DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: An intercalation-locked parallel-stranded DNA tetraplex

Abstract

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(ACBrUCGGABrUGAT). 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.

Authors:
; ;
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)
OSTI Identifier:
1171850
Resource Type:
Accepted Manuscript
Journal Name:
Nucleic Acids Research
Additional Journal Information:
Journal Volume: 43; Journal Issue: 3; Journal ID: ISSN 0305-1048
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English

Citation Formats

Tripathi, S., Zhang, D., and Paukstelis, P. J. An intercalation-locked parallel-stranded DNA tetraplex. United States: N. p., 2015. Web. doi:10.1093/nar/gkv033.
Tripathi, S., Zhang, D., & Paukstelis, P. J. An intercalation-locked parallel-stranded DNA tetraplex. United States. https://doi.org/10.1093/nar/gkv033
Tripathi, S., Zhang, D., and Paukstelis, P. J. Tue . "An intercalation-locked parallel-stranded DNA tetraplex". United States. https://doi.org/10.1093/nar/gkv033. https://www.osti.gov/servlets/purl/1171850.
@article{osti_1171850,
title = {An intercalation-locked parallel-stranded DNA tetraplex},
author = {Tripathi, S. and Zhang, D. and Paukstelis, P. J.},
abstractNote = {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(ACBrUCGGABrUGAT). 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.},
doi = {10.1093/nar/gkv033},
journal = {Nucleic Acids Research},
number = 3,
volume = 43,
place = {United States},
year = {Tue Jan 27 00:00:00 EST 2015},
month = {Tue Jan 27 00:00:00 EST 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 10 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Synthesis from DNA of a molecule with the connectivity of a cube
journal, April 1991

  • Chen, Junghuei; Seeman, Nadrian C.
  • Nature, Vol. 350, Issue 6319
  • DOI: 10.1038/350631a0

Design and self-assembly of two-dimensional DNA crystals
journal, August 1998

  • Winfree, Erik; Liu, Furong; Wenzler, Lisa A.
  • Nature, Vol. 394, Issue 6693
  • DOI: 10.1038/28998

Rapid Chiral Assembly of Rigid DNA Building Blocks for Molecular Nanofabrication
journal, December 2005


Folding DNA to create nanoscale shapes and patterns
journal, March 2006


From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal
journal, September 2009

  • Zheng, Jianping; Birktoft, Jens J.; Chen, Yi
  • Nature, Vol. 461, Issue 7260
  • DOI: 10.1038/nature08274

Folding DNA into Twisted and Curved Nanoscale Shapes
journal, August 2009


DNA Origami with Complex Curvatures in Three-Dimensional Space
journal, April 2011


Programmable and autonomous computing machine made of biomolecules
journal, November 2001

  • Benenson, Yaakov; Paz-Elizur, Tamar; Adar, Rivka
  • Nature, Vol. 414, Issue 6862
  • DOI: 10.1038/35106533

Circuits and programmable self-assembling DNA structures
journal, September 2002

  • Carbone, A.; Seeman, N. C.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 20
  • DOI: 10.1073/pnas.202418299

Deoxyribozyme-Based Ligase Logic Gates and Their Initial Circuits
journal, May 2005

  • Stojanovic, Milan N.; Semova, Stanka; Kolpashchikov, Dmitry
  • Journal of the American Chemical Society, Vol. 127, Issue 19
  • DOI: 10.1021/ja043003a

Two Computational Primitives for Algorithmic Self-Assembly:  Copying and Counting
journal, December 2005

  • Barish, Robert D.; Rothemund, Paul W. K.; Winfree, Erik
  • Nano Letters, Vol. 5, Issue 12
  • DOI: 10.1021/nl052038l

Enzyme-Free Nucleic Acid Logic Circuits
journal, December 2006


DNA-Templated Self-Assembly of Protein Arrays and Highly Conductive Nanowires
journal, September 2003


DNA nanotubes self-assembled from triple-crossover tiles as templates for conductive nanowires
journal, January 2004

  • Liu, D.; Park, S. H.; Reif, J. H.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 3
  • DOI: 10.1073/pnas.0305860101

DNA-Templated Self-Assembly of Two-Dimensional and Periodical Gold Nanoparticle Arrays
journal, January 2006

  • Sharma, Jaswinder; Chhabra, Rahul; Liu, Yan
  • Angewandte Chemie International Edition, Vol. 45, Issue 5
  • DOI: 10.1002/anie.200503208

