An intercalation-locked parallel-stranded DNA tetraplex

Tripathi, S.; Zhang, D.; Paukstelis, P. J.

doi:10.1093/nar/gkv033

An intercalation-locked parallel-stranded DNA tetraplex

Journal Article · Mon Jan 26 23:00:00 EST 2015 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkv033· OSTI ID:1171850

Tripathi, S.; Zhang, D.; Paukstelis, P. J.

DNA has proved to be an excellent material for nanoscale construction because complementary DNA duplexes are programmable and structurally predictable. However, in the absence of Watson–Crick pairings, DNA can be structurally more diverse. Here, we describe the crystal structures of d(ACTCGGATGAT) and the brominated derivative, d(AC^BrUCGGA^BrUGAT). These oligonucleotides form parallel-stranded duplexes with a crystallographically equivalent strand, resulting in the first examples of DNA crystal structures that contains four different symmetric homo base pairs. Two of the parallel-stranded duplexes are coaxially stacked in opposite directions and locked together to form a tetraplex through intercalation of the 5'-most A–A base pairs between adjacent G–G pairs in the partner duplex. The intercalation region is a new type of DNA tertiary structural motif with similarities to the i-motif. ¹H–¹H nuclear magnetic resonance and native gel electrophoresis confirmed the formation of a parallel-stranded duplex in solution. Finally, we modified specific nucleotide positions and added d(GAY) motifs to oligonucleotides and were readily able to obtain similar crystals. This suggests that this parallel-stranded DNA structure may be useful in the rational design of DNA crystals and nanostructures.

View Accepted Manuscript (DOE)

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); NSF

OSTI ID:: 1171850

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 3 Vol. 43; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (54)

