Title: Engineering tertiary chirality in helical biopolymers

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
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  1. Department of Chemistry, New York University, New York, NY 10003
  2. Department of Mathematics and Statistics, University of South Florida, Tampa, FL 33620
  3. Department of Mathematics, University of Oregon, Eugene, OR 97403
  4. Department of Chemistry, Purdue University, West Lafayette, IN 47907

Tertiary chirality describes the handedness of supramolecular assemblies and relies not only on the primary and secondary structures of the building blocks but also on topological driving forces that have been sparsely characterized. Helical biopolymers, especially DNA, have been extensively investigated as they possess intrinsic chirality that determines the optical, mechanical, and physical properties of the ensuing material. Here, we employ the DNA tensegrity triangle as a model system to locate the tipping points in chirality inversion at the tertiary level by X-ray diffraction. We engineer tensegrity triangle crystals with incremental rotational steps between immobile junctions from 3 to 28 base pairs (bp). We construct a mathematical model that accurately predicts and explains the molecular configurations in both this work and previous studies. Our design framework is extendable to other supramolecular assemblies of helical biopolymers and can be used in the design of chiral nanomaterials, optically active molecules, and mesoporous frameworks, all of which are of interest to physical, biological, and chemical nanoscience.

Research Organization:
New York Univ. (NYU), NY (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC)
Grant/Contract Number:
SC0007991
OSTI ID:
2341646
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 19 Vol. 121; ISSN 0027-8424
Publisher:
Proceedings of the National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English

References (64)