Programming DNA Tube Circumferences
journal, August 2008


Gold Nanoparticle Self-Similar Chain Structure Organized by DNA Origami
journal, March 2010

  • Ding, Baoquan; Deng, Zhengtao; Yan, Hao
  • Journal of the American Chemical Society, Vol. 132, Issue 10
  • DOI: 10.1021/ja9101198

Nucleic acid junctions and lattices
journal, November 1982


Crystal Structure of a Continuous Three-Dimensional DNA Lattice
journal, August 2004


Three-Dimensional DNA Crystals as Molecular Sieves
journal, May 2006

  • Paukstelis, Paul J.
  • Journal of the American Chemical Society, Vol. 128, Issue 21
  • DOI: 10.1021/ja061322r

Three-Dimensional DNA Crystals with pH-Responsive Noncanonical Junctions
journal, July 2012

  • Muser, Stephanie E.; Paukstelis, Paul J.
  • Journal of the American Chemical Society, Vol. 134, Issue 30
  • DOI: 10.1021/ja3025033

The poly dA helix: a new structural motif for high performance DNA-based molecular switches
journal, March 2009

  • Chakraborty, Saikat; Sharma, Suruchi; Maiti, Prabal K.
  • Nucleic Acids Research, Vol. 37, Issue 9
  • DOI: 10.1093/nar/gkp133

G-Quadruplex-Forming Oligonucleotide Conjugated to Magnetic Nanoparticles: Synthesis, Characterization, and Enzymatic Stability Assays
journal, February 2012

  • Musumeci, Domenica; Oliviero, Giorgia; Roviello, Giovanni N.
  • Bioconjugate Chemistry, Vol. 23, Issue 3
  • DOI: 10.1021/bc200305t

DNA Nanotechnology Based on i-Motif Structures
journal, May 2014

  • Dong, Yuanchen; Yang, Zhongqiang; Liu, Dongsheng
  • Accounts of Chemical Research, Vol. 47, Issue 6
  • DOI: 10.1021/ar500073a

i-Motif DNA: Structure, stability and targeting with ligands
journal, August 2014

  • Day, Henry A.; Pavlou, Pavlos; Waller, Zoë A. E.
  • Bioorganic & Medicinal Chemistry, Vol. 22, Issue 16
  • DOI: 10.1016/j.bmc.2014.05.047

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
journal, February 1994

  • Robinson, Howard; van Boom, Jacques H.; Wang, Andrew H. -J.
  • Journal of the American Chemical Society, Vol. 116, Issue 4
  • DOI: 10.1021/ja00083a050

Alternating d(G-A) sequences form a parallel-stranded DNA homoduplex.
journal, October 1992


5'-CGA sequence is a strong motif for homo base-paired parallel-stranded DNA duplex as revealed by NMR analysis.
journal, June 1993

  • Robinson, H.; Wang, A. H.
  • Proceedings of the National Academy of Sciences, Vol. 90, Issue 11
  • DOI: 10.1073/pnas.90.11.5224

Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012

  • Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
  • Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
  • DOI: 10.1107/S0907444912001308

Features and development of Coot
journal, March 2010

  • Emsley, P.; Lohkamp, B.; Scott, W. G.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
  • DOI: 10.1107/S0907444910007493

The PDB_REDO server for macromolecular structure model optimization
journal, May 2014


Base-tetrad swapping results in dimerization of RNA quadruplexes: Implications for formation of the i-motif RNA octaplex
journal, February 2006

  • Pan, B.; Shi, K.; Sundaralingam, M.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 9
  • DOI: 10.1073/pnas.0507730103

Crystal structure of a DNA/Ba2+ G-quadruplex containing a water-mediated C-tetrad
journal, November 2014

  • Zhang, Diana; Huang, Terry; Lukeman, Philip S.
  • Nucleic Acids Research, Vol. 42, Issue 21
  • DOI: 10.1093/nar/gku1122

Crystal structure of the complementary quadruplex formed by d(GCATGCT) at atomic resolution
journal, February 2003


X-ray structure of d(CGAA), parallel-stranded DNA duplex with homo base pairs
journal, November 2002

  • Kobuna, T.; Sunami, T.; Kondo, J.
  • Nucleic Acids Symposium Series, Vol. 2, Issue 1
  • DOI: 10.1093/nass/2.1.179

Stabilization of the i -motif by intramolecular adenine–adenine–thymine base triple in the structure of d(ACCCT)
journal, February 1999