DNA-Templated Self-Assembly of Two-Dimensional and Periodical Gold Nanoparticle Arrays Sharma, Jaswinder; Chhabra, Rahul; Liu, Yan Angewandte Chemie, Vol. 118, Issue 5 https://doi.org/10.1002/ange.200503208	journal	January 2006
Nucleic acid junctions and lattices Seeman, Nadrian C. Journal of Theoretical Biology, Vol. 99, Issue 2 https://doi.org/10.1016/0022-5193(82)90002-9	journal	November 1982
Multilayer hemin/G-quadruplex wrapped gold nanoparticles as tag for ultrasensitive multiplex immunoassay by chemiluminescence imaging Zong, Chen; Wu, Jie; Xu, Jie Biosensors and Bioelectronics, Vol. 43 https://doi.org/10.1016/j.bios.2012.12.051	journal	May 2013
(CGA)4: parallel, anti-parallel, right-handed and left-handed homoduplexes of a trinucleotide repeat DNA Kejnovská, Iva; Tůmová, Marcela; Vorlı́čková, Michaela Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1527, Issue 1-2 https://doi.org/10.1016/s0304-4165(01)00150-7	journal	July 2001
Interlocked mismatch-aligned arrowhead DNA motifs Kettani, Abdelali; Bouaziz, Serge; Skripkin, Eugene Structure, Vol. 7, Issue 7 https://doi.org/10.1016/s0969-2126(99)80104-x	journal	July 1999
DNA Nanotechnology Based on i-Motif Structures Dong, Yuanchen; Yang, Zhongqiang; Liu, Dongsheng Accounts of Chemical Research, Vol. 47, Issue 6 https://doi.org/10.1021/ar500073a	journal	May 2014
G-Quadruplex-Forming Oligonucleotide Conjugated to Magnetic Nanoparticles: Synthesis, Characterization, and Enzymatic Stability Assays Musumeci, Domenica; Oliviero, Giorgia; Roviello, Giovanni N. Bioconjugate Chemistry, Vol. 23, Issue 3 https://doi.org/10.1021/bc200305t	journal	February 2012
Deoxyribozyme-Based Ligase Logic Gates and Their Initial Circuits Stojanovic, Milan N.; Semova, Stanka; Kolpashchikov, Dmitry Journal of the American Chemical Society, Vol. 127, Issue 19 https://doi.org/10.1021/ja043003a	journal	May 2005
Three-Dimensional DNA Crystals as Molecular Sieves Paukstelis, Paul J. Journal of the American Chemical Society, Vol. 128, Issue 21 https://doi.org/10.1021/ja061322r	journal	May 2006
Three-Dimensional DNA Crystals with pH-Responsive Noncanonical Junctions Muser, Stephanie E.; Paukstelis, Paul J. Journal of the American Chemical Society, Vol. 134, Issue 30 https://doi.org/10.1021/ja3025033	journal	July 2012
Two Computational Primitives for Algorithmic Self-Assembly: Copying and Counting Barish, Robert D.; Rothemund, Paul W. K.; Winfree, Erik Nano Letters, Vol. 5, Issue 12 https://doi.org/10.1021/nl052038l	journal	December 2005
Design and self-assembly of two-dimensional DNA crystals Winfree, Erik; Liu, Furong; Wenzler, Lisa A. Nature, Vol. 394, Issue 6693 https://doi.org/10.1038/28998	journal	August 1998
Programmable and autonomous computing machine made of biomolecules Benenson, Yaakov; Paz-Elizur, Tamar; Adar, Rivka Nature, Vol. 414, Issue 6862 https://doi.org/10.1038/35106533	journal	November 2001
Folding DNA to create nanoscale shapes and patterns Rothemund, Paul W. K. Nature, Vol. 440, Issue 7082, p. 297-302 https://doi.org/10.1038/nature04586	journal	March 2006
From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal Zheng, Jianping; Birktoft, Jens J.; Chen, Yi Nature, Vol. 461, Issue 7260 https://doi.org/10.1038/nature08274	journal	September 2009
DNA nanotubes self-assembled from triple-crossover tiles as templates for conductive nanowires Liu, D.; Park, S. H.; Reif, J. H. Proceedings of the National Academy of Sciences, Vol. 101, Issue 3 https://doi.org/10.1073/pnas.0305860101	journal	January 2004
Halogen bonds in biological molecules Auffinger, P.; Hays, F. A.; Westhof, E. Proceedings of the National Academy of Sciences, Vol. 101, Issue 48 https://doi.org/10.1073/pnas.0407607101	journal	November 2004
Base-tetrad swapping results in dimerization of RNA quadruplexes: Implications for formation of the i-motif RNA octaplex Pan, B.; Shi, K.; Sundaralingam, M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 9 https://doi.org/10.1073/pnas.0507730103	journal	February 2006
Directing macromolecular conformation through halogen bonds Voth, A. R.; Hays, F. A.; Ho, P. S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 15 https://doi.org/10.1073/pnas.0610531104	journal	March 2007
Circuits and programmable self-assembling DNA structures Carbone, A.; Seeman, N. C. Proceedings of the National Academy of Sciences, Vol. 99, Issue 20 https://doi.org/10.1073/pnas.202418299	journal	September 2002
5'-CGA sequence is a strong motif for homo base-paired parallel-stranded DNA duplex as revealed by NMR analysis. Robinson, H.; Wang, A. H. Proceedings of the National Academy of Sciences, Vol. 90, Issue 11 https://doi.org/10.1073/pnas.90.11.5224	journal	June 1993
Intercalated cytosine motif and novel adenine clusters in the crystal structure of the Tetrahymena telomere Cai, L.; Chen, L.; Raghavan, S. Nucleic Acids Research, Vol. 26, Issue 20 https://doi.org/10.1093/nar/26.20.4696	journal	October 1998
Crystal structure of the complementary quadruplex formed by d(GCATGCT) at atomic resolution Thorpe, J. H. Nucleic Acids Research, Vol. 31, Issue 3 https://doi.org/10.1093/nar/gkg168	journal	February 2003
The poly dA helix: a new structural motif for high performance DNA-based molecular switches Chakraborty, Saikat; Sharma, Suruchi; Maiti, Prabal K. Nucleic Acids Research, Vol. 37, Issue 9 https://doi.org/10.1093/nar/gkp133	journal	March 2009
X-ray structure of d(CGAA), parallel-stranded DNA duplex with homo base pairs Kobuna, T.; Sunami, T.; Kondo, J. Nucleic Acids Symposium Series, Vol. 2, Issue 1 https://doi.org/10.1093/nass/2.1.179	journal	November 2002
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/s0907444910007493	journal	March 2010
