Quantum-mechanical survey of the novel conformational and tautomeric transformations of the classical Watson-Crick А·Т(WC), reverse Watson-Crick А·Т(rWC), Hoogsteen А·Т(Н) and reverse Hoogsteen А·Т(rН) DNA base pairs

Chemistry & Chemical Technology
Proceedings of the 8th International Youth Science Forum "Litteris et Artibus", November 22–24, 2018, Lviv: Lviv Polytechnic National University, 2018, pp. 136–150

Authors

First and Last Name Academic degree E-mail Affiliation
Ol’ha Brovarets’ Sc.D. o.o.brovarets [at] gmail.com Department of Molecular and Quantum Biophysics, Institute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine; Department of Molecular Biotechnology and Bioinformatics, Institute of High Technologies, Taras Shevchenko National University of Kyiv; Department of Pharmacology, Bogomolets National Medical University
Kyiv, Ukraine
Kostiantyn Tsiupa Sc.D. o.o.brovarets [at] gmail.com Department of Molecular and Quantum Biophysics, Institute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine
Kyiv, Ukraine
Andrii Dinets Ph.D. andrii.dinets [at] gmail.com Department of Pharmacology, Bogomolets National Medical University
Kyiv, Ukraine
Dmytro Hovorun Sc.D. d.m.hovorun [at] imbg.org.ua Department of Molecular and Quantum Biophysics, Institute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine; Department of Molecular Biotechnology and Bioinformatics, Institute of High Technologies, Taras Shevchenko National University of Kyiv; Department of Pathophysiology, Bogomolets National Medical University
Kyiv, Ukraine

I and my co-authors (if any) authorize the use of the Paper in accordance with the Creative Commons CC BY license

First published on this website: 07.11.2018 - 14:42
Abstract

This study represents novel and previously unknown conformational and tautomeric transformations of the classical Watson-Crick А·Т DNA base pairs – Watson-Crick А·Т(WC), reverse Watson-Crick А·Т(rWC), Hoogsteen А·Т(Н) and reverse Hoogsteen А·Т(rН), leading to the novel, non-planar conformations or tautomers of these base pairs.

References

[1]  J. Donohue and  K.N. Trueblood. “Base pairing in DNA,” J. Mol. Biol., vol. 2, 1960, pp. 363–371.

[2]  N.A. Tchurikov et al., “Parallel DNA: Generation of a duplex between two Drosophila sequences in vitro”. FEBS Lett., vol. 257, 1989, pp.415–418.

[3]  E. Cubero, F.J. Luque and M. Orozco, “Theoretical studies of d(A:T)-based parallel-stranded DNA duplexes,” J. Am. Chem. Soc., vol. 123, 2001, pp. 12018–12025.

[4]  V.R. Parvathy et al., “NMR structure of a parallel-stranded DNA duplex at atomic resolution,” Nucleic Acids Res., vol. 30, 2002, pp. 1500–1511.

[5]  V.I. Poltev, “Analysis of the conformational features of Watson–Crick duplex fragments by molecular mechanics and quantum mechanics methods,” Biophysics, vol. 61, 2016, pp. 217-226.

[6]  M.Y. Ye et al., “Adaptively recognizing parallel-stranded duplex structure for fluorescent DNA polarity analysis,” Anal. Chem., vol. 89, 2017, pp. 8604-8608. 

[7]  M. Szabat and R. Kierzek, “Parallel stranded DNA and RNA duplexes: structural features and potential applications,” FEBS J., vol. 284, 2017, pp. 3986-3998. 

[8]  O.O. Brovarets',  “Under what conditions does G·C Watson-Crick DNA base pair acquire all four configurations characteristic for A·T Watson-Crick DNA base pair,” Ukr. Biochem. J., vol. 85, 2013, pp. 98-103.

[9]  O.O. Brovarets',  “Structural and energetic properties of the four configurations of the A·T and G·C DNA base pairs,” Ukr. Biochem. J., vol. 85, 2013, pp. 104-110.

[10]  K. Hoogsteen, “The crystal and molecular structure of a hydrogenbonded complex between 1-methylthymine and 9-methyladenine,” Acta Cryst., vol. 16, 1963, pp. 907–916. 

[11]  N.G. Abrescia et al., “Crystal structure of an antiparallel DNA fragment with Hoogsteen base pairing,” Proc. Natl. Acad. Sci. USA, vol. 99, 2002, pp. 2806–2811.