  • Weil, Jonathan; Min, Tongpil; Yang, Cheng
  • Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 2
  • DOI: 10.1107/S0907444998012529

A tetrameric DNA structure with protonated cytosine-cytosine base pairs
journal, June 1993

  • Gehring, Kalle; Leroy, Jean-Louis; Guéron, Maurice
  • Nature, Vol. 363, Issue 6429
  • DOI: 10.1038/363561a0

Intercalated cytosine motif and novel adenine clusters in the crystal structure of the Tetrahymena telomere
journal, October 1998


A minimal i-motif stabilized by minor groove G:T:G:T tetrads
journal, October 2012

  • Escaja, Núria; Viladoms, Júlia; Garavís, Miguel
  • Nucleic Acids Research, Vol. 40, Issue 22
  • DOI: 10.1093/nar/gks911

The anatomy of A-, B-, and Z-DNA
journal, April 1982


Halogen bonds in biological molecules
journal, November 2004

  • Auffinger, P.; Hays, F. A.; Westhof, E.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 48
  • DOI: 10.1073/pnas.0407607101

Directing macromolecular conformation through halogen bonds
journal, March 2007

  • Voth, A. R.; Hays, F. A.; Ho, P. S.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 15
  • DOI: 10.1073/pnas.0610531104

Halogen Bonds in Crystal Engineering: Like Hydrogen Bonds yet Different
journal, May 2014

  • Mukherjee, Arijit; Tothadi, Srinu; Desiraju, Gautam R.
  • Accounts of Chemical Research, Vol. 47, Issue 8
  • DOI: 10.1021/ar5001555

DNA-Templated Self-Assembly of Two-Dimensional and Periodical Gold Nanoparticle Arrays
journal, January 2006

  • Sharma, Jaswinder; Chhabra, Rahul; Liu, Yan
  • Angewandte Chemie, Vol. 118, Issue 5
  • DOI: 10.1002/ange.200503208

Nucleic acid junctions and lattices
journal, November 1982


(CGA)4: parallel, anti-parallel, right-handed and left-handed homoduplexes of a trinucleotide repeat DNA
journal, July 2001

  • Kejnovská, Iva; Tůmová, Marcela; Vorlı́čková, Michaela
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1527, Issue 1-2
  • DOI: 10.1016/s0304-4165(01)00150-7

Interlocked mismatch-aligned arrowhead DNA motifs
journal, July 1999


DNA Nanotechnology Based on i-Motif Structures
journal, May 2014

  • Dong, Yuanchen; Yang, Zhongqiang; Liu, Dongsheng
  • Accounts of Chemical Research, Vol. 47, Issue 6
  • DOI: 10.1021/ar500073a

G-Quadruplex-Forming Oligonucleotide Conjugated to Magnetic Nanoparticles: Synthesis, Characterization, and Enzymatic Stability Assays
journal, February 2012

  • Musumeci, Domenica; Oliviero, Giorgia; Roviello, Giovanni N.
  • Bioconjugate Chemistry, Vol. 23, Issue 3
  • DOI: 10.1021/bc200305t

Deoxyribozyme-Based Ligase Logic Gates and Their Initial Circuits
journal, May 2005

  • Stojanovic, Milan N.; Semova, Stanka; Kolpashchikov, Dmitry
  • Journal of the American Chemical Society, Vol. 127, Issue 19
  • DOI: 10.1021/ja043003a

Three-Dimensional DNA Crystals as Molecular Sieves
journal, May 2006

  • Paukstelis, Paul J.
  • Journal of the American Chemical Society, Vol. 128, Issue 21
  • DOI: 10.1021/ja061322r

Three-Dimensional DNA Crystals with pH-Responsive Noncanonical Junctions
journal, July 2012

  • Muser, Stephanie E.; Paukstelis, Paul J.
  • Journal of the American Chemical Society, Vol. 134, Issue 30
  • DOI: 10.1021/ja3025033

Two Computational Primitives for Algorithmic Self-Assembly:  Copying and Counting
journal, December 2005

  • Barish, Robert D.; Rothemund, Paul W. K.; Winfree, Erik
  • Nano Letters, Vol. 5, Issue 12
  • DOI: 10.1021/nl052038l

Design and self-assembly of two-dimensional DNA crystals
journal, August 1998

  • Winfree, Erik; Liu, Furong; Wenzler, Lisa A.
  • Nature, Vol. 394, Issue 6693
  • DOI: 10.1038/28998

Programmable and autonomous computing machine made of biomolecules
journal, November 2001

  • Benenson, Yaakov; Paz-Elizur, Tamar; Adar, Rivka
  • Nature, Vol. 414, Issue 6862
  • DOI: 10.1038/35106533

Folding DNA to create nanoscale shapes and patterns
journal, March 2006


From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal
journal, September 2009

  • Zheng, Jianping; Birktoft, Jens J.; Chen, Yi
  • Nature, Vol. 461, Issue 7260
  • DOI: 10.1038/nature08274

DNA nanotubes self-assembled from triple-crossover tiles as templates for conductive nanowires
journal, January 2004

  • Liu, D.; Park, S. H.; Reif, J. H.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 3
  • DOI: 10.1073/pnas.0305860101

Halogen bonds in biological molecules
journal, November 2004

  • Auffinger, P.; Hays, F. A.; Westhof, E.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 48
  • DOI: 10.1073/pnas.0407607101

Base-tetrad swapping results in dimerization of RNA quadruplexes: Implications for formation of the i-motif RNA octaplex
journal, February 2006

  • Pan, B.; Shi, K.; Sundaralingam, M.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 9
  • DOI: 10.1073/pnas.0507730103

Directing macromolecular conformation through halogen bonds
journal, March 2007

  • Voth, A. R.; Hays, F. A.; Ho, P. S.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 15
  • DOI: 10.1073/pnas.0610531104

Circuits and programmable self-assembling DNA structures
journal, September 2002

  • Carbone, A.; Seeman, N. C.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 20
  • DOI: 10.1073/pnas.202418299

5'-CGA sequence is a strong motif for homo base-paired parallel-stranded DNA duplex as revealed by NMR analysis.
journal, June 1993

  • Robinson, H.; Wang, A. H.
  • Proceedings of the National Academy of Sciences, Vol. 90, Issue 11
  • DOI: 10.1073/pnas.90.11.5224

Intercalated cytosine motif and novel adenine clusters in the crystal structure of the Tetrahymena telomere
journal, October 1998


Crystal structure of the complementary quadruplex formed by d(GCATGCT) at atomic resolution
journal, February 2003


The poly dA helix: a new structural motif for high performance DNA-based molecular switches
journal, March 2009

  • Chakraborty, Saikat; Sharma, Suruchi; Maiti, Prabal K.
  • Nucleic Acids Research, Vol. 37, Issue 9
  • DOI: 10.1093/nar/gkp133

X-ray structure of d(CGAA), parallel-stranded DNA duplex with homo base pairs
journal, November 2002

  • Kobuna, T.; Sunami, T.; Kondo, J.
  • Nucleic Acids Symposium Series, Vol. 2, Issue 1
  • DOI: 10.1093/nass/2.1.179

DNA-Templated Self-Assembly of Protein Arrays and Highly Conductive Nanowires
journal, September 2003


Rapid Chiral Assembly of Rigid DNA Building Blocks for Molecular Nanofabrication
journal, December 2005


Programming DNA Tube Circumferences
journal, August 2008


DNA Origami with Complex Curvatures in Three-Dimensional Space
journal, April 2011


The anatomy of A-, B-, and Z-DNA
journal, April 1982


Works referencing / citing this record:

Strength in Numbers: Development of a Fluorescence Sensor Array for Secondary Structures of DNA
journal, January 2019

  • Zuffo, Michela; Xie, Xiao; Granzhan, Anton
  • Chemistry - A European Journal, Vol. 25, Issue 7
  • DOI: 10.1002/chem.201805422

A DNA G-quadruplex/i-motif hybrid
posted_content, August 2019

  • Chu, Betty; Zhang, Daoning; Paukstelis, Paul J.
  • bioRxiv
  • DOI: 10.1101/737296

A DNA G-quadruplex/i-motif hybrid
text, January 2019


A DNA G-quadruplex/i-motif hybrid
journal, November 2019

  • Chu, Betty; Zhang, Daoning; Paukstelis, Paul J.
  • Nucleic Acids Research
  • DOI: 10.1093/nar/gkz1008

Stability of the pH-Dependent Parallel-Stranded d(CGA) Motif
posted_content, July 2020


A DNA G-quadruplex/i-motif hybrid
posted_content, August 2019

  • Chu, Betty; Zhang, Daoning; Paukstelis, Paul J.
  • bioRxiv
  • DOI: 10.1101/737296