ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Figure 1Loading Img

Geometrical and Electronic Structure Variability of the Sugar−phosphate Backbone in Nucleic Acids

View Author Information
Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic, Flemingovo náměstí 2, 166 10, Prague 6, Czech Republic, Institute of Biophysics, Academy of Sciences of the Czech Republic, Královopolská 135, 612 65 Brno, Czech Republic, Molecular Modeling and Bioinformatics Unit, Institut de Recerca Biomèdica, Parc Científic de Barcelona, Josep Samitier 1-5, Barcelona 08028, Spain, Departament de Bioquímica i Biologia Molecular, Universitat de Barcelona, Avgda Diagonal 645, Barcelona 08028, Spain, Barcelona Supercomputing Center, Jordi Girona 31, Edifici Torre Girona, Barcelona 08034, Spain, Department of Medicinal Chemistry and Department of Pharmaceutics and Pharmaceutical Chemistry, College of Pharmacy, University of Utah, Salt Lake City, Utah 84112, Department of Physical Chemistry and Institute of Biomedicine (IBUB), Faculty of Pharmacy, University of Barcelona, Avenida Diagonal 643, 08028 Barcelona, Spain, and Computational Biology Program, Barcelona Supercomputer Center, Jordi Girona 29, Edifici Nexus II, Barcelona 08034, Spain
* Corresponding author. E-mail: [email protected]
†Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic.
‡Institute of Biophysics, Academy of Sciences of the Czech Republic.
§Parc Científic de Barcelona.
∥Departament de Bioquímica i Biologia Molecular, Universitat de Barcelona.
⊥Barcelona Supercomputing Center, Edifici Torre Girona.
#University of Utah.
∇Faculty of Pharmacy, University of Barcelona.
○Barcelona Supercomputer Center, Edifici Nexus II.
Cite this: J. Phys. Chem. B 2008, 112, 27, 8188–8197
Publication Date (Web):June 18, 2008
https://doi.org/10.1021/jp801245h
Copyright © 2008 American Chemical Society

    Article Views

    885

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Other access options
    Supporting Info (1)»

    Abstract

    The anionic sugar−phosphate backbone of nucleic acids substantially contributes to their structural flexibility. To model nucleic acid structure and dynamics correctly, the potentially sampled substates of the sugar−phosphate backbone must be properly described. However, because of the complexity of the electronic distribution in the nucleic acid backbone, its representation by classical force fields is very challenging. In this work, the three-dimensional potential energy surfaces with two independent variables corresponding to rotations around the α and γ backbone torsions are studied by means of high-level ab initio methods (B3LYP/6-31+G*, MP2/6-31+G*, and MP2 complete basis set limit levels). The ability of the AMBER ff99 [Wang, J. M.; Cieplak, P.; Kollman, P. A. J. Comput. Chem.2000, 21, 1049−1074] and parmbsc0 [Perez, A.; Marchan, I.; Svozil, D.; Šponer, J.; Cheatham, T. E.; Laughten, C. A.; Orozco, M. Biophys. J.2007, 92, 3817−3829] force fields to describe the various α/γ conformations of the DNA backbone accurately is assessed by comparing the results with those of ab initio quantum chemical calculations. Two model systems differing in structural complexity were used to describe the α/γ energetics. The simpler one, SPM, consisting of a sugar and methyl group linked through a phosphodiester bond was used to determine higher-order correlation effects covered by the CCSD(T) method. The second, more complex model system, SPSOM, includes two deoxyribose residues (without the bases) connected via a phosphodiester bond. It has been shown by means of a natural bond orbital analysis that the SPSOM model provides a more realistic representation of the hyperconjugation network along the C5′−O5′−P−O3′−C3′ linkage. However, we have also shown that quantum mechanical investigations of this model system are nontrivial because of the complexity of the SPSOM conformational space. A comparison of the ab initio data with the ff99 potential energy surface clearly reveals an incorrect ff99 force-field description in the regions where the γ torsion is in the trans conformation. An explanation is proposed for why the α/γ flips are eliminated so successfully when the parmbsc0 force-field modification is used.

    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. You can change your affiliated institution below.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    The characteristics of the CH···O HBs, solvation free energies, NBO analysis results, SPSOM model-system charges, and geometries (xyz coordinates) of all the investigated conformations on the ff99, parmbsc0, B3LYP/6-31+G*, and MP2/6-31+G* PESs. 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

    This article is cited by 50 publications.

