ACS Publications. Most Trusted. Most Cited. Most Read
Cooperativity and Specificity of Cys2His2 Zinc Finger Protein−DNA Interactions: A Molecular Dynamics Simulation Study

OR SEARCH CITATIONS

My Activity
Publications

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Phys. Chem. B 2010, 114, 22, 7662-7671
    Article

    Cooperativity and Specificity of Cys2His2 Zinc Finger Protein−DNA Interactions: A Molecular Dynamics Simulation Study
    Click to copy article linkArticle link copied!

    View Author Information
    Department of Chemistry, Seoul National University, Seoul, Republic of Korea
    * To whom correspondence should be addressed. E-mail: [email protected]. Phone: 82-2-880-9197. Fax: 82-2-871-8119.
    Other Access OptionsSupporting Information (1)

    The Journal of Physical Chemistry B

    Cite this: J. Phys. Chem. B 2010, 114, 22, 7662–7671
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jp1017289
    Published May 14, 2010
    Copyright © 2010 American Chemical Society
    Request reuse permissions

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    Cys2His2 zinc finger proteins are one of the most frequently observed DNA-binding motifs in eukaryotes. They have been widely used as a framework for designing new DNA-binding proteins. In this work, the binding affinity and conformational change of the Zif268−DNA complex were successfully reproduced with MD simulations and MM-PBSA analysis. The following new discoveries on the zinc finger protein−DNA interactions were obtained by careful energy decomposition analysis. First, a dramatic increase in the binding affinity was observed when the third zinc finger is added, indicating a cooperative nature. This cooperativity is shown to be a consequence of the small but distinctive conformational change of DNA, which enables a tight fit of the protein into the major groove of DNA. Second, specificity of the amino acid−nucleotide recognitions observed in the crystal structure is explained as originating from the ability of specific side chains and bases to take the optimal geometries for favorable interactions between polar groups. The success of the current approach implies that similar methods could be further applied to the study of protein−DNA interactions involving longer polyfingers or different linkers between fingers to provide insights for design of novel zinc finger proteins.

    Copyright © 2010 American Chemical Society

    Subjects

    what are subjects

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    Fifteen supplementary tables and four supplementary figures. This material is available free of charge via the Internet at http://pubs.acs.org.

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!
    Citation Statements
    Explore this article's citation statements on scite.ai
    powered by  Scite

    This article is cited by 34 publications.

