Deducing the energetic cost of protein folding in zinc finger proteins using designed metallopeptides

Journal of the American Chemical Society

Volumn 129, Issue 42, 2007, Pages 12815-12827

  Reddi, Amit R ^a   Guzman, Tabitha R ^a   Breece, Robert M ^b   Tierney, David L ^b   Gibney, Brian R ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOACTIVITY; CALORIMETRY; GENES; PROTONS; THERMODYNAMIC PROPERTIES; TRANSCRIPTION;

HUMAN GENOMES; METALLOPEPTIDES; PEPTIDE SCAFFOLDS; PROTEIN-PROTEIN INTERACTIONS;

PROTEIN FOLDING;

METALLOPROTEIN; TRANSCRIPTION FACTOR; ZINC; ZINC FINGER PROTEIN;

ARTICLE; CALORIMETRY; COMPLEX FORMATION; ENERGY; ENTHALPY; ENTROPY; FLUOROMETRY; METAL BINDING; POTENTIOMETRY; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; THERMODYNAMICS;

AMINO ACID MOTIFS; CALORIMETRY; CYSTEINE; HISTIDINE; HYDROGEN-ION CONCENTRATION; KINETICS; LIGANDS; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PEPTIDES; PROTEIN FOLDING; SPECTROMETRY, FLUORESCENCE; THERMODYNAMICS; ZINC; ZINC FINGERS;

EID: 35548991935     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja073902+     Document Type: Article

References (87)

