Recent advances in molecular machines based on toehold-mediated strand displacement reaction

doi:10.1007/s40484-017-0097-2

Quant. Biol.

2017, Vol. 5

Issue (1) : 25-41 https://doi.org/10.1007/s40484-017-0097-2

REVIEW

Recent advances in molecular machines based on toehold-mediated strand displacement reaction

Yijun Guo¹,Bing Wei^1,²,Shiyan Xiao¹,Dongbao Yao¹,Hui Li¹,Huaguo Xu³,Tingjie Song¹,Xiang Li¹,Haojun Liang^1,²(

)

¹. CAS Key Laboratory of Soft Matter Chemistry, iChEM (Collaborative Innovation Center of Chemistry for Energy Materials), Department of Polymer Science and Engineering, University of Science and Technology of China, Hefei 230026, China
². Hefei National Laboratory for Physical Sciences at the Microscale, University of Science and Technology of China, Hefei 230026, China
³. College of Materials and Textile Engineering institute, Jiaxing University, Jiaxing 314000, China

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Abstract

Background: The DNA strand displacement reaction, which uses flexible and programmable DNA molecules as reaction components, is the basis of dynamic DNA nanotechnology, and has been widely used in the design of complex autonomous behaviors.

Results: In this review, we first briefly introduce the concept of toehold-mediated strand displacement reaction and its kinetics regulation in pure solution. Thereafter, we review the recent progresses in DNA complex circuit, the assembly of AuNPs driven by DNA molecular machines, and the detection of single nucleotide polymorphism (SNP) using DNA toehold exchange probes in pure solution and in interface state. Lastly, the applications of toehold-mediated strand displacement in the genetic regulation and silencing through combining gene circuit with RNA interference systems are reviewed.

Conclusions: The toehold-mediated strand displacement reaction makes DNA an excellent material for the fabrication of molecular machines and complex circuit, and may potentially be used in the disease diagnosis and the regulation of gene silencing in the near future.

Author Summary The controllable kinetics of strand displacement reaction, along with the programmability of DNA sequence, make DNA an excellent material for the fabrication of molecular machines and complex circuit, and may potentially be used in the disease diagnosis. In this review, we discuss the applications of toehold-mediated strand displacement in the constructions of exquisite molecular devices, complex functional circuits and reaction networks, and biomedical applications such as SNP discrimination and gene-induced disease detection and gene regulation.

Keywords toehold-mediated strand displacement DNA molecular machines SNP gene expression regulation

PACS:

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Corresponding Author(s): Haojun Liang

Just Accepted Date: 22 January 2017 Issue Date: 22 March 2017

Cite this article:

Yijun Guo,Bing Wei,Shiyan Xiao, et al. Recent advances in molecular machines based on toehold-mediated strand displacement reaction[J]. Quant. Biol., 2017, 5(1): 25-41.

URL:

https://academic.hep.com.cn/qb/EN/10.1007/s40484-017-0097-2
https://academic.hep.com.cn/qb/EN/Y2017/V5/I1/25

Fig.1 Mechanism of toehold exchange reaction.

Fig.2 Toehold control and Intuitive Energy Landscape (IEL) model of DNA strand displacement.

(A) Experiments show that kinetics of strand displacement depend on sequence and length of toeholds. The “Maximum” (green) shows the kinetics of strand displacement mediated by strong toehold (only G/C nucleotides), whereas the “Minimum” (red) shows that of weak toehold (only A/T nucleotides), and the “Typical” (black) shows that of toehold with equal numbers of all four nucleotides; reprinted with permission from Ref. [17], Copyright 2009 American Chemical Society. (B) The IEL models strand displacement by dividing the free energy into several states (A–F) with the parameters of sawtooth amplitude (ΔGs) and plateau height (ΔGp); reprinted with permission from Ref. [18], Copyright 2013 Oxford University Press.

Fig.3 Various “coverings” for toehold hiding.

Toeholds are hidden by (A) hybridization; reprinted with permission from Ref. [20], Copyright 2008 American Chemical Society. (B) Bulge-loop structure; reprinted with permission from Ref. [21], Copyright 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim. (C) Hairpin; reprinted with permission from Ref. [22], Copyright 2013 American Chemical Society. (D) Nucleobase-caging groups; reprinted with permission from Ref. [24], Copyright 2013 American Chemical Society. (E) Parallel Hoogsteen motif; reprinted with permission from Ref. [25], Copyright 2014 American Chemical Society.

Fig.4 Toehold split schemes.

(A) The toehold domain and the branch migration (BM) domain were distributed on different strands (C-TH and C-BM), and they formed the “associative toehold” (C-duplex) via additional hybridization. (B) Experiment results of the strand displacement mediated by “associative toehold”. (A) and (B), reprinted with permission from Ref. [26], Copyright 2012 American Chemical Society. (C) The toehold domain and the BM domain were distributed on the same strand and interspaced by a spacer domain, leading to the formation of “remote toehold”. (D) Experiment results of the strand displacement mediated by “remote toehold”. (C) and (D), reprinted with permission from Ref. [29], Copyright 2011 American Chemical Society.

