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Kinetics of Diffusion-Mediated DNA Hybridization in Lipid Monolayer Films Determined by Single-Molecule Fluorescence Spectroscopy
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    Kinetics of Diffusion-Mediated DNA Hybridization in Lipid Monolayer Films