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/s0907444912001308	journal	March 2012
Stabilization of the i -motif by intramolecular adenine–adenine–thymine base triple in the structure of d(ACCCT) Weil, Jonathan; Min, Tongpil; Yang, Cheng Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 2 https://doi.org/10.1107/s0907444998012529	journal	February 1999
The PDB_REDO server for macromolecular structure model optimization Joosten, Robbie P.; Long, Fei; Murshudov, Garib N. IUCrJ, Vol. 1, Issue 4 https://doi.org/10.1107/s2052252514009324	journal	May 2014
DNA-Templated Self-Assembly of Protein Arrays and Highly Conductive Nanowires Yan, H. Science, Vol. 301, Issue 5641 https://doi.org/10.1126/science.1089389	journal	September 2003
Rapid Chiral Assembly of Rigid DNA Building Blocks for Molecular Nanofabrication Goodman, R. P. Science, Vol. 310, Issue 5754 https://doi.org/10.1126/science.1120367	journal	December 2005
Programming DNA Tube Circumferences Yin, P.; Hariadi, R. F.; Sahu, S. Science, Vol. 321, Issue 5890 https://doi.org/10.1126/science.1157312	journal	August 2008
DNA Origami with Complex Curvatures in Three-Dimensional Space Han, D.; Pal, S.; Nangreave, J. Science, Vol. 332, Issue 6027 https://doi.org/10.1126/science.1202998	journal	April 2011
The anatomy of A-, B-, and Z-DNA Dickerson, R.; Drew, H.; Conner, B. Science, Vol. 216, Issue 4545 https://doi.org/10.1126/science.7071593	journal	April 1982
DNA-Templated Self-Assembly of Two-Dimensional and Periodical Gold Nanoparticle Arrays Sharma, Jaswinder; Chhabra, Rahul; Liu, Yan Angewandte Chemie International Edition, Vol. 45, Issue 5 https://doi.org/10.1002/anie.200503208	journal	January 2006
Alternating d(G-A) sequences form a parallel-stranded DNA homoduplex. Rippe, K.; Fritsch, V.; Westhof, E. The EMBO Journal, Vol. 11, Issue 10 https://doi.org/10.1002/j.1460-2075.1992.tb05463.x	journal	October 1992
Processing diffraction data with mosflm Leslie, Andrew G. W.; Powell, Harold R. Evolving Methods for Macromolecular Crystallography https://doi.org/10.1007/978-1-4020-6316-9_4	book	January 2007
(CGA)4: parallel, anti-parallel, right-handed and left-handed homoduplexes of a trinucleotide repeat DNA Kejnovská, Iva; Tůmová, Marcela; Vorlı́čková, Michaela Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1527, Issue 1-2 https://doi.org/10.1016/S0304-4165(01)00150-7	journal	July 2001
i-Motif DNA: Structure, stability and targeting with ligands Day, Henry A.; Pavlou, Pavlos; Waller, Zoë A. E. Bioorganic & Medicinal Chemistry, Vol. 22, Issue 16 https://doi.org/10.1016/j.bmc.2014.05.047	journal	August 2014
Crystal Structure of a Continuous Three-Dimensional DNA Lattice Paukstelis, Paul J.; Nowakowski, Jacek; Birktoft, Jens J. Chemistry & Biology, Vol. 11, Issue 8 https://doi.org/10.1016/j.chembiol.2004.05.021	journal	August 2004
Halogen Bonds in Crystal Engineering: Like Hydrogen Bonds yet Different Mukherjee, Arijit; Tothadi, Srinu; Desiraju, Gautam R. Accounts of Chemical Research, Vol. 47, Issue 8 https://doi.org/10.1021/ar5001555	journal	May 2014
5'-CGA Motif Induces Other Sequences To Form Homo Base-Paired Parallel-Stranded DNA Duplex: The Structure of (G-A)n Derived from Four DNA Oligomers Containing (G-A)3 Sequence Robinson, Howard; van Boom, Jacques H.; Wang, Andrew H. -J. Journal of the American Chemical Society, Vol. 116, Issue 4 https://doi.org/10.1021/ja00083a050	journal	February 1994
Gold Nanoparticle Self-Similar Chain Structure Organized by DNA Origami Ding, Baoquan; Deng, Zhengtao; Yan, Hao Journal of the American Chemical Society, Vol. 132, Issue 10 https://doi.org/10.1021/ja9101198	journal	March 2010
Synthesis from DNA of a molecule with the connectivity of a cube Chen, Junghuei; Seeman, Nadrian C. Nature, Vol. 350, Issue 6319 https://doi.org/10.1038/350631a0	journal	April 1991
A tetrameric DNA structure with protonated cytosine-cytosine base pairs Gehring, Kalle; Leroy, Jean-Louis; Guéron, Maurice Nature, Vol. 363, Issue 6429 https://doi.org/10.1038/363561a0	journal	June 1993
Crystal structure of d(GCGAAAGCT) containing a parallel-stranded duplex with homo base pairs and an anti-parallel duplex with Watson-Crick base pairs Sunami, T. Nucleic Acids Research, Vol. 30, Issue 23 https://doi.org/10.1093/nar/gkf639	journal	December 2002
A minimal i-motif stabilized by minor groove G:T:G:T tetrads Escaja, Núria; Viladoms, Júlia; Garavís, Miguel Nucleic Acids Research, Vol. 40, Issue 22 https://doi.org/10.1093/nar/gks911	journal	October 2012
Crystal structure of a DNA/Ba2+ G-quadruplex containing a water-mediated C-tetrad Zhang, Diana; Huang, Terry; Lukeman, Philip S. Nucleic Acids Research, Vol. 42, Issue 21 https://doi.org/10.1093/nar/gku1122	journal	November 2014
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
Stabilization of the i -motif by intramolecular adenine–adenine–thymine base triple in the structure of d(ACCCT) Weil, Jonathan; Min, Tongpil; Yang, Cheng Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 2 https://doi.org/10.1107/S0907444998012529	journal	February 1999
The PDB_REDO server for macromolecular structure model optimization Joosten, Robbie P.; Long, Fei; Murshudov, Garib N. IUCrJ, Vol. 1, Issue 4 https://doi.org/10.1107/S2052252514009324	journal	May 2014
Enzyme-Free Nucleic Acid Logic Circuits Seelig, G.; Soloveichik, D.; Zhang, D. Y. Science, Vol. 314, Issue 5805 https://doi.org/10.1126/science.1132493	journal	December 2006
Folding DNA into Twisted and Curved Nanoscale Shapes Dietz, H.; Douglas, S. M.; Shih, W. M. Science, Vol. 325, Issue 5941 https://doi.org/10.1126/science.1174251	journal	August 2009