    1. Marie Zgarbová, Petr Jurečka, Pavel Banáš, Marek Havrila, Jiří Šponer, and Michal Otyepka . Noncanonical α/γ Backbone Conformations in RNA and the Accuracy of Their Description by the AMBER Force Field. The Journal of Physical Chemistry B 2017, 121 (11) , 2420-2433. https://doi.org/10.1021/acs.jpcb.7b00262
    2. Collins Nganou, Scott D. Kennedy, and David W. McCamant . Disagreement Between the Structure of the dTpT Thymine Pair Determined by NMR and Molecular Dynamics Simulations Using Amber 14 Force Fields. The Journal of Physical Chemistry B 2016, 120 (7) , 1250-1258. https://doi.org/10.1021/acs.jpcb.6b00191
    3. James C. Robertson and Thomas E Cheatham, III . DNA Backbone BI/BII Distribution and Dynamics in E2 Protein-Bound Environment Determined by Molecular Dynamics Simulations. The Journal of Physical Chemistry B 2015, 119 (44) , 14111-14119. https://doi.org/10.1021/acs.jpcb.5b08486
    4. Holger Kruse, Arnost Mladek, Konstantinos Gkionis, Andreas Hansen, Stefan Grimme, and Jiri Sponer . Quantum Chemical Benchmark Study on 46 RNA Backbone Families Using a Dinucleotide Unit. Journal of Chemical Theory and Computation 2015, 11 (10) , 4972-4991. https://doi.org/10.1021/acs.jctc.5b00515
    5. Arnošt Mládek, Pavel Banáš, Petr Jurečka, Michal Otyepka, Marie Zgarbová, and Jiří Šponer . Energies and 2′-Hydroxyl Group Orientations of RNA Backbone Conformations. Benchmark CCSD(T)/CBS Database, Electronic Analysis, and Assessment of DFT Methods and MD Simulations. Journal of Chemical Theory and Computation 2014, 10 (1) , 463-480. https://doi.org/10.1021/ct400837p
    6. Yi-Chao Zhang, Juan Liang, Peng Lian, Yiwen Han, Yifan Chen, Linquan Bai, Zhijun Wang, Jingdan Liang, Zixin Deng, and Yi-Lei Zhao . Theoretical Study on Steric Effects of DNA Phosphorothioation: B-Helical Destabilization in Rp-Phosphorothioated DNA. The Journal of Physical Chemistry B 2012, 116 (35) , 10639-10648. https://doi.org/10.1021/jp302494b
    7. Miroslav Krepl, Marie Zgarbová, Petr Stadlbauer, Michal Otyepka, Pavel Banáš, Jaroslav Koča, Thomas E. Cheatham, III, Petr Jurečka, and Jiří Šponer . Reference Simulations of Noncanonical Nucleic Acids with Different χ Variants of the AMBER Force Field: Quadruplex DNA, Quadruplex RNA, and Z-DNA. Journal of Chemical Theory and Computation 2012, 8 (7) , 2506-2520. https://doi.org/10.1021/ct300275s
    8. Karmen Condic-Jurkic, Ana-Sunčana Smith, Hendrik Zipse, and David M. Smith . The Protonation States of the Active-Site Histidines in (6–4) Photolyase. Journal of Chemical Theory and Computation 2012, 8 (3) , 1078-1091. https://doi.org/10.1021/ct2005648
    9. Arnošt Mládek, Judit E. Šponer, Petr Kulhánek, Xiang-Jun Lu, Wilma K. Olson, and Jiří Šponer . Understanding the Sequence Preference of Recurrent RNA Building Blocks Using Quantum Chemistry: The Intrastrand RNA Dinucleotide Platform. Journal of Chemical Theory and Computation 2012, 8 (1) , 335-347. https://doi.org/10.1021/ct200712b
    10. Andrea L. Millen, Breanne L. Kamenz, Fern M. V. Leavens, Richard A. Manderville, and Stacey D. Wetmore . Conformational Flexibility of C8-Phenoxylguanine Adducts in Deoxydinucleoside Monophosphates. The Journal of Physical Chemistry B 2011, 115 (44) , 12993-13002. https://doi.org/10.1021/jp2057332
    11. Marie Zgarbová, Michal Otyepka, Jiří Šponer, Arnošt Mládek, Pavel Banáš, Thomas E. Cheatham, III, and Petr Jurečka . Refinement of the Cornell et al. Nucleic Acids Force Field Based on Reference Quantum Chemical Calculations of Glycosidic Torsion Profiles. Journal of Chemical Theory and Computation 2011, 7 (9) , 2886-2902. https://doi.org/10.1021/ct200162x