[12]  N.G. Abrescia et al., “X-ray and NMR studies of the DNA oligomer d(ATATAT): Hoogsteen base pairing in duplex DNA,” Biochemistry, vol. 43, 2004, pp. 4092–4100.

[13]  J. Pous et al., “Stabilization by extra-helical thymines of a DNA duplex with Hoogsteen base pairs,” J. Am. Chem. Soc., vol. 130, 2008, pp. 6755–6760.

[14]  L. Campos et al., “Overview of the structure of allAT oligonucleotides: organization in helices and packing interactions,” Biophys. J., vol. 91, 2006, pp. 892–903.

[15]  E.N. Nikolova et al., “A historical account of Hoogsteen base-pairs in duplex DNA,” Biopolymers, vol. 99, 2014, pp. 955-968.

[16]  H.S. Alvey et al.,. “Widespread transient Hoogsteen base-pairs in canonical duplex DNA with variable energetics,” Nature Comm., vol. 5, 2014, pp. 4786-4794.

[17]  F.J. Acosta-Reyes et al., “Structure of the DNA duplex d(ATTAAT)2 with Hoogsteen hydrogen bonds,” PLoS One, vol. 10, 17 March 2015. [Online]. Available: PLoS One, https://doi.org/10.1371/journal.pone.0120241 [Accessed: 1 Sep 2018].

[18]  C. Yang, E. Kim and Y. Pak, “Free energy landscape and transition pathways from Watson–Crick to Hoogsteen base pairing in free duplex DNA,” Nucleic Acids Res., vol. 43, 2015, pp. 7769-7778. 

[19]  H.  Zhou, Occurrence and function of Hoogsteen base pairs in nucleic acids. PhD Thesis: Department of Biochemistry, Duke University, 2016.

[20]  B. Sathyamoorthy et al., “Insights into Watson–Crick/Hoogsteen breathing dynamics and damage repair from the solution structure and dynamic ensemble of DNA duplexes containing m1A,” Nucleic Acids Res., vol. 45, 2017, pp. 5586-5601.

[21]  A.E.V.  Haschemeyer and H.M. Sobell, ”The crystal structure of an intermolecular nucleoside complex: Adenosine and 5-bromouridine,” Proc. Natl Acad. Sci. USA, vol. 50, 1963, pp. 872–877.

[22]  J. Sühnel, ”Beyond nucleic acid base pairs: From triads to heptads,” Biopolymers, vol. 61, 2002, pp. 32–51. 

[23]  E.I. Zagryadskaya, F.R. Doyon and S.V. Steinberg, “Importance of the reverse Hoogsteen base pair 54–58 for tRNA function,” Nucleic Acids Res., vol. 31, 2003, pp. 3946–3953. 

[24]  K. Liu et al., “A novel DNA duplex. A parallel-stranded DNA helix with Hoogsteen base pairing,” Biochemistry, vol. 2, 1993, pp. 11802-11809. 

[25]  P. von Hippel, N.P. Johnson and A.H.  Marcus, “Fifty years of DNA “breathing”: reflections on old and new approaches,” Biopolymers, 99 (12), 2013, pp. 923–954.

[26]  M. Frank-Kamenetskii and S. Prakash, “Fluctuations in the DNA double helix: a critical review,” Phys. Life Rev., Vol. 11, Iss. 2, 2014, pp. 153-170.

[27]  D. Chakraborty and D.J. Wales, “Energy landscape and pathways for transitions between Watson-Crick and Hoogsteen base pairing in DNA,” J. Phys. Chem. Lett., vol. 9, 2018,

pp. 229-241.

[28]  O.O. Brovarets’, K.S. Tsiupa and D.M. Hovorun, “Surprising conformers of the biologically important A·T DNA base pairs: QM/QTAIM proofs,” Front. Chem, 27 Feb 2018. [Online]. Available: Front. Chem., doi: 10.3389/fchem.2018.00008 [Accessed: 1 Sep 2018].

[29]  O.O. Brovarets’, K.S. Tsiupa and D.M. Hovorun, “Non-dissociative structural transitions of the Watson-Crick and reverse Watson-Crick А·Т DNA base pairs into the Hoogsteen and reverse Hoogsteen forms,” Sci. Rept, vol. 8, 10 July 2018. [Online]. Available: Nature, https://doi.org/10.1038/s41598-018-28636-y [Accessed: 1 Sep 2018].