Powering ≈50 µm Motion by a Molecular Event in DNA Crystals journal May 2022
Augmented DNA Nanoarchitectures: A Structural Library of 3D Self‐Assembling Tensegrity Triangle Variants journal October 2022
Metal‐Mediated DNA Nanotechnology in 3D: Structural Library by Templated Diffraction journal June 2023
Reconfigurable Two‐Dimensional DNA Lattices: Static and Dynamic Angle Control journal November 2021
A Self‐Assembled Rhombohedral DNA Crystal Scaffold with Tunable Cavity Sizes and High‐Resolution Structural Detail journal August 2020
Programmable 3D Hexagonal Geometry of DNA Tensegrity Triangles journal January 2023
The absence of tertiary interactions in a self-assembled DNA crystal structure: SELF-ASSEMBLED DNA CRYSTAL STRUCTURE journal March 2012
The Rule of Thirds: Controlling Junction Chirality and Polarity in 3D DNA Tiles journal December 2022
The crystal structures of DNA Holliday junctions journal June 2001
Self-Assembly of 3D DNA Crystals Containing a Torsionally Stressed Component journal November 2017
The linking number in systems with Periodic Boundary Conditions journal November 2015
Direct Homologous dsDNA–dsDNA Pairing: How, Where, and Why? journal February 2020
Architecture with GIDEON, a program for design in structural DNA nanotechnology journal December 2006
The PX Motif of DNA Binds Specifically to Escherichia coli DNA Polymerase I journal December 2018
Paranemic Crossover DNA: There and Back Again journal June 2018
Atomistic Picture of Opening–Closing Dynamics of DNA Holliday Junction Obtained by Molecular Simulations journal April 2023
3D Hexagonal Arrangement of DNA Tensegrity Triangles journal October 2021
Designing Higher Resolution Self-Assembled 3D DNA Crystals via Strand Terminus Modifications journal June 2019
Tensegrity:  Construction of Rigid DNA Triangles with Flexible Four-Arm DNA Junctions journal March 2004
Highly Connected Two-Dimensional Crystals of DNA Six-Point-Stars journal December 2006
DNA Crystals as Vehicles for Biocatalysis journal May 2014
Designed Two-Dimensional DNA Holliday Junction Arrays Visualized by Atomic Force Microscopy journal June 1999
The Formation and Displacement of Ordered DNA Triplexes in Self-Assembled Three-Dimensional DNA Crystals journal February 2023
Engineering DNA Crystals toward Studying DNA–Guest Molecule Interactions journal February 2023
Tuning Geometric Chirality in Metallic and Hybrid Nanostructures by Controlled Nanoscale Crystal Symmetry Breaking journal March 2023
Controlled Hierarchical Self-Assembly of Nanoparticles and Chiral Molecules into Tubular Nanocomposites journal April 2023
Construction and Structure Determination of a Three-Dimensional DNA Crystal journal August 2016
Tuning the Cavity Size and Chirality of Self-Assembling 3D DNA Crystals journal August 2017
Making Engineered 3D DNA Crystals Robust journal September 2019
Design and self-assembly of two-dimensional DNA crystals journal August 1998
An immobile nucleic acid junction constructed from oligonucleotides journal October 1983
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
Double Holliday junctions are intermediates of DNA break repair journal March 2010
Creating complex molecular topologies by configuring DNA four-way junctions journal July 2016
Synthesizing topological structures containing RNA journal March 2017
Self-assembly of three-dimensional prestressed tensegrity structures from DNA journal June 2010
The influence of Holliday junction sequence and dynamics on DNA crystal self-assembly journal June 2022
Single crystals of mechanically entwined helical covalent polymers journal May 2021
Photonically active bowtie nanoassemblies with chirality continuum journal March 2023
Harnessing a paper-folding mechanism for reconfigurable DNA origami journal July 2023
In vivo cloning of artificial DNA nanostructures journal October 2008
Double-stranded DNA homology produces a physical signature journal June 2010
Discrete Frenet frame, inflection point solitons, and curve visualization with applications to folded proteins journal June 2011
Coot model-building tools for molecular graphics journal November 2004
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
Data processing and analysis with the autoPROC toolbox journal March 2011
Networks with controlled chirality via self-assembly of chiral triblock terpolymers journal October 2020
Recombination-Independent Recognition of DNA Homology for Repeat-Induced Point Mutation (RIP) Is Modulated by the Underlying Nucleotide Sequence journal May 2016
[3T12] Self-assembling left-handed tensegrity triangle with 12 interjunction base pairs and R3 symmetry journal April 2024
[3T13] Self-assembling left-handed tensegrity triangle with 13 interjunction base pairs and R3 symmetry journal April 2024
[3T14] Self-assembling left-handed tensegrity triangle with 14 interjunction base pairs and R3 symmetry journal April 2024
[3T15] Self-assembling DNA motif with 15 base pairs between junctions and P32 symmetry other April 2024
[3T16] Self-assembling right-handed tensegrity triangle with 16 interjunction base pairs and R3 symmetry other April 2024
[3T17] Self-assembling right-handed tensegrity triangle with 17 interjunction base pairs and R3 symmetry other April 2024
[3T18] Self-assembling right-handed tensegrity triangle with 18 interjunction base pairs and P63 symmetry other April 2024
[3T14+10] Self-assembling left-handed tensegrity triangle with 14 interjunction base pairs and a 10 bp linker with R3 symmetry other February 2024
[4T17] Self-assembling right-handed four-turn tensegrity triangle with 17 interjunction base pairs and R3 symmetry other April 2024
[4T24] Self-assembling left-handed tensegrity triangle with 24 interjunction base pairs and R3 symmetry other April 2024
[4T28] Self-assembling right-handed tensegrity triangle with 28 interjunction base pairs and R3 symmetry journal April 2024
[2T13] Self-assembling left-handed two-turn tensegrity triangle with 13 interjunction base pairs and R3 symmetry other April 2024
[2T5] Self-assembling DNA motif with 5 base pairs between junctions and P32 symmetry other May 2024
Small Circular DNA Molecules as Triangular Scaffolds for the Growth of 3D Single Crystals journal May 2020
Ribbons: Their Geometry and Topology journal January 2004