    12. Arnošt Mládek, Jiří Šponer, Bobby G. Sumpter, Miguel Fuentes-Cabrera, and Judit E. Šponer . On the Geometry and Electronic Structure of the As-DNA Backbone. The Journal of Physical Chemistry Letters 2011, 2 (5) , 389-392. https://doi.org/10.1021/jz200015n
    13. Arnošt Mládek, Judit E. Šponer, Petr Jurečka, Pavel Banáš, Michal Otyepka, Daniel Svozil, and Jiří Šponer. Conformational Energies of DNA Sugar−Phosphate Backbone: Reference QM Calculations and a Comparison with Density Functional Theory and Molecular Mechanics. Journal of Chemical Theory and Computation 2010, 6 (12) , 3817-3835. https://doi.org/10.1021/ct1004593
    14. Jiří Šponer, Judit E. Šponer, Anton I. Petrov, and Neocles B. Leontis . Quantum Chemical Studies of Nucleic Acids: Can We Construct a Bridge to the RNA Structural Biology and Bioinformatics Communities?. The Journal of Physical Chemistry B 2010, 114 (48) , 15723-15741. https://doi.org/10.1021/jp104361m
    15. Andrea L. Millen, Richard A. Manderville and Stacey D. Wetmore . Conformational Flexibility of C8-Phenoxyl-2′-deoxyguanosine Nucleotide Adducts. The Journal of Physical Chemistry B 2010, 114 (12) , 4373-4382. https://doi.org/10.1021/jp911993f
    16. Mark A. Ditzler, Michal Otyepka, Jiřì Šponer and Nils G. Walter . Molecular Dynamics and Quantum Mechanics of RNA: Conformational and Chemical Change We Can Believe In. Accounts of Chemical Research 2010, 43 (1) , 40-47. https://doi.org/10.1021/ar900093g
    17. Daniel R. Roe and Anne M. Chaka. Structural Basis of Pathway-Dependent Force Profiles in Stretched DNA. The Journal of Physical Chemistry B 2009, 113 (46) , 15364-15371. https://doi.org/10.1021/jp906749j
    18. Eva Fadrná, Nad’a Špačková, Joanna Sarzyñska, Jaroslav Koča, Modesto Orozco, Thomas E. Cheatham, III, Tadeusz Kulinski and Jiří Šponer . Single Stranded Loops of Quadruplex DNA As Key Benchmark for Testing Nucleic Acids Force Fields. Journal of Chemical Theory and Computation 2009, 5 (9) , 2514-2530. https://doi.org/10.1021/ct900200k
    19. Alexander D. MacKerell, Jr.. Contribution of the Intrinsic Mechanical Energy of the Phosphodiester Linkage to the Relative Stability of the A, BI, and BII Forms of Duplex DNA. The Journal of Physical Chemistry B 2009, 113 (10) , 3235-3244. https://doi.org/10.1021/jp8102782
    20. Pablo Dans. Multiscale simulations of DNA from electrons to nucleosomes: 22 years of the Ascona B-DNA Consortium. Biophysical Reviews 2024, 87 https://doi.org/10.1007/s12551-024-01194-6
    21. Xuan Liu, Weifei Wang, Zexin Zhao, Long Xu, Bo Yang, Dongming Lan, Yonghua Wang. Monoacylglycerol lipase from marine Geobacillus sp. showing lysophospholipase activity and its application in efficient soybean oil degumming. Food Chemistry 2023, 406 , 134506. https://doi.org/10.1016/j.foodchem.2022.134506
    22. Po-Yu Ho, Tsu Yu Chou, Chuen Kam, Wenbin Huang, Zikai He, Alfonso H. W. Ngan, Sijie Chen. A dual organelle-targeting mechanosensitive probe. Science Advances 2023, 9 (2) https://doi.org/10.1126/sciadv.abn5390
    23. Mohit Chawla, Kanav Kalra, Zhen Cao, Luigi Cavallo, Romina Oliva. Occurrence and stability of anion–π interactions between phosphate and nucleobases in functional RNA molecules. Nucleic Acids Research 2022, 50 (20) , 11455-11469. https://doi.org/10.1093/nar/gkac1081
    24. Nathália Magalhães P. Rosa, Frederico Henrique do C. Ferreira, Nicholas P. Farrell, Luiz Antônio S. Costa. Substitution-inert polynuclear platinum complexes and Glycosaminoglycans: A molecular dynamics study of its non-covalent interactions. Journal of Inorganic Biochemistry 2022, 232 , 111811. https://doi.org/10.1016/j.jinorgbio.2022.111811
    25. Stephen Neidle, Mark Sanderson. The building blocks of DNA and RNA. 2022, 29-51. https://doi.org/10.1016/B978-0-12-819677-9.00004-4