    1. Sekhar Talluri. Engineering and Design of Programmable Genome Editors. The Journal of Physical Chemistry B 2022, 126 (28) , 5140-5150. https://doi.org/10.1021/acs.jpcb.2c03761
    2. Ly H. Nguyen, Tuyen T. Tran, Lien Thi Ngoc Truong, Hanh Hong Mai, Toan T. Nguyen. Overcharging of the Zinc Ion in the Structure of the Zinc-Finger Protein Is Needed for DNA Binding Stability. Biochemistry 2020, 59 (13) , 1378-1390. https://doi.org/10.1021/acs.biochem.9b01055
    3. Ryan C. Godwin, Ryan L. Melvin, William H. Gmeiner, and Freddie R. Salsbury, Jr. . Binding Site Configurations Probe the Structure and Dynamics of the Zinc Finger of NEMO (NF-κB Essential Modulator). Biochemistry 2017, 56 (4) , 623-633. https://doi.org/10.1021/acs.biochem.6b00755
    4. Abhijnan Chattopadhyay, Levani Zandarashvili, Ross H. Luu, and Junji Iwahara . Thermodynamic Additivity for Impacts of Base-Pair Substitutions on Association of the Egr-1 Zinc-Finger Protein with DNA. Biochemistry 2016, 55 (47) , 6467-6474. https://doi.org/10.1021/acs.biochem.6b00757
    5. Cheng Tan, Wenfei Li, and Wei Wang . Localized Frustration and Binding-Induced Conformational Change in Recognition of 5S RNA by TFIIIA Zinc Finger. The Journal of Physical Chemistry B 2013, 117 (50) , 15917-15925. https://doi.org/10.1021/jp4052165
    6. Tong Zhu, Xudong Xiao, Changge Ji, and John Z. H. Zhang . A New Quantum Calibrated Force Field for Zinc–Protein Complex. Journal of Chemical Theory and Computation 2013, 9 (3) , 1788-1798. https://doi.org/10.1021/ct301091z
    7. Lin Chen, Ji-Long Zhang, Li-Ying Yu, Qing-Chuan Zheng, Wen-Ting Chu, Qiao Xue, Hong-Xing Zhang, and Chia-Chung Sun . Influence of Hyperthermophilic Protein Cren7 on the Stability and Conformation of DNA: Insights from Molecular Dynamics Simulation and Free Energy Analysis. The Journal of Physical Chemistry B 2012, 116 (41) , 12415-12425. https://doi.org/10.1021/jp305860h
    8. Hirotoshi Mori and Kaori Ueno-Noto . A Theoretical Study of the Physicochemical Mechanisms Associated with DNA Recognition Modulation in Artificial Zinc-Finger Proteins. The Journal of Physical Chemistry B 2011, 115 (16) , 4774-4780. https://doi.org/10.1021/jp1097348
    9. Yufei Li, Lin Chen, Zhisen Han, Jingyun Na, Ruige Wang, Tao Jing, Bing Zhao. Exploring the effects of mutations on NFAT5‐DNA binding using molecular dynamics simulations and energy calculations. International Journal of Quantum Chemistry 2022, 122 (21) https://doi.org/10.1002/qua.26980
    10. Xiang-Feng Wang, Jian Sun, Xin-Lu Wang, Jia-Kun Tian, Zhen-Wei Tian, Ji-Long Zhang, Ran Jia. MD investigation on the binding of microphthalmia-associated transcription factor with DNA. Journal of Saudi Chemical Society 2022, 26 (2) , 101420. https://doi.org/10.1016/j.jscs.2022.101420
    11. Mazen Y. Hamed, Reema Siam, Roza Zaid. The role of zinc finger linkers in zinc finger protein binding to DNA. Journal of Computer-Aided Molecular Design 2021, 35 (9) , 973-986. https://doi.org/10.1007/s10822-021-00413-6
    12. Li-Hua Bie, Jun-Wen Fei, Jun Gao. Molecular mechanism of methyl-dependent and spatial-specific DNA recognition of c-Jun homodimer. Journal of Molecular Modeling 2021, 27 (8) https://doi.org/10.1007/s00894-021-04840-y
    13. Xiaowen Wang, Honghui Zhang, Wenjin Li. DNA-binding mechanisms of human and mouse cGAS: a comparative MD and MM/GBSA study. Physical Chemistry Chemical Physics 2020, 22 (45) , 26390-26401. https://doi.org/10.1039/D0CP04162A
    14. Ji Lei, Xingxing Gou, Shaopeng Wei, Jinhong Zhou, Zongxiao Li. Spectroscopy, Thermodynamics and Molecular Docking of Fraxinellone with DNA. Bulletin of Environmental Contamination and Toxicology 2020, 104 (6) , 864-870. https://doi.org/10.1007/s00128-020-02860-7
    15. Mazen Y. Hamed. Role of protein structure and the role of individual fingers in zinc finger protein–DNA recognition: a molecular dynamics simulation study and free energy calculations. Journal of Computer-Aided Molecular Design 2018, 32 (6) , 657-669. https://doi.org/10.1007/s10822-018-0119-9
    16. Sangita Kachhap, Pragya Priyadarshini, Balvinder Singh. Molecular dynamics simulations show altered secondary structure of clawless in binary complex with DNA providing insights into aristaless-clawless-DNA ternary complex formation. Journal of Biomolecular Structure and Dynamics 2017, 35 (6) , 1153-1167. https://doi.org/10.1080/07391102.2016.1175967
    17. Chun-Chi Chou, Shu-Yi Wei, Yuan-Chao Lou, Chinpan Chen, . In-depth study of DNA binding of Cys2His2 finger domains in testis zinc-finger protein. PLOS ONE 2017, 12 (4) , e0175051. https://doi.org/10.1371/journal.pone.0175051
    18. Wieslaw Nowak. Applications of Computational Methods to Simulations of Proteins Dynamics. 2017, 1627-1669. https://doi.org/10.1007/978-3-319-27282-5_31
    19. Wieslaw Nowak. Applications of Computational Methods to Simulations of Protein Dynamics. 2016, 1-43. https://doi.org/10.1007/978-94-007-6169-8_31-2
