Direct probing of solvent accessibility and mobility at the binding interface of polymerase (Dpo4)-DNA complex

Journal of Physical Chemistry A

Volumn 117, Issue 50, 2013, Pages 13926-13934

  Qin, Yangzhong ^a   Yang, Yi ^a   Zhang, Luyuan ^a   Fowler, Jason D ^a   Qiu, Weihong ^a   Wang, Lijuan ^a   Suo, Zucai ^a   Zhong, Dongping ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINARY AND TERNARY COMPLEXES; ENTROPIC STABILIZATION; FEMTO-SECOND RESOLUTION; INTERFACIAL WATER MOLECULES; INTERMOLECULAR INTERACTIONS; MOLECULAR DYNAMICS SIMULATIONS; PICOSECOND TIME SCALE; SOLVENT ACCESSIBILITY;

AMINO ACIDS; DNA; HYDRATION; MOLECULAR DYNAMICS; POLYMERS;

INTERFACE STATES;

DNA; DNA DIRECTED DNA POLYMERASE BETA; SOLVENT; WATER;

ARTICLE; CHEMISTRY; CONFORMATION; ENZYME ACTIVE SITE; ENZYMOLOGY; METABOLISM; MOLECULAR DYNAMICS; PROTEIN BINDING; SULFOLOBUS SOLFATARICUS;

CATALYTIC DOMAIN; DNA; DNA POLYMERASE BETA; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; SOLVENTS; SULFOLOBUS SOLFATARICUS; WATER;

EID: 84890939582     PISSN: 10895639     EISSN: 15205215     Source Type: Journal    
DOI: 10.1021/jp410051w     Document Type: Article

References (49)

1. Levy, Y.; Onuchic, J. N. Water Mediation in Protein Folding and Molecular Recognition Annu. Rev. Biophys. Biomol. Struct. 2006, 35, 389-415
2. Jayaram, B.; Jain, T. The Role of Water in Protein-DNA Recognition Annu. Rev. Biophys. Biomol. Struct. 2004, 33, 343-361
3. Reddy, C. K.; Das, A.; Jayaram, B. Do Water Molecules Mediate Protein-DNA Recognition? J. Mol. Biol. 2001, 314 (3) 619-632
4. Janin, J. Wet and Dry Interfaces: The Role of Solvent in Protein-Protein and Protein-DNA Recognition Struct. Fold. Des. 1999, 7 (12) R277-R279
5. Schwabe, J. W. R. The Role of Water in Protein DNA Interactions Curr. Opin. Struct. Biol. 1997, 7 (1) 126-134
6. Billeter, M.; Guntert, P.; Luginbuhl, P.; Wuthrich, K. Hydration and DNA Recognition by Homeodomains Cell 1996, 85 (7) 1057-1065
7. Fraenkel, E.; Pabo, C. O. Comparison of X-Ray and NMR Structures for the Antennapedia Homeodomain-DNA Complex Nat. Struct. Biol. 1998, 5 (8) 692-697
8. Davey, C. A.; Sargent, D. F.; Luger, K.; Maeder, A. W.; Richmond, T. J. Solvent Mediated Interactions in the Structure of the Nucleosome Core Particle at 1.9 Angstrom Resolution J. Mol. Biol. 2002, 319 (5) 1097-1113
9. Ferreiro, D. U.; Sanchez, I. E.; Gay, G. D. Transition State for Protein-DNA Recognition Proc. Natl. Acad. Sci. U. S. A. 2008, 105 (31) 10797-10802
10. Tsui, V.; Radhakrishnan, I.; Wright, P. E.; Case, D. A. NMR and Molecular Dynamics Studies of the Hydration of a Zinc Finger-DNA Complex J. Mol. Biol. 2000, 302 (5) 1101-1117
11. Sunnerhagen, M.; Denisov, V. P.; Venu, K.; Bonvin, A. M. J. J.; Carey, J.; Halle, B.; Otting, G. Water Molecules in DNA Recognition I: Hydration Lifetimes of Trp Operator DNA in Solution Measured by NMR Spectroscopy J. Mol. Biol. 1998, 282 (4) 847-858
12. Kosztin, D.; Bishop, T. C.; Schulten, K. Binding of the Estrogen Receptor to DNA. The Role of Waters Biophys. J. 1997, 73 (2) 557-570
13. Gorfe, A. A.; Caflisch, A.; Jelesarov, I. The Role of Flexibility and Hydration on the Sequence-Specific DNA Recognition by the Tn916 Integrase Protein: A Molecular Dynamics Analysis J. Mol. Recognit. 2004, 17 (2) 120-131
14. Otting, G.; Liepinsh, E.; Wuthrich, K. Protein Hydration in Aqueous-Solution Science 1991, 254 (5034) 974-980
15. Zhong, D.; Pal, S. K.; Zewail, A. H. Femtosecond Studies of Protein-DNA Binding and Dynamics: Histone I ChemPhysChem 2001, 2 (4) 219-227
16. Yang, W. Damage Repair DNA Polymerases Y Curr. Opin. Struct. Biol. 2003, 13 (1) 23-30
17. Wong, J. H.; Fiala, K. A.; Suo, Z.; Ling, H. Snapshots of a Y-family DNA Polymerase in Replication: Substrate-Induced Conformational Transitions and Implications for Fidelity of Dpo4 J. Mol. Biol. 2008, 379 (2) 317-330
18. Ling, H.; Boudsocq, F.; Woodgate, R.; Yang, W. Crystal Structure of a Y-family DNA Polymerase in Action: A Mechanism for Error-Prone and Lesion-Bypass Replication Cell 2001, 107 (1) 91-102
19. Fiala, K. A.; Suo, Z. Mechanism of DNA Polymerization Catalyzed by Sulfolobus Solfataricus P2 DNA Polymerase IV Biochemistry 2004, 43 (7) 2116-2125
20. Rechkoblit, O.; Malinina, L.; Cheng, Y.; Kuryavyi, V.; Broyde, S.; Geacintov, N. E.; Patel, D. J. Stepwise Translocation of Dpo4 Polymerase During Error-Free Bypass of an OxoG lesion PLoS Biol. 2006, 4 (1) 25-42
21. Wang, L. H.; Yu, X. Y.; Hu, P.; Broyde, S.; Zhang, Y. K. A Water-Mediated and Substrate-Assisted Catalytic Mechanism for Sulfolobus Solfataricus DNA Polymerase IV J. Am. Chem. Soc. 2007, 129 (15) 4731-4737
22. Wang, Y.; Schlick, T. Quantum Mechanics/Molecular Mechanics Investigation of the Chemical Reaction in Dpo4 Reveals Water-Dependent Pathways and Requirements for Active Site Reorganization J. Am. Chem. Soc. 2008, 130 (40) 13240-13250
23. Zhong, D. Hydration Dynamics and Coupled Water-Protein Fluctuations Probed by Intrinsic Tryptophan Adv. Chem. Phys. 2009, 143, 83-149
24. Zhang, L.; Wang, L.; Kao, Y. T.; Qiu, W.; Yang, Y.; Okobiah, O.; Zhong, D. Mapping Hydration Dynamics Around a Protein Surface Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (47) 18461-18466
25. Zhang, L.; Yang, Y.; Kao, Y. T.; Wang, L.; Zhong, D. Protein Hydration Dynamics and Molecular Mechanism of Coupled Water-Protein Fluctuations J. Am. Chem. Soc. 2009, 131 (30) 10677-10691
26. Qin, Y.; Chang, C. W.; Wang, L.; Zhong, D. Validation of Response Function Construction and Probing Heterogeneous Protein Hydration by Intrinsic Tryptophan J. Phys. Chem. B 2012, 116 (45) 13320-13330
27. Fiala, K. A.; Suo, Z. Pre-Steady-State Kinetic Studies of the Fidelity of Sulfolobus Solfataricus P2 DNA Polymerase IV Biochemistry 2004, 43 (7) 2106-2115
28. Fiala, K. A.; Sherrer, S. M.; Brown, J. A.; Suo, Z. Mechanistic Consequences of Temperature on DNA Polymerization Catalyzed by a Y-family DNA Polymerase Nucleic Acids Res. 2008, 36 (6) 1990-2001
29. Zhang, L.; Kao, Y. T.; Qiu, W.; Wang, L.; Zhong, D. Femtosecond Studies of Tryptophan Fluorescence Dynamics in Proteins: Local Solvation and Electronic Quenching J. Phys. Chem. B 2006, 110 (37) 18097-18103
30. Lakowicz, J. R. Principles of Fluorescence Spectroscopy; Springer: Berlin, 2007.
31. Matsika, S. Three-State Conical Intersections in Nucleic Acid Bases J. Phys. Chem. A 2005, 109 (33) 7538-7545
32. Hudock, H. R.; Martinez, T. J. Excited-State Dynamics of Cytosine Reveal Multiple Intrinsic Subpicosecond Pathways ChemPhysChem 2008, 9 (17) 2486-2490
33. Qiu, W.; Zhang, L.; Kao, Y. T.; Lu, W.; Li, T.; Kim, J.; Sollenberger, G. M.; Wang, L.; Zhong, D. Ultrafast Hydration Dynamics in Melittin Folding and Aggregation: Helix Formation and Tetramer Self-Assembly J. Phys. Chem. B 2005, 109 (35) 16901-16910
34. Qiu, W.; Zhang, L.; Okobiah, O.; Yang, Y.; Wang, L.; Zhong, D.; Zewail, A. H. Ultrafast Solvation Dynamics of Human Serum Albumin: Correlations with Conformational Transitions and Site-Selected Recognition J. Phys. Chem. B 2006, 110 (21) 10540-10549
35. Qiu, W.; Kao, Y. T.; Zhang, L.; Yang, Y.; Wang, L.; Stites, W. E.; Zhong, D.; Zewail, A. H. Protein Surface Hydration Mapped by Site-Specific Mutations Proc. Natl. Acad. Sci. U. S. A. 2006, 103 (38) 13979-13984
36. Li, T.; Hassanali, A. A.; Kao, Y. T.; Zhong, D.; Singer, S. J. Hydration Dynamics and Time Scales of Coupled Water-Protein Fluctuations J. Am. Chem. Soc. 2007, 129 (11) 3376-3382
37. Li, T.; Hassanali, A. A.; Singer, S. J. Origin of Slow Relaxation Following Photoexcitation of W7 in Myoglobin and the Dynamics of Its Hydration Layer J. Phys. Chem. B 2008, 112 (50) 16121-16134
38. Yang, J.; Zhang, L.; Wang, L.; Zhong, D. Femtosecond Conical Intersection Dynamics of Tryptophan in Proteins and Validation of Slowdown of Hydration Layer Dynamics J. Am. Chem. Soc. 2012, 134 (40) 16460-16463
39. Pal, S. K.; Peon, J.; Bagchi, B.; Zewail, A. H. Biological Water: Femtosecond Dynamics of Macromolecular Hydration J. Phys. Chem. B 2002, 106 (48) 12376-12395
40. Pal, S. K.; Zewail, A. H. Dynamics of Water in Biological Recognition Chem. Rev. 2004, 104 (4) 2099-2123
41. Zhong, D.; Pal, S. K.; Zewail, A. H. Biological Water: A Critique Chem. Phys. Lett. 2011, 503 (1-3) 1-11
42. Lu, W.; Qiu, W.; Kim, J.; Okobiah, O.; Hu, H.; Gokel, G. W.; Zhong, D. Femtosecond Studies of Crown Ethers: Supramolecular Solvation, Local Solvent Structure and Cation-Pi Interaction Chem. Phys. Lett. 2004, 394 (4-6) 415-422
43. Grebenkov, D. S.; Goddard, Y. A.; Diakova, G.; Korb, J. P.; Bryant, R. G. Dimensionality of Diffusive Exploration at the Protein Interface in Solution J. Phys. Chem. B 2009, 113 (40) 13347-13356
44. Armstrong, B. D.; Choi, J.; Lopez, C.; Wesener, D. A.; Hubbell, W.; Cavagnero, S.; Han, S. Site-Specific Hydration Dynamics in the Nonpolar Core of a Molten Globule by Dynamic Nuclear Polarization of Water J. Am. Chem. Soc. 2011, 133 (15) 5987-5995
45. Jesenska, A.; Sykora, J.; Olzynska, A.; Brezovsky, J.; Zdrahal, Z.; Damborsky, J.; Hof, M. Nanosecond Time-Dependent Stokes Shift at the Tunnel Mouth of Haloalkane Dehalogenases J. Am. Chem. Soc. 2009, 131 (2) 494-501
46. Nucci, N. V.; Pometun, M. S.; Wand, A. J. Site-Resolved Measurement of Water-Protein Interactions by Solution NMR Nat. Struct. Mol. Biol. 2011, 18 (2) 245-249
47. Chang, C. W.; Guo, L.; Kao, Y. T.; Li, J.; Tan, C.; Li, T.; Saxena, C.; Liu, Z.; Wang, L.; Sancar, A.; Zhong, D. Ultrafast Solvation Dynamics at Binding and Active Sites of Photolyases Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (7) 2914-2919
48. Chang, C. W.; He, T. F.; Guo, L.; Stevens, J. A.; Li, T.; Wang, L.; Zhong, D. Mapping Solvation Dynamics at the Function Site of Flavodoxin in Three Redox States J. Am. Chem. Soc. 2010, 132 (36) 12741-12747
49. Steiner, R. F. In Topics in Fluorescence Spectroscopy; Lakowicz, J. R., Ed.; Plenum Press: New York, 1991; Vol. 2, pp 1-51.