    26. Leiqiang Han, Shuang Liang, Weiwei Mu, Zipeng Zhang, Limin Wang, Shumin Ouyang, Bufan Yao, Yongjun Liu, Na Zhang. Amphiphilic small molecular mates match hydrophobic drugs to form nanoassemblies based on drug-mate strategy. Asian Journal of Pharmaceutical Sciences 2022, 17 (1) , 129-138. https://doi.org/10.1016/j.ajps.2021.11.002
    27. Yongna Yuan, Matthew J. L. Mills, Zhuangzhuang Zhang, Yan Ma, Chunyan Zhao, Wei Su. A general RNA force field: comprehensive analysis of energy minima of molecular fragments of RNA. Journal of Molecular Modeling 2021, 27 (5) https://doi.org/10.1007/s00894-021-04746-9
    28. Nathália M. P. Rosa, Júlio A. F. Arvellos, Luiz Antônio S. Costa. Molecular dynamics simulation of non-covalent interactions between polynuclear platinum(II) complexes and DNA. JBIC Journal of Biological Inorganic Chemistry 2020, 25 (7) , 963-978. https://doi.org/10.1007/s00775-020-01817-9
    29. Si-Ming Liao, Nai-Kun Shen, Ge Liang, Bo Lu, Zhi-Long Lu, Li-Xin Peng, Feng Zhou, Li-Qin Du, Yu-Tuo Wei, Guo-Ping Zhou, Ri-Bo Huang. Inhibition of α-amylase Activity by Zn 2+ : Insights from Spectroscopy and Molecular Dynamics Simulations. Medicinal Chemistry 2019, 15 (5) , 510-520. https://doi.org/10.2174/1573406415666181217114101
    30. Atul Rangadurai, Huiqing Zhou, Dawn K Merriman, Nathalie Meiser, Bei Liu, Honglue Shi, Eric S Szymanski, Hashim M Al-Hashimi. Why are Hoogsteen base pairs energetically disfavored in A-RNA compared to B-DNA?. Nucleic Acids Research 2018, 11 https://doi.org/10.1093/nar/gky885
    31. Rodrigo Galindo-Murillo, Daniel R. Roe, Thomas E. Cheatham. Convergence and reproducibility in molecular dynamics simulations of the DNA duplex d(GCACGAACGAACGAACGC). Biochimica et Biophysica Acta (BBA) - General Subjects 2015, 1850 (5) , 1041-1058. https://doi.org/10.1016/j.bbagen.2014.09.007
    32. Holger Kruse, Jiří Šponer. Towards biochemically relevant QM computations on nucleic acids: controlled electronic structure geometry optimization of nucleic acid structural motifs using penalty restraint functions. Physical Chemistry Chemical Physics 2015, 17 (2) , 1399-1410. https://doi.org/10.1039/C4CP04680C
    33. Alexey Savelyev, Alexander D. MacKerell. All‐atom polarizable force field for DNA based on the classical drude oscillator model. Journal of Computational Chemistry 2014, 35 (16) , 1219-1239. https://doi.org/10.1002/jcc.23611
    34. Valeri Poltev, Victor M. Anisimov, Victor I. Danilov, Dolores Garcia, Carolina Sanchez, Alexandra Deriabina, Eduardo Gonzalez, Francisco Rivas, Nina Polteva. The role of molecular structure of sugar‐phosphate backbone and nucleic acid bases in the formation of single‐stranded and double‐stranded DNA structures. Biopolymers 2014, 101 (6) , 640-650. https://doi.org/10.1002/bip.22432
    35. Rodrigo Galindo‐Murillo, Christina Bergonzo, Thomas E. Cheatham. Molecular Modeling of Nucleic Acid Structure: Setup and Analysis. Current Protocols in Nucleic Acid Chemistry 2014, 56 (1) https://doi.org/10.1002/0471142700.nc0710s56
    36. Thomas E. Cheatham, David A. Case. Twenty‐five years of nucleic acid simulations. Biopolymers 2013, 99 (12) , 969-977. https://doi.org/10.1002/bip.22331
    37. Arnošt Mládek, Miroslav Krepl, Daniel Svozil, Petr Čech, Michal Otyepka, Pavel Banáš, Marie Zgarbová, Petr Jurečka, Jiří Šponer. Benchmark quantum-chemical calculations on a complete set of rotameric families of the DNA sugar–phosphate backbone and their comparison with modern density functional theory. Physical Chemistry Chemical Physics 2013, 15 (19) , 7295. https://doi.org/10.1039/c3cp44383c