Fig.5 DNA-AuNP assembly.

The architect of prescribed nanoparticle arrays through programming the (A) primary; reprinted with permission from Ref. [46], Copyright 2008 Nature Publishing Group. (B, C) three-dimensional structures of DNA. (B), reprinted with permission from Ref. [48], Copyright 2015 Nature Publishing Group. (C), reprinted with permission from Ref. [49], Copyright 2016 Nature Publishing Group.

Fig.6 Graphical representation of the dynamic DNA-fueled molecular machine strategy and the mechanism of DNA-AuNP assembly.

Fig.7 Toehold-mediated strand displacement reaction on the chip surface to discriminate SNP.

(A) Schematic representation of the DNA toehold exchange process on chip surface to detect single-base changes. (B) Real-time DPI measurements of surface mass decrease on a sensor chip surface modified with a dsDNA probe (PC) with the addition of correct target ssDNA (Correct). Different spurious targets have a single-base mismatch at different positions (m1T to m19T). (C) Calculated toehold exchange efficiencies on chip surface with the addition of correct target ssDNA and different spurious targets; reprinted with permission from Ref. [13], Copyright 2014 Royal Society of Chemistry.

Fig.8 QCM?sensing?platform?application.

(A) Schematic representation of the designed QCM-D biosensing platform for real-time detection of target p53 using a self-assembled DNA nanostructure as an efficient signal amplifier. QCM-D response curves show the corresponding frequency and dissipation shifts of 20 nM of target p53 for the above three steps; reprinted with permission from Ref. [74], Copyright 2012 Royal Society of Chemistry. (B) Schematic representation of the construction and rationale of DNA-SA dendrimer-amplified QCM sensing platform; reprinted with permission from Ref. [75], Copyright 2015 Royal Society of Chemistry.

Fig.9 Schematic representation of the design rationale of discrimination of a single-base change on platform of QCM.

Fig.10 DNA-AuNP assembly applied to graphical representation SNP discrimination.

(A) Graphical representation of SNP discrimination using DNA-fueled molecular machine-based DNA-AuNP assembly; reprinted with permission from Ref. [15], Copyright 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim. (B) Graphical representation of the integrating catalytic circuit with self-assembly of DNA-AuNP conjugates; reprinted with permission from Ref. [14], Copyright 2015 American Chemical Society.

Fig.11 Schematics of RNA-based riboregulator biosensors and synthetic biology applications by RNA toehold-mediated strand displacement reaction.

(A) Conventional riboregulators repress the gene by trapping the RBS through a hairpin structure, which is released under the existence of the trans-acting RNA (taRNA). (B) Toehold switches repress translation by locking the start codon (AUG) sequence and placing the RBS through the stem structure. In RNA–RNA interactions, the toehold reaction activates translation and aligns the hairpin structure via binding with a complementary RNA (trigger RNA); reprinted with permission from Ref. [10], Copyright 2014 Elsevier Inc.

Fig.12 The creation of synthetic biology platforms on paper.

The cell-free transcription and translation systems are combined with the created synthetic gene networks and then freeze-dried onto paper discs to establish stability for long-term extracellular storage of synthetic gene network. The synthetic biology platforms can be observed for the corresponding response when response factor RNA or small molecules are added.

Fig.13 The workflow of paper-based RNA toehold displacement sensors for Zika virus detection.

The sequence of toehold switches of paper-based RNA sensor were designed to the desired device parameters in silico, combined with the RNA sensor and cell-free protein expression system embedded into paper discs, and freeze-dried for stable diagnostic. The Zika virus RNA can be selected by a color change in the paper, which were isothermally amplified to a proper concentration via NASBA and NASBACC, and used to rehydrate the paper sensor for activating reaction; reprinted with permission from Ref. [98], Copyright 2016 Elsevier Inc.

Fig.14 Conditional RNAi regulated by strand displacement.

(A) Schematic illustrations of the designed activatable siRNA system; reprinted with permission from Ref. [101]. Copyright 2009 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim. (B) Schematic illustration of MONi-RNAi strategy and mechanism; reprinted with permission from Ref. [102], Copyright 2011 American Chemical Society.

Fig.15 The biosensor device for mRNA signal and the signal transduction process.

The mRNA signal contains a “trigger-sequence motif” 43-nt long. The biosensor device consists of a Pr:As duplex which “protecting” (Pr) strand is pre-annealed to an “antisense” (As) strand with two 10-nt single-stranded overhangs, and a single “sense” (S) strand. The Pr:As duplex can interact with the trigger-sequence motif. After the strand migration, the released As strand hybridizes with the single-stranded S strand to form a canonical siRNA duplex S: As; reprinted with permission from Ref. [104], Copyright 2010 Oxford University Press.

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