[30]  O.O. Brovarets’, K.S. Tsiupa and D.M. Hovorun, “Unexpected A·T(WC)↔A·T(rWC)/A·T(rH) and A·T(H)↔A·T(rH)/A·T(rWC) conformational transitions between the classical A·T DNA base pairs: A QM/QTAIM comprehensive study”. Int. J. Quantum. Chem, vol. 118, 10 April 2018. [Online]. Available: RSC Advances, doi: 10.1039/C8RA01446A [Accessed: 1 Sep 2018].

[31]  O.O. Brovarets’ et al., “Unexpected routes of the mutagenic tautomerization of the T nucleobase in the classical A·T DNA base pairs: A QM/QTAIM comprehensive view”. Front. Chem., 2018. [Online]. Available: Front. Chem., doi: 10.3389/fchem.2018.00532 [Accessed: 1 Oct 2018].

[32]  J. Tirado-Rives and W.L. Jorgensen, “Performance of B3LYP Density Functional Methods for a large set of organic molecules,” J. Chem. Theory Comput., vol. 4, 2008, pp. 297–306. 

[33]  R.G. Parr and W. Yang, Density-functional theory of atoms and molecules. Oxford: Oxford University Press, 1989.

[34]  C. Lee, W. Yang and R.G. Parr, “Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density,” Phys. Rev. B., vol. 37, 1988, pp. 785-789. 

[35]  P.C. Hariharan and J.A Pople, “The influence of polarization functions on molecular orbital hydrogenation energies,” Theor. Chim. Acta, vol. 28, 1973, pp. 213−222. 

[36]  R. Krishnan et al., “Self‐consistent molecular orbital methods. XX. A basis set for correlated wave functions,” J. Chem. Phys., vol. 72, 1980, pp. 650−654.

[37]  M.J. Frisch at al., GAUSSIAN 09 (Revision B.01). Wallingford CT: Gaussian Inc, 2010.

[38]  C.F. Matta, “How dependent are molecular and atomic properties on the electronic structure method? Comparison of Hartree-Fock, DFT, and MP2 on a biologically relevant set of molecules,” J. Comput. Chem., vol. 31, 2010, pp. 1297–1311.

[39]  O.O. Brovarets’ and D.M. Hovorun, “Quantum-chemical investigation of tautomerization ways of Watson-Crick DNA base pair guanine-cytosine,” Ukr. Biochem. J., vol. 82, 2010, pp. 55-60. 

[40]  O.O. Brovarets’ and D.M. Hovorun, “Quantum-chemical investigation of the elementary molecular mechanisms of pyrimidine·purine transversions,” Ukr. Biochem. J., vol. 82, 2010, pp. 57-67.

[41]  O.O. Brovarets’ and D.M. Hovorun, “How the long G·G* Watson-Crick DNA base mispair comprising keto and enol tautomers of the guanine tautomerises? The results of the QM/QTAIM investigation,” Phys. Chem. Chem. Phys., vol. 6, 2014, pp. 15886-15899. 

[42]  O.O. Brovarets’ and D.M. Hovorun, “The nature of the transition mismatches with Watson-Crick architecture: the G*·T or G·T* DNA base mispair or both? A QM/QTAIM perspective for the biological problem,” J. Biomol. Struct. & Dynam., vol. 33, 2015, pp. 925-945. 

[43]  O.O. Brovarets', R.O. Zhurakivsky and D.M. Hovorun, “DPT tautomerisation of the wobble guanine·thymine DNA base mispair is not mutagenic: QM and QTAIM arguments,” J. Biomol. Struct. & Dynam., vol. 33, 2015, pp. 674-689.

[44]  M.A. Palafox, “Molecular structure differences between the antiviral nucleoside analogue 5-iodo-2`-deoxyuridine and the natural nucleoside 2`-deoxythymidine using MP2 and DFT methods: conformational analysis, crystal simulations, DNA pairs and possible behavior,” J. Biomol. Struct. & Dynam., vol. 32, 2014, pp. 831–851. 

[45]  A.A. El-Sayed et al., “Conformational analysis of the anti-HIV Nikavir prodrug: comparisons with AZT and thymidine, and establishment of structure-activity relationships/tendencies in other 6`-derivatives,” J. Biomol. Struct. & Dynam., vol. 33, 2015, pp. 723–748.