    20. Sangita Kachhap, Balvinder Singh. Role of DNA conformation & energetic insights in Msx-1-DNA recognition as revealed by molecular dynamics studies on specific and nonspecific complexes. Journal of Biomolecular Structure and Dynamics 2015, 33 (10) , 2069-2082. https://doi.org/10.1080/07391102.2014.995709
    21. Patricia Esperón, Claudio Scazzocchio, Margot Paulino. In vitro and in silico analysis of the Aspergillus nidulans DNA–CreA repressor interactions. Journal of Biomolecular Structure and Dynamics 2014, 32 (12) , 2033-2041. https://doi.org/10.1080/07391102.2013.843474
    22. Felipe Merino, Calista Keow Leng Ng, Veeramohan Veerapandian, Hans Robert Schöler, Ralf Jauch, Vlad Cojocaru. Structural Basis for the SOX-Dependent Genomic Redistribution of OCT4 in Stem Cell Differentiation. Structure 2014, 22 (9) , 1274-1286. https://doi.org/10.1016/j.str.2014.06.014
    23. Jiali Gu, Min Liu, Fei Guo, Wenping Xie, Wenqiang Lu, Lidan Ye, Zhirong Chen, Shenfeng Yuan, Hongwei Yu. Virtual screening of mandelate racemase mutants with enhanced activity based on binding energy in the transition state. Enzyme and Microbial Technology 2014, 55 , 121-127. https://doi.org/10.1016/j.enzmictec.2013.10.008
    24. Yi-Pei Chen, Chad C. Catbagan, Jeannette T. Bowler, Trevor Gokey, Natalie D.M. Goodwin, Anton B. Guliaev, Weiming Wu, Taro Amagata. Evaluation of benzoic acid derivatives as sirtuin inhibitors. Bioorganic & Medicinal Chemistry Letters 2014, 24 (1) , 349-352. https://doi.org/10.1016/j.bmcl.2013.11.004
    25. Jian Gao, Wei Cui, Yuguo Du, Mingjuan Ji. Insight into the molecular mechanism about lowered dihydrofolate binding affinity to dihydrofolate reductase-like 1 (DHFRL1). Journal of Molecular Modeling 2013, 19 (12) , 5187-5198. https://doi.org/10.1007/s00894-013-2018-2
    26. CHENG TAN, WENFEI LI, WEI WANG. SPECIFIC BINDING OF A SHORT miRNA SEQUENCE BY ZINC KNUCKLES OF Lin28: A MOLECULAR DYNAMICS SIMULATION STUDY. Journal of Theoretical and Computational Chemistry 2013, 12 (08) , 1341015. https://doi.org/10.1142/S0219633613410150
    27. Wen-Ting Chu, Qing-Chuan Zheng. Conformational Changes of Enzymes and DNA in Molecular Dynamics. 2013, 179-217. https://doi.org/10.1016/B978-0-12-411636-8.00005-5
    28. Lin Chen, Qing-Chuan Zheng, Li-Ying Yu, Wen-Ting Chu, Ji-Long Zhang, Qiao Xue, Hong-Xing Zhang, Chia-Chung Sun. Insights into the thermal stabilization and conformational transitions of DNA by hyperthermophile protein Sso7d: molecular dynamics simulations and MM-PBSA analysis. Journal of Biomolecular Structure and Dynamics 2012, 30 (6) , 716-727. https://doi.org/10.1080/07391102.2012.689702
    29. Hong Zhang, Yao Yao, Huibin Yang, Xia Wang, Zhuo Kang, Yan Li, Guohui Li, Yonghua Wang. Molecular dynamics and free energy studies on the carboxypeptidases complexed with peptide/small molecular inhibitor: Mechanism for drug resistance. Insect Biochemistry and Molecular Biology 2012, 42 (8) , 583-595. https://doi.org/10.1016/j.ibmb.2012.04.005
    30. Claudio Carra, Francis A. Cucinotta. Accurate prediction of the binding free energy and analysis of the mechanism of the interaction of replication protein A (RPA) with ssDNA. Journal of Molecular Modeling 2012, 18 (6) , 2761-2783. https://doi.org/10.1007/s00894-011-1288-9
    31. Nadine Homeyer, Holger Gohlke. Free Energy Calculations by the Molecular Mechanics Poisson−Boltzmann Surface Area Method. Molecular Informatics 2012, 31 (2) , 114-122. https://doi.org/10.1002/minf.201100135
    32. Yongping Pan, Ruth Nussinov, . The Role of Response Elements Organization in Transcription Factor Selectivity: The IFN-β Enhanceosome Example. PLoS Computational Biology 2011, 7 (6) , e1002077. https://doi.org/10.1371/journal.pcbi.1002077
    33. Amos Adler, Yoon-Dong Park, Peter Larsen, Vijayaraj Nagarajan, Kurt Wollenberg, Jin Qiu, Timothy G. Myers, Peter R. Williamson. A Novel Specificity Protein 1 (SP1)-like Gene Regulating Protein Kinase C-1 (Pkc1)-dependent Cell Wall Integrity and Virulence Factors in Cryptococcus neoformans. Journal of Biological Chemistry 2011, 286 (23) , 20977-20990. https://doi.org/10.1074/jbc.M111.230268
    34. Liane Saíz-Urra, Miguel Angel Cabrera, Matheus Froeyen. Exploring the conformational changes of the ATP binding site of gyrase B from Escherichia coli complexed with different established inhibitors by using molecular dynamics simulation. Journal of Molecular Graphics and Modelling 2011, 29 (5) , 726-739. https://doi.org/10.1016/j.jmgm.2010.12.005
    Download PDF
    Go to The Journal of Physical Chemistry B
    Get e-Alerts
    Get e-Alerts

    The Journal of Physical Chemistry B

    Cite this: J. Phys. Chem. B 2010, 114, 22, 7662–7671
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jp1017289
    Published May 14, 2010
    Copyright © 2010 American Chemical Society
    Request reuse permissions

    Article Views

    1505

    Altmetric

    -

    Citations

    34
    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.