Cited By (5)

Stability of the pH-Dependent Parallel-Stranded d(CGA) Motif Luteran, E. M.; Kahn, J. D.; Paukstelis, P. J. bioRxiv https://doi.org/10.1101/2020.07.02.184911	posted_content	July 2020
A DNA G-quadruplex/i-motif hybrid Chu, Betty; Zhang, Daoning; Paukstelis, Paul J. bioRxiv https://doi.org/10.1101/737296	posted_content	August 2019
Strength in Numbers: Development of a Fluorescence Sensor Array for Secondary Structures of DNA Zuffo, Michela; Xie, Xiao; Granzhan, Anton Chemistry - A European Journal, Vol. 25, Issue 7 https://doi.org/10.1002/chem.201805422	journal	January 2019
A DNA G-quadruplex/i-motif hybrid Chu, Betty; Zhang, Daoning; Paukstelis, Paul J. Nucleic Acids Research https://doi.org/10.1093/nar/gkz1008	journal	November 2019
A DNA G-quadruplex/i-motif hybrid Chu, Betty; Zhang, Daoning; Paukstelis, Paul J. Oxford U Press https://doi.org/10.13016/ngt1-eevw	text	January 2019

Similar Records

The hydrogen-bonding structure in parallel-stranded duplex DNA is reverse Watson-Crick

Journal Article · Mon Mar 25 23:00:00 EST 1991 · Biochemistry; (United States) · OSTI ID:5510864

A DNA G-quadruplex/i-motif hybrid

Journal Article · Wed Nov 13 23:00:00 EST 2019 · Nucleic Acids Research · OSTI ID:1607551

An intercalation-locked parallel-stranded DNA tetraplex

Citation Formats

References (54)

Cited By (5)

Similar Records

Related Subjects