1. Dyson, H. J.; Wright, P. E. Curr. Opin. Struct. Biol. 2002, 12, 54-60.
2. Wittung-Stafshede, P. Acc. Chem. Res. 2002, 35, 201-208.
3. Wilson, C. J.; Apiyo, D.; Wittung-Stafshede, P. Q. Rev. Biophys. 2005, 3, 1-30.
4. Ghosh, D.; Pecoraro, V. L. Curr. Opin. Chem. Biol. 2005, 9, 97-103.
5. Auld, D. S. BioMetals 2001, 14, 271-313.
6. Cox, E. H.; McLendon, G. L. Curr. Opin. Struct. Biol. 2000, 4, 162-165.
7. Frankel, A. D.; Berg, J. M.; Pabo, C. O. Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 4841-4845.
8. Berg, J. M. Curr. Opin. Struct. Biol. 1993, 3, 11-16.
9. Schmiedeskamp, M.; Klevit, R. E. Curr. Opin. Struct. Biol. 1994, 4, 28-35.
10. Matthews, J. M.; Sunde, M. IUMB Life 2002, 54, 351-355.
11. Low, L. Y.; Hernandez, H.; Robinson, C. V.; O'Brien, R.; Grossmann, J. G.; Ladbury, J. E.; Luisi, B. J. Mol. Biol. 2002, 319, 87-106.
12. Blaise, C. A.; Berg, J. M. Biochemistry 2002, 41, 15068-15073.
13. Simpson, R. J. Y.; Cram, E. D.; Czolij, R.; Matthews, J. M.; Crossley, M.; Mackay, J. P. J. Biol. Chem. 2003, 278, 28011-28018.
14. Okuda, M.; Tanaka, A.; Hanaoka, F.; Ohkuma, Y.; Nishimura, Y. J. Biochem. 2005, 138, 443-449.
15. Payne, J. C.; Rous, B. W.; Tenderholt, A. L.; Godwin, H. A. Biochemistry 2003, 42, 14214-14224.
16. Gockel, P.; Vahrenkamp, H.; Zuberbühler, A. D. Helv. Chim. Acta 1993, 76, 511-520.
17. Vogler, R.; Vahrenkamp, H. Eur. J. Inorg. Chem. 2002, 761-766.
18. Vallee, B. L.; Auld, D. S. Acc. Chem. Res. 1993, 26, 543-551.
19. Regan, L.; Clarke, N. D. Biochemistry 1990, 29, 10878-10883.
20. Krizek, B. A.; Amann, B. T.; Kilfoil, V. J.; Merkle, D. L.; Berg, J. M. J. Am. Chem. Soc. 1991, 113, 4518-4523.
21. Handel, T. M.; Williams, S. A.; DeGrado, W. F. Science 1993, 261, 879-885.
22. Struthers, M. D.; Cheng, R. P.; Imperiali, B. Science 1996, 271, 342-345.
23. Struthers, M. D.; Cheng, R. P.; Imperiali, B. J. Am. Chem. Soc. 1996, 118, 3073-3081.
24. Dahiyat, B. I.; Mayo, S. L. Science 1997, 278, 82-87.
25. Wisz, M. S.; Garrett, C. Z.; Hellinga, H. W. Biochemistry 1998, 37, 8269-8277.
26. Pabo, C. O.; Peisach, E.; Grant, R. A. Annu. Rev. Biochem. 2001, 70, 313-340.
27. Ambroggio, X. I.; Kuhlman, B. J. Am. Chem. Soc. 2006, 128, 1154-1161.
28. Dhanasekaran, M.; Negi, S.; Sugiura, Y. Acc. Chem. Res. 2006, 39, 45-52.
29. Robertson, D. E.; Farid, R. S.; Moser, C. C.; Urbauer, J. L.; Mulholland, S. E.; Pidikiti, R.; Lear, J. D.; Wand, A. J.; DeGrado, W. F.; Dutton, P. L. Nature 1994, 368, 425-432.
30. Petras, A. K.; Reddi, A. R.; Kennedy, M. L.; Hyslop, A. G.; Gibney, B. R. Inorg. Chem. 2006, 45, 9941-9958.
31. Reddi, A. R.; Gibney, B. R. Biochemistry 2007, 46, 3745-3758.
32. Reddi, A. R.; Reedy, C. J.; Mui, S.; Gibney, B. R. Biochemistry 2007, 46, 291-305.
33. Martell, A. E.; Smith, R. M. Critical Stability Constants; Plenum Press: New York, 1974.
34. Harris, H. L.; Hudson, B. S. Biochemistry 1990, 29, 5276-5285.
35. Magyar, J. S.; Godwin, H. A. Anal. Biochem. 2003, 320, 39-54.
36. Wiseman, T.; Williston, S.; Brandts, J. F.; Lin, L. N. Anal. Biochem. 1989, 179, 131-137.
37. Freire, E.; Mayorga, O.; Straume, M. Anal. Biochem. 1990, 62, 950A-959A.
38. Ladbury, J. E.; Chowdhry, B. Z. Chem. Biol. 1996, 3, 791-801.
39. Zhang, Y.; Akilesh, S.; Wilcox, D. E. Inorg. Chem. 2000, 39, 3057-3064.
40. Richens, D. T. The Chemistry of Aqua Ions; John Wiley & Sons: New York, 1997.
41. Zhu, M.; Pan, G. J. Phys. Chem. A 2005, 109, 7648-7652.
42. Fukada, H.; Takahashi, K. Proteins 1998, 33, 159-166.
43. Costello, A. L.; Periyannan, G.; Yang, K.-W.; Crowder, M. W.; Tierney, D. L. J. Biol. Inorg. Chem. 2006, 11, 351-358.
44. Sixpack is available free of charge from http://www-ssrl.slac.stanford. edu/~swebb/index.htm.
45. Clark-Baldwin, K.; Tierney, D. L.; Govindaswamy, N.; Gruff, E. S; Kim, C.; Berg, J.; Koch, S. A.; Penner-Hahn, J. E. J. Am. Chem. Soc. 1998, 120, 8401-8409.
46. Thomas, P. W.; Stone, E. M.; Costello, A. L.; Tierney, D. L.; Fast, W. Biochemistry 2005, 44, 7559-7565.
47. Pavletich, N. P.; Pabo, C. O. Science 1991, 252, 809-817.
48. Gibney, B. R.; Mulholland, S. E.; Rabanal, F.; Dutton, P. L. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 15041-15046.
49. Vilar, R. Struct. Bonding 2004, 111, 85-137.
50. Lakowicz, J. R. Principles of Fluorescence Spectroscopy; Kluwer Academic: New York, 1999.
51. Lever, A. B. P. Inorganic Electronic Spectroscopy; Elsevier: Amsterdam, 1984.
52. Bertini, I.; Luchinat, C. Adv. Inorg. Chem. 1984, 6, 71-111.
53. Krizek, B. A.; Merkle, D. L.; Berg, J. M. Inorg. Chem. 1993, 32, 937-940.
54. Anglin, J. R.; Davidson, A. Inorg. Chem. 1975, 14, 234-237.
55. Mathews, C. K.; Van Holde, K. E. Biochemistry; Benjamin/Cummings Publishing Company: Menlo Park, CA, 1996.
56. Bombarda, E.; Cherradi, H.; Morellet, N.; Roques, B. P.; Mély, Y. Biochemistry 2002, 41, 4312-4320.
57. Griep, M. A.; Adkins, B. J.; Hromas, D.; Johnson, S.; Miller, J. Biochemistry 1997, 36, 544-553.
58. Bal, W.; Schwerdtle, T.; Hartwig, A. Chem. Res. Toxicol. 2003, 16, 242-248.
59. Roehm, P. C.; Berg, J. M. Biochemistry 1997, 36, 10240-10245.
60. Payne, J. C.; Rous, B. W.; Tenderholt, A. L.; Godwin, H. A. Biochemistry 2003, 42, 14214-14224.
61. Green, L. M.; Berg, J. M. Proc. Natl. Acad. Sci. U.S.A. 1989, 86, 4047-4051.
62. Green, L. M.; Berg, J. M. Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 6403-6407.
63. (a) Berkovits, H. J.; Berg, J. M. Biochemistry 1999, 38, 16826-16830.
64. (b) Berkovitz-Cymet, H. J.; Amann, B. T.; Berg, J. M. J. Am. Chem. Soc. 2004, 43, 898-903.
65. Bombarda, E.; Cherradi, H.; Morellet, N.; Roqugs, B. P.; Mély, Y. Biochemistry 2002, 41, 4312-4320.
66. Bavoso, A.; Ostuni, A.; Battistuzzi, G.; Menabue, L.; Saladini, M.; Sola, M. Biochem. Biophys. Res. Commun. 1998, 242, 385-389.
67. Posewitz, M. C.; Wilcox, D. E. Chem. Res. Toxicol. 1995, 8, 1020-1028.
68. Berg, J. M.; Merkle, D. L. J. Am. Chem. Soc. 1989, 111, 3759-3761.
69. Lachenmann, M. J.; Ladbury, J. E.; Dong, J.; Huang, K.; Carey, P.; Weiss, M. A. Biochemistry 2004, 43, 13910-13925.
70. Lachenmann, M. J.; Ladbury, J. E.; Phillips, N. B.; Narayana, N.; Qian, X.; Weiss, M. A. J. Mol. Biol. 2002, 316, 969-989.
71. Hori, Y.; Sugiura, Y. J. Am. Chem. Soc. 2002, 124, 9362-9363.
72. McLendon, G.; Hull, H.; Larkin, K.; Chang, W. J. Biol. Inorg. Chem. 1999, 4, 171-174.
73. Kou, W.; Kolla, H. S.; Ortiz-Acevedo, A.; Haines, D. C.; Junker, M.; Dieckmann, G. R. J. Biol. Inorg. Chem. 2005, 10, 167-180.
74. Mély, Y.; Cornille, F.; Fournie-Zaluski, M.; Darlix, J.; Roques, B. P.; Gérard, D. Biopolymers 1991, 31, 899-906.
75. DiTusa, C. A.; Christensen, T.; McCall, K. A.; Fierke, C. A.; Toone, E. J. Biochemistry 2001, 40, 5338-5344.
76. DiTusa, C. A.; McCall, K. A.; Christensen, T.; Mahapatro, M.; Fierke, C. A.; Toone, E. J. Biochemistry 2001, 40, 5345-5351.
77. Yuichiro, H.; Suzuki, K.; Okuno, Y.; Nagaoko, M.; Futaki, S.; Sugiura, Y. J. Am. Chem. Soc. 2000, 122, 7648-7653.
78. Julian, N.; Demene, H.; Morellet, N.; Maigret, B.; Roques, B. P. FEBS 1993, 331, 43-48.
79. Webster, L. C.; Zhang, K.; Chance, B.; Ayene, I.; Culp, J. S.; Huang, W. J.; Wu, F. Y. H.; Ricciardi, R. P. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 9989-9993.
80. folding values in Table 5 are all within the 1.4 kcal/mol error of our measurements.
81. Zagrovic, B.; Snow, C. D.; Khaliq, S.; Shirts, M. R.; Pande, V. S. J. Mol. Biol. 2002, 323, 153-164.
82. Ghosh, M.; Elsby, L. M.; Mal, T. K.; Gooding, J. M.; Roberts, S. G. E.; Ikura, M. Biochem. J. 2004, 378, 317-324.
83. Cerasoli, E.; Sharpe, B. K.; Woolfson, D. N. J. Am. Chem. Soc. 2005, 127, 15008-15009.
84. Sharp, K. Protein Sci. 2001, 10, 661-667.
85. Beasley, J. R.; Doyle, D. F.; Chen, L.; Cohen, D. S.; Fine, B. R.; Pielak, G. J. Proteins 2002, 49, 398-402.
86. Liu, L.; Guo, Q.-X. Chem. Rev. 2001, 101, 673-696.
87. Lumry, R.; Rajender, S. Biopolymers 1970, 9, 1125-1227.