    38. Jonathan M. Fogg, Graham L. Randall, B. Montgomery Pettitt, De Witt L. Sumners, Sarah A. Harris, Lynn Zechiedrich. Bullied no more: when and how DNA shoves proteins around. Quarterly Reviews of Biophysics 2012, 45 (3) , 257-299. https://doi.org/10.1017/S0033583512000054
    39. David L Beveridge, Thomas E Cheatham, Mihaly Mezei. The ABCs of molecular dynamics simulations on B-DNA, circa 2012. Journal of Biosciences 2012, 37 (3) , 379-397. https://doi.org/10.1007/s12038-012-9222-6
    40. J. Šponer, M. Otyepka, P. Banáš, K. Réblová, N. G. Walter. Molecular Dynamics Simulations of RNA Molecules. 2012, 129-155. https://doi.org/10.1039/9781849735056-00129
    41. Jiří Šponer, Arnošt Mládek, Judit E. Šponer, Daniel Svozil, Marie Zgarbová, Pavel Banáš, Petr Jurečka, Michal Otyepka. The DNA and RNA sugar–phosphate backbone emerges as the key player. An overview of quantum-chemical, structural biology and simulation studies. Physical Chemistry Chemical Physics 2012, 14 (44) , 15257. https://doi.org/10.1039/c2cp41987d
    42. Tymofii Yu. Nikolaienko, Leonid A. Bulavin, Dmytro M. Hovorun. Structural flexibility of DNA-like conformers of canonical 2′-deoxyribonucleosides. Physical Chemistry Chemical Physics 2012, 14 (44) , 15554. https://doi.org/10.1039/c2cp43120c
    43. Cassandra D. M. Churchill, Stacey D. Wetmore. Developing a computational model that accurately reproduces the structural features of a dinucleoside monophosphate unit within B-DNA. Physical Chemistry Chemical Physics 2011, 13 (36) , 16373. https://doi.org/10.1039/c1cp21689a
    44. Valeri I. Poltev, Victor M. Anisimov, Victor I. Danilov, Tanja van Mourik, Alexandra Deriabina, Eduardo González, Maria Padua, Dolores Garcia, Francisco Rivas, Nina Polteva. DFT study of polymorphism of the DNA double helix at the level of dinucleoside monophosphates. International Journal of Quantum Chemistry 2010, 110 (13) , 2548-2559. https://doi.org/10.1002/qua.22748
    45. Martin Kabeláč, Filip Zimandl, Tomáš Fessl, Zdeněk Chval, Filip Lankaš. A comparative study of the binding of QSY 21 and Rhodamine 6G fluorescence probes to DNA: structure and dynamics. Physical Chemistry Chemical Physics 2010, 12 (33) , 9677. https://doi.org/10.1039/c004020g
    46. Stéphane Téletchéa, Tormod Skauge, Einar Sletten, Jiří Kozelka. Cisplatin Adducts on a GGG Sequence within a DNA Duplex Studied by NMR Spectroscopy and Molecular Dynamics Simulations. Chemistry – A European Journal 2009, 15 (45) , 12320-12337. https://doi.org/10.1002/chem.200901158
    47. Valery I. Poltev, Victor M. Anisimov, Victor I. Danilov, Alexandra Deriabina, Eduardo Gonzalez, Dolores Garcia, Francisco Rivas, Agata Jurkiewicz, Andrzej Leś, Nina Polteva. DFT study of minimal fragments of nucleic acid single chain for explication of sequence dependence of DNA duplex conformation. Journal of Molecular Structure: THEOCHEM 2009, 912 (1-3) , 53-59. https://doi.org/10.1016/j.theochem.2009.03.022
    48. Fang-Fang Wang, Li-Dong Gong, Dong-Xia Zhao. Studies on the torsions of nucleic acids using ABEEMσπ/MM method. Journal of Molecular Structure: THEOCHEM 2009, 909 (1-3) , 49-56. https://doi.org/10.1016/j.theochem.2009.05.019
    49. Jeremy Curuksu, Martin Zacharias. Enhanced conformational sampling of nucleic acids by a new Hamiltonian replica exchange molecular dynamics approach. The Journal of Chemical Physics 2009, 130 (10) https://doi.org/10.1063/1.3086832
    50. Jonathan M. Fogg, Daniel J. Catanese, Graham L. Randall, Michelle C. Swick, Lynn Zechiedrich. Differences Between Positively and Negatively Supercoiled DNA that Topoisomerases May Distinguish. 2009, 73-121. https://doi.org/10.1007/978-1-4419-0670-0_5

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect