Structure of the DNA Duplex D(ATTAAT)2 with Hoogsteen Hydrogen Bonds

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2015 Mar 18

PMID 25781995

Citations 14

Authors

Francisco J Acosta-Reyes

Elida Alechaga

Juan A Subirana

J Lourdes Campos

Affiliations

Soon will be listed here.

Abstract

The traditional Watson-Crick base pairs in DNA may occasionally adopt a Hoogsteen conformation, with a different organization of hydrogen bonds. Previous crystal structures have shown that the Hoogsteen conformation is favored in alternating AT sequences of DNA. Here we present new data for a different sequence, d(ATTAAT)2, which is also found in the Hoogsteen conformation. Thus we demonstrate that other all-AT sequences of DNA with a different sequence may be found in the Hoogsteen conformation. We conclude that any all-AT sequence might acquire this conformation under appropriate conditions. We also compare the detailed features of DNA in either the Hoogsteen or Watson-Crick conformations.

Citing Articles

Experimental detection of conformational transitions between forms of DNA: problems and prospects.

Zubova E, Strelnikov I Biophys Rev. 2023; 15(5):1053-1078.

PMID: 37974981 PMC: 10643659. DOI: 10.1007/s12551-023-01143-9.

Sequence dependence of transient Hoogsteen base pairing in DNA.

Perez de Alba Ortiz A, Vreede J, Ensing B PLoS Comput Biol. 2022; 18(5):e1010113.

PMID: 35617357 PMC: 9177043. DOI: 10.1371/journal.pcbi.1010113.

The A·T(rWC)/A·T(H)/A·T(rH) ↔ A·T*(rw)/A·T*(w)/A·T*(rw) mutagenic tautomerization sequential proton transfer: a QM/QTAIM study.

Brovarets O, Tsiupa K, Hovorun D RSC Adv. 2022; 8(24):13433-13445.

PMID: 35542561 PMC: 9079753. DOI: 10.1039/c8ra01446a.

Probing the Hydrogen-Bonding Environment of Individual Bases in DNA Duplexes with Isotope-Edited Infrared Spectroscopy.

Fick R, Liu A, Nussbaumer F, Kreutz C, Rangadurai A, Xu Y J Phys Chem B. 2021; 125(28):7613-7627.

PMID: 34236202 PMC: 8311644. DOI: 10.1021/acs.jpcb.1c01351.

Slow motions in A·T rich DNA sequence.

Ben Imeddourene A, Zargarian L, Buckle M, Hartmann B, Mauffret O Sci Rep. 2020; 10(1):19005.

PMID: 33149183 PMC: 7642443. DOI: 10.1038/s41598-020-75645-x.

References

Abrescia N, Thompson A, Huynh-Dinh T, Subirana J . Crystal structure of an antiparallel DNA fragment with Hoogsteen base pairing. Proc Natl Acad Sci U S A. 2002; 99(5):2806-11. PMC: 122429. DOI: 10.1073/pnas.052675499. View

Sehgal N, Fritz A, Morris K, Torres I, Chen Z, Xu J . Gene density and chromosome territory shape. Chromosoma. 2014; 123(5):499-513. PMC: 5726871. DOI: 10.1007/s00412-014-0480-y. View

Yakovchuk P, Protozanova E, Frank-Kamenetskii M . Base-stacking and base-pairing contributions into thermal stability of the DNA double helix. Nucleic Acids Res. 2006; 34(2):564-74. PMC: 1360284. DOI: 10.1093/nar/gkj454. View

McCoy A, Grosse-Kunstleve R, Adams P, Winn M, Storoni L, Read R . Phaser crystallographic software. J Appl Crystallogr. 2009; 40(Pt 4):658-674. PMC: 2483472. DOI: 10.1107/S0021889807021206. View

Kirouac K, Ling H . Structural basis of error-prone replication and stalling at a thymine base by human DNA polymerase iota. EMBO J. 2009; 28(11):1644-54. PMC: 2693154. DOI: 10.1038/emboj.2009.122. View

Nair D, Johnson R, Prakash S, Prakash L, Aggarwal A . Replication by human DNA polymerase-iota occurs by Hoogsteen base-pairing. Nature. 2004; 430(6997):377-80. DOI: 10.1038/nature02692. View

Campos L, Valls N, Urpi L, Gouyette C, Sanmartin T, Richter M . Overview of the structure of all-AT oligonucleotides: organization in helices and packing interactions. Biophys J. 2006; 91(3):892-903. PMC: 1563779. DOI: 10.1529/biophysj.106.084210. View

Pous J, Urpi L, Subirana J, Gouyette C, Navaza J, Campos J . Stabilization by extra-helical thymines of a DNA duplex with Hoogsteen base pairs. J Am Chem Soc. 2008; 130(21):6755-60. DOI: 10.1021/ja078022+. View

Nikolova E, Kim E, Wise A, OBrien P, Andricioaei I, Al-Hashimi H . Transient Hoogsteen base pairs in canonical duplex DNA. Nature. 2011; 470(7335):498-502. PMC: 3074620. DOI: 10.1038/nature09775. View

10.

Abrescia N, Gonzalez C, Gouyette C, Subirana J . X-ray and NMR studies of the DNA oligomer d(ATATAT): Hoogsteen base pairing in duplex DNA. Biochemistry. 2004; 43(14):4092-100. DOI: 10.1021/bi0355140. View

11.

Moreno T, Pous J, Subirana J, Campos J . Coiled-coil conformation of a pentamidine-DNA complex. Acta Crystallogr D Biol Crystallogr. 2010; 66(Pt 3):251-7. DOI: 10.1107/S0907444909055693. View

12.

Cubero E, Abrescia N, Subirana J, Luque F, Orozco M . Theoretical study of a new DNA structure: the antiparallel Hoogsteen duplex. J Am Chem Soc. 2003; 125(47):14603-12. DOI: 10.1021/ja035918f. View

13.

Subirana J, Messeguer X . The distribution of alternating AT sequences in eukaryotic genomes suggests a role in homologous chromosome recognition in meiosis. J Theor Biol. 2011; 283(1):28-34. DOI: 10.1016/j.jtbi.2011.05.025. View

14.

Pfoh R, Cuesta-Seijo J, Sheldrick G . Interaction of an echinomycin-DNA complex with manganese ions. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2009; 65(Pt 7):660-4. PMC: 2705629. DOI: 10.1107/S1744309109019654. View

15.

Nikolova E, Zhou H, Gottardo F, Alvey H, Kimsey I, Al-Hashimi H . A historical account of Hoogsteen base-pairs in duplex DNA. Biopolymers. 2013; 99(12):955-68. PMC: 3844552. DOI: 10.1002/bip.22334. View

16.

Murshudov G, Skubak P, Lebedev A, Pannu N, Steiner R, Nicholls R . REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr. 2011; 67(Pt 4):355-67. PMC: 3069751. DOI: 10.1107/S0907444911001314. View

17.

Yang W . An overview of Y-Family DNA polymerases and a case study of human DNA polymerase η. Biochemistry. 2014; 53(17):2793-803. PMC: 4018060. DOI: 10.1021/bi500019s. View

18.

Nair D, Johnson R, Prakash L, Prakash S, Aggarwal A . Human DNA polymerase iota incorporates dCTP opposite template G via a G.C + Hoogsteen base pair. Structure. 2005; 13(10):1569-77. DOI: 10.1016/j.str.2005.08.010. View

19.

Nikolova E, Gottardo F, Al-Hashimi H . Probing transient Hoogsteen hydrogen bonds in canonical duplex DNA using NMR relaxation dispersion and single-atom substitution. J Am Chem Soc. 2012; 134(8):3667-70. PMC: 3791138. DOI: 10.1021/ja2117816. View

20.

Lu X, Olson W . 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res. 2003; 31(17):5108-21. PMC: 212791. DOI: 10.1093/nar/gkg680. View