberg, H., Zon, L. I., and Evans, T. (1993) GATA-4 is a novel transcription factor expressed in endocardium of the developing heart, Development 118, 817-827.
51. Morrisey, E. E., Ip, H. S., Lu, M. M., and Parmacek, M. S. (1996) GATA-6: a zinc finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm, Dev. Biol. 177, 309-322.
52. Morrisey, E. E., Ip, H. S., Tang, Z., Lu, M. M., and Parmacek, M. S. (1997) GATA-5: a transcriptional activator expressed in a novel temporally and spatially restricted pattern during embryonic development, Dev. Biol. 183, 21-36.
53. Suzuki, E., Evans, T., Lowry, J., Truong, L., Bell, D. W., Testa, J. R., and Walsh, K. (1996) The human GATA-6 gene: structure, chromosomal location, and regulation of expression by tissue-specific and mitogen-responsive signals, Genomics 38, 283-290.
54. Pevny, L., Simon, M. C., Robertson, E., Klein, W. H., Tsai, S. F., D'Agati, V., Orkin, S. H., and Costantini, F. (1991) Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1, Nature 349, 257-260.
55. Pandolfi, P. P., Roth, M. E., Karis, A., Leonard, M. W., Dzierzak, E., Grosveld, F. G., Engel, J. D., and Lindenbaum, M. H. (1995) Targeted disruption of the GATA-3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis, Nat. Genet. 11, 40-44.
56. Molkentin, J. D., Lin, Q., Duncan, S. A., and Olson, E. N. (1997) Requirement of the transcription factor GATA-4 for heart tube formation and ventral morphogenesis, Genes Dev. 11, 1061-1072.
57. Kuo, C. T., Morrisey, E. E., Anandappa, R., Sigrist, K., Lu, M. M., Parmacek, M. S., Soudais, C., and Leiden, J. M. (1997) GATA-4 transcription factor is required for ventral morphogenesis and heart tube formation, Genes Dev. 11, 1048-1060.
58. Koutsourakis, M., Langeveld, A., Patient, R., Beddington, R., and Grosveld, F. (1999) The transcription factor GATA-6 is essential for early extraembryonic development, Development 126, 723-732.
59. Ghirlando, R., and Trainor, C. D. (2000) GATA-1 bends DNA in a site-independent fashion, J. Biol. Chem. 275, 28152-28156.
60. McBride, K., and Nemer, M. (2001) Regulation of the ANF and BNP promoters by GATA factors: lessons learned for cardiac transcription, Can. J. Physiol. Pharmacol. 79, 673-681.
61. Blobel, G. A., Simon, M. C., and Orkin, S. H. (1995) Rescue of GATA-1-deficient embryonic stem cells by heterologous GATA-binding proteins, Mol. Cell Biol. 15, 626-633.
62. Ko, L. J., and Engel, J. D. (1993) DNA-binding specificities of the GATA transcription factor family, Mol. Cell. Biol. 13, 4011-4022.
63. Vallee, B. L., and Holmquist, B. (1980) in Methodsfor Determining Metal Ion Environments in Proteins: Structure and Function of Metalloproteins (Damall, D. W., and Wilkins, R. G., Eds.), Elsevier/North-Holland, New York.
64. The sequence for the zinc finger consensus peptide (CP-1) is: PYKCPECGKSFSQKSDLVKHQRTHTG.
65. Riddles, P. W., Blakeley, R. L., and Zerner, B. (1983) Reassessment of Ellman's Reagent, Methods Enzymol. 91, 49-60.
66. Binstead, R., Zuberbuhler, A., and Jung, B., Spectrum Software Associates.
67. Scheller, K. H., Abel, T. H. J., Polanyi, P. E., Wenk, P. K., Fischer, B. E., and Sigel, H. (1980) Metal ion/buffer interactions. Stability of binary and ternary complexes containing 2-[Bis(2-hydroxy-ethyl)amino]-2(hydroxymethyl)-1, 3-propanediol (BisTris) and Adenosine 5′-Triphosphate (ATP), Eur. J. Biochem. 107, 455-466.
68. Scott, R. A. (2000) in Physical Methods in Bioinorganic Chemistry Spectroscopy and Magnetism (Que, L., Ed.) pp 465-503, University Science Books, Sausalito, CA.
69. Brown, I. D., and Altermatt, D. (1985) Bond-valence parameters obtained from a systematic analysis of the inorganic crystal-structure database, Acta Crystallogr., Sect. B 41, 244-247.
70. Brese, N. E., and Okeeffe, M. (1991) Bond-valence parameters for solids, Acta Crystallogr., Sect. B 47, 192-197.
71. Thorp, H. H. (1992) Bond valence sum analysis of metal-ligand bond lengths in metalloenzymes and model complexes, Inorg. Chem. 31, 1585-1588.
72. Liu, W. T., and Thorp, H. H. (1993) Bond valence sum analysis of metal-ligand bond lengths in metalloenzymes and model complexes. 2. Refined distances and other enzymes, Inorg. Chem. 32, 4102-4105.
73. Thorp, H. H. (1998) Bond valence sum analysis of metalloenzymes. 3. Predicting bond lengths in adjacent redox states using inner-sphere reorganizational energies, Inorg. Chem. 37, 5690-5692.
74. Clark-Baldwin, K., Tierney, D. L., Govindaswamy, N., Gruff, E. S., Kim, C., Berg; J., Koch, S. A., and Penner-Hahn, J. E. (1998) The limitations of X-ray absorption spectroscopy for determining the structure of zinc sites in proteins. When is a tetrathiolate not a tetrathiolate?, J. Am. Chem. Soc. 120, 8401-8409.
75. Colangelo, C. M., Lewis, L. M., Cosper, N. J., and Scott, R. A. (2000) Structural evidence for a common zinc binding domain in archaeal and eukaryal transcription factor IIB proteins, J. Biol. Inorg. Chem. 5, 276-283.
76. 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.
77. Basolo, F., and Johnson, R. C. (1964) Coordination Chemistry, W. A. Benjamin, New York.
78. Martell, A. E., and Hancock, R. D. (1996) Metal Complexes in Aqueous Solutions, Plenum Publishing, New York.
79. Claudio, E. S., Magyar, J. S., and Godwin, H. A. (2003) Fundamental coordination chemistry, environmental chemistry, and biochemistry of lead(II), Prog. Inorg. Chem. 51, 1-144.
80. Pearson, W. R., Wood, T., Zhang, Z., and Miller, W. (1997) Comparison of DNA sequences with protein sequences, Genomics 46, 24-36.