The mechanochemistry of a structural zinc finger

Journal of Physical Chemistry Letters

Volumn 6, Issue 13, 2015, Pages 3335-3340

  Perales Calvo, Judit ^a   Lezamiz, Ainhoa ^a   Garcia Manyes, Sergi ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ATOMIC FORCE MICROSCOPY; BINS; CHEMICAL BONDS; COVALENT BONDS; MECHANICAL STABILITY; PROTEINS; THERMODYNAMIC STABILITY;

DIRECT IDENTIFICATIONS; DISULFIDE BOND FORMATION; EXPERIMENTAL APPROACHES; KINETIC PROPERTIES; NATURALLY OCCURRING; PROTEIN ENGINEERING; SINGLE MOLECULE FORCE SPECTROSCOPY; ZINC FINGER MOTIFS;

ZINC;

EID: 84942581390     PISSN: None     EISSN: 19487185     Source Type: Journal    
DOI: 10.1021/acs.jpclett.5b01371     Document Type: Article

References (41)

1. Thomson, A. J.; Gray, H. B. Bio-Inorganic Chemistry. Curr. Opin. Chem. Biol. 1998, 2, 155-158.
2. Sousa, S. F.; Lopes, A. B.; Fernandes, P. A.; Ramos, M. J. The Zinc Proteome: a Tale of Stability and Functionality. Dalton Trans 2009, 38, 7946-7956.
3. Andreini, C.; Banci, L.; Bertini, I.; Rosato, A. Zinc Through the Three Domains of Life. J. Proteome Research 2006, 5, 3173-3178.
4. Krishna, S. S.; Majumdar, I.; Grishin, N. V. Structural Classification of Zinc Fingers: Survey and Summary. Nucleic Acids Res. 2003, 31, 532-550.
5. Laity, J. H.; Lee, B. M.; Wright, P. E. Zinc Finger Proteins: New Insights into Structural and Functional Diversity. Curr. Opin. Struct. Biol. 2001, 11, 39-46.
6. Maret, W.; Li, Y. Coordination Dynamics of Zinc in Proteins. Chem. Rev. 2009, 109, 4682-4707.
7. Cox, E. H.; McLendon, G. L. Zinc-Dependent Protein Folding. Curr. Opin. Chem. Biol. 2000, 4, 162-165.
8. Beyer, M. K.; Clausen-Schaumann, H. Mechanochemistry: The Mechanical Activation of Covalent Bonds. Chem. Rev. 2005, 105, 2921-2948.
9. Oberhauser, A. F.; Carrion-Vazquez, M. Mechanical Biochemistry of Proteins: One Molecule at a Time. J. Biol. Chem. 2008, 283, 6617-6621.
10. Grandbois, M.; Beyer, M.; Rief, M.; Clausen-Schaumann, H.; Gaub, H. E. How Strong is a Covalent Bond? Science 1999, 283, 1727-1730.
11. Garcia-Manyes, S.; Liang, J.; Szoszkiewicz, R.; Kuo, T. L.; Fernandez, J. M. Force-Activated Reactivity Switch in a Bimolecular Chemical Reaction. Nat. Chem. 2009, 1, 236-242.
12. Zheng, P.; Li, H. Highly Covalent Ferric-Thiolate Bonds Exhibit Surprisingly Low Mechanical Stability. J. Am. Chem. Soc. 2011, 133, 6791-6798.
13. Zheng, P.; Takayama, S. I. J.; Mauk, A. G.; Li, H. B. Hydrogen Bond Strength Modulates the Mechanical Strength of Ferric-Thiolate Bonds in Rubredoxin. J. Am. Chem. Soc. 2012, 134, 4124-4131.
14. Zheng, P.; Takayama, S. J.; Mauk, A. G.; Li, H. B. Single Molecule Force Spectroscopy Reveals That Iron Is Released from the Active Site of Rubredoxin by a Stochastic Mechanism. J. Am. Chem. Soc. 2013, 135, 7992-8000.
15. Ainavarapu, S. R.; Li, L.; Badilla, C. L.; Fernandez, J. M. Ligand Binding Modulates the Mechanical Stability of Dihydrofolate Reductase. Biophys. J. 2005, 89, 3337-3344.
16. Cao, Y.; Yoo, T.; Li, H. Single Molecule Force Spectroscopy Reveals Engineered Metal Chelation is a General Approach to Enhance Mechanical Stability of Proteins. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 11152-11157.
17. Hu, X.; Li, H. Force Spectroscopy Studies on Protein-Ligand Interactions: a Single Protein Mechanics Perspective. FEBS Lett. 2014, 588, 3613-3620.
18. Martinez-Yamout, M.; Legge, G. B.; Zhang, O. W.; Wright, P. E.; Dyson, H. J. Solution Structure of the Cysteine-Rich Domain of the Escherichia coli Chaperone Protein DnaJ. J. Mol. Biol. 2000, 300, 805-818.
19. Cheetham, M. E.; Caplan, A. J. Structure, Function and Evolution of DnaJ: Conservation and Adaptation of Chaperone Function. Cell Stress Chaperones 1998, 3, 28-36.
20. Szabo, A.; Langer, T.; Schroder, H.; Flanagan, J.; Bukau, B.; Hartl, F. U. The ATP Hydrolysis-Dependent Reaction Cycle of the Escherichia coli Hsp70 system DnaK, DnaJ, and GrpE. Proc. Natl. Acad. Sci. U. S. A. 1994, 91, 10345-10349.
21. Zheng, P.; Li, H. Direct Measurements of the Mechanical Stability of Zinc-Thiolate Bonds in Rubredoxin by Single-Molecule Atomic Force Microscopy. Biophys. J. 2011, 101, 1467-1473.
22. Peng, Q.; Li, H. B. Domain Insertion Effectively Regulates the Mechanical Unfolding Hierarchy of Elastomeric Proteins: Toward Engineering Multifunctional Elastomeric Proteins. J. Am. Chem. Soc. 2009, 131, 14050-14056.
23. Li, H. B.; Fernandez, J. M. Mechanical Design of the First Proximal Ig Domain of Human Cardiac Titin Revealed by Single Molecule Force Spectroscopy. J. Mol. Biol. 2003, 334, 75-86.
24. Brockwell, D. J.; Beddard, G. S.; Paci, E.; West, D. K.; Olmsted, P. D.; Smith, D. A.; Radford, S. E. Mechanically Unfolding the Small, Topologically Simple Protein L. Biophys. J. 2005, 89, 506-519.
25. Liu, R.; Garcia-Manyes, S.; Sarkar, A.; Badilla, C. L.; Fernandez, J. M. Mechanical Characterization of Protein L in the Low-Force Regime by Electromagnetic Tweezers/Evanescent Nanometry. Biophys. J. 2009, 96, 3810-3821.
26. Banecki, B.; Liberek, K.; Wall, D.; Wawrzynow, A.; Georgopoulos, C.; Bertoli, E.; Tanfani, F.; Zylicz, M. Structure-Function Analysis of the Zinc Finger Region of the DnaJ Molecular Chaperone. J. Biol. Chem. 1996, 271, 14840-14848.
27. Perales-Calvo, J.; Muga, A.; Moro, F. Role of DnaJ G/F-rich Domain in Conformational Recognition and Binding of Protein Substrates. J. Biol. Chem. 2010, 285, 34231-34239.
28. Picot, D.; Ohanessian, G.; Frison, G. Thermodynamic Stability Versus Kinetic Lability of ZnS4 Core. Chem.-Asian J. 2010, 5, 1445-1454.
29. Solomon, E. I.; Gorelsky, S. I.; Dey, A. Metal-Thiolate Bonds in Bioinorganic Chemistry. J. Comput. Chem. 2006, 27, 1415-1428.
30. Lee, Y. M.; Lim, C. Factors Controlling the Reactivity of Zinc Finger Cores. J. Am. Chem. Soc. 2011, 133, 8691-8703.
31. Linke, K.; Wolfram, T.; Bussemer, J.; Jakob, U. The Roles of the Two Zinc Binding Sites in DnaJ. J. Biol. Chem. 2003, 278, 44457-44466.
32. Shi, Y Y.; Tang, W.; Hao, S. F.; Wang, C. C. Contributions of Cysteine Residues in Zn2 to Zinc Fingers and Thiol-Disulfide Oxidoreductase Activities of Chaperone DnaJ. Biochemistry 2005, 44, 1683-1689.
33. Reddi, A. R.; Gibney, B. R. Role of Protons in the Thermodynamic Contribution of a Zn(II)-Cys(4) Site Toward Metalloprotein Stability. Biochemistry 2007, 46, 3745-3758.
34. Reddi, A. R.; Guzman, T. R.; Breece, R. M.; Tierney, D. L.; Gibney, B. R. Deducing the Energetic Cost of Protein Folding in Zinc Finger Proteins Using Designed Metallopeptides. J. Am. Chem. Soc. 2007, 129, 12815-12827.
35. Li, H.; Wang, H. C.; Cao, Y.; Sharma, D.; Wang, M. Configurational Entropy Modulates the Mechanical Stability of Protein GB1. J. Mol. Biol. 2008, 379, 871-880.
36. Li, J.; Qian, X.; Sha, B. The Crystal Structure of the Yeast Hsp40 Ydj1 Complexed with its Peptide Substrate. Structure 2003, 11, 1475-1483.
37. Szabo, A.; Korszun, R.; Hartl, F. U.; Flanagan, J. A Zinc Fingerlike Domain of the Molecular Chaperone DnaJ is Involved in Binding to Denatured Protein Substrates. EMBO J. 1996, 15, 408-417.
38. Montgomery, D. L.; Morimoto, R. I.; Gierasch, L. M. Mutations in the Substrate Binding Domain of the Escherichia coli 70 kDa Molecular Chaperone, DnaK, which Alter Substrate Affinity or Interdomain Coupling. J. Mol. Biol. 1999, 286, 915-932.
39. Bertz, M.; Rief, M. Ligand Binding Mechanics of Maltose Binding Protein. J. Mol. Biol. 2009, 393, 1097-1105.
40. Schlierf, M.; Li, H.; Fernandez, J. M. The Unfolding Kinetics of Ubiquitin Captured with Single-Molecule Force-ClampTechniques. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 7299-7304.
41. Popa, I.; Kosuri, P.; Alegre-Cebollada, J.; Garcia-Manyes, S.; Fernandez, J. M. Force Dependency of Biochemical Reactions Measured by Single-Molecule Force-Clamp spectroscopy. Nat. Protoc. 2013, 8, 1261-1276.