[46]  C. Peng et al., “Using redundant internal coordinates to optimize equilibrium geometries and transition states,” J. Comput. Chem., vol. 17, 1996, pp. 49–56. 

[47]  P.W.  Atkins. Physical chemistry. Oxford: Oxford University Press, 1998.

[48]  M.J. Frisch, M. Head-Gordon and J.A. Pople, “Semi-direct algorithms for the MP2 energy and gradient,” Chem. Phys. Lett., vol. 166, 1990, pp. 281-289.

[49]  R.A. Kendall, Jr., T.H. Dunning and R.J. Harrison, “Electron affinities of the first-row atoms revisited. Systematic basis sets and wave functions,” J. Chem. Phys., vol. 96, 1992, pp. 6796−6806.

[50]  S.F. Boys and F. Bernardi. “The calculation of small molecular interactions by the differences of separate total energies. Some procedures with reduced errors,” Mol. Phys., vol. 19, 1970, pp. 553–566. 

[51]  M. Gutowski et al., “The basis set superposition error in correlated electronic structure calculations,” Chem. Phys. Lett., vol. 124, 1986, pp. 370–375. 

[52]  J.A. Sordo, S. Chin and T.L. Sordo, “On the counterpoise correction for the basis set superposition error in large systems,” Theor. Chim. Acta, vol. 74, 1988, pp. 101–110. 

[53]  J.A. Sordo, “On the use of the Boys–Bernardi function counterpoise procedure to correct barrier heights for basis set superposition error,” J. Mol. Struct., vol. 537, 2001, pp. 245–251. 

[54]  R.F.W. Bader. Atoms in molecules: A quantum theory. Oxford: Oxford University Press, 1990.

[55]  C.F. Matta and J. Hernández-Trujillo, “Bonding in polycyclic aromatic hydrocarbons in terms of the electron density and of electron delocalization,” J. Phys. Chem. A, vol. 107, 2003, pp. 7496-7504.

[56]  C.F. Matta, N. Castillo and R.J. Boy, “Atomic contributions to bond dissociation energies in aliphatic hydrocarbons,” J. Chem. Phys., vol. 125, 204103 (2006). [Online]. Available: AIP, https://doi.org/10.1063/1.2378720 [Accessed: 1 Oct 2018].

[57]  C.F. Matta, “Modeling biophysical and biological properties from the characteristics of the molecular electron density, electron localization and delocalization matrices, and the electrostatic potential,” J. Comput. Chem., vol. 35, 2014, pp.1165-1198.

[58]  C. Lecomte, E. Esinosa and C.F. Matta, “On atom–atom ‘short contact’ bonding interactions in crystals,” IUCrJ, vol. 2, 2015, pp. 161–163.

[59]  T.A. Keith, AIMAll (Version 10.07.01), 2010. [Online]. Available: http://aim.tkgristmill.com [Accessed: 1 Nov 2010].

[60]  C.F. Matta, N. Castillo and R.J. Boyd, “Extended weak bonding interactions in DNA: π-stacking (base-base), base-backbone, and backbone-backbone interactions,” J. Phys. Chem. B, vol. 110, 2006, pp. 563-578.

[61]  O.O. Brovarets’, R.O. Zhurakivsky and D.M. Hovorun, “Is the DPT tautomerisation of the long A·G Watson-Crick DNA base mispair a source of the adenine and guanine mutagenic tautomers? A QM and QTAIM response to the biologically important question,” J. Comput. Chem., vol. 35, 2014, pp. 451-466. 

[62]  O.O. Brovarets’ and D.M. Hovorun, “DPT tautomerisation of the G·Asyn and A*·G*syn DNA mismatches: A QM/QTAIM combined atomistic investigation,” Phys. Chem. Chem. Phys., vol. 16, 2014, pp. 9074-9085. 

[63]  O.O. Brovarets’ and D.M. Hovorun, “Tautomeric transition between wobble А·С DNA base mispair and Watson-Crick-like A·C* mismatch: miscrostructural mechanism and biological significance,” Phys. Chem. Chem. Phys., vol. 17, 2015, pp. 15103–15110. 

[64]  C.F. Matta and R.J. Boyd, Eds., The Quantum Theory of Atoms in Molecules: from solid state to DNA and drug design. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA, 2007. 

[65]  A.V. Iogansen, “Direct proportionality of the hydrogen bonding energy and the intensification of the stretching ν(XH) vibration in infrared spectra,” Spectrochim. Acta Part A: Mol. Biomol. Spectrosc., vol. 55, 1999, pp. 1585–1612.

[66]  O.O. Brovarets’, R.O. Zhurakivsky and D.M. Hovorun, “The physico-chemical mechanism of the tautomerisation via the DPT of the long Hyp*·Hyp Watson-Crick base pair containing rare tautomer: a QM and QTAIM detailed look,” Chem. Phys. Lett., vol. 578, 2013, pp. 126–132.

[67]  O.O. Brovarets’ and D.M. Hovorun, “Does the G·G*syn DNA mismatch containing canonical and rare tautomers of the guanine tautomerise through the DPT? A QM/QTAIM microstructural study,” Mol. Phys., vol. 112, 27 June 2014. [Online]. Available: Taylor & Francis Online, https://doi.org/10.1080/00268976.2014.927079 [Accessed: 1 Oct 2018].

[68]  O.O. Brovarets’ et al., “A QM/QTAIM research under the magnifying glass of the DPT tautomerisation of the wobble mispairs involving 2-aminopurine,” New J. Chem., vol. 41, 2017, pp. 7232-7243. 

[69]  O.O. Brovarets’, I.S. Voiteshenko and D.M. Hovorun, “Physico-chemical profiles of the wobble↔Watson-Crick G*·2AP(w)↔G·2AP(WC) and A·2AP(w)↔A*·2AP(WC) tautomerisations: a QM/QTAIM comprehensive survey,” Phys. Chem. Chem. Phys., vol. 20, 2017, pp. 623-636. 

[70]  O.O. Brovarets' and D.M. Hovorun, “A novel conception for spontaneous transversions caused by homo-pyrimidine DNA mismatches: a QM/QTAIM highlight,” Phys. Chem. Chem. Phys., vol. 17, 2015, pp. 21381-21388. 

[71]  W. Saenger. Principles of nucleic acid structure. New York: Springer, 1984.

[72]  O.O. Brovarets' and D.M. Hovorun, “New structural hypostases of the A·T and G·C Watson-Crick DNA base pairs caused by their mutagenic tautomerisation in a wobble manner: a QM/QTAIM prediction,” RSС Adv., vol. 5, 2015, pp. 99594-99605. 

[73]  O.O. Brovarets' and D.M. Hovorun, “How many tautomerisation pathways connect Watson-Crick-like G*·T DNA base mispair and wobble mismatches?” J. Biomol. Struct. & Dynam., vol. 33, 2015, pp. 2297-2315. 

[74]  O.O. Brovarets', R.O. Zhurakivsky and D.M. Hovorun, “DPT tautomerisation of the wobble guanine·thymine DNA base mispair is not mutagenic: QM and QTAIM arguments,” J. Biomol. Struct. & Dynam., vol. 33, 2015, pp. 674-689.

[75]  O.O. Brovarets', R.O. Zhurakivsky and D.M. Hovorun. “Structural, energetic and tautomeric properties of the T·T*/T*·T DNA mismatch involving mutagenic tautomer of thymine: a QM and QTAIM insight,” Chem. Phys. Lett., vol. 592, 2014, pp. 247-255. 

Official paper

Comments

Secretary CCT
researcher, secretary

Dear autors,

Your paper has been accepted!

We are glad to inform you that your conference paper has been accepted to participate in the 8th International Joint Youth Science Forum «Litteris et Artibus» & 13th International Conference «Young Scientists Towards the Challenges of Modern Technology», particularly in «Chemistry & Chemical Technology» (CCT) conference (November 22-24, 2018, Lviv, Ukraine)! Your paper will be published in digital proceedings with ISSN and DOI on the website https://openreviewhub.org/lea-2018.

Please, answer the following participation questions:

•   Are you going to take part in the conference in person?

•   Do you require official invitation letter from Lviv Polytechnic? (The invitation letter will be scanned and sent to your e-mail).

Presentation delivery regulations:

Conference participants will present their work on posters. Content and design of posters is arbitrary, but it should include the basic provisions of your paper: authors names, title, main points, equations, figures etc. as well as exclude solid color, gradient or other costly to print backgrounds. The poster's upper part may include some information about your organization (title and logo, brief contact information).

Selected papers will be presented orally.

Looking forward to receiving your poster! See you in Lviv soon!

Best regards,

Oksana Orobchuk,

Secretary CCT

Thu, 11/15/2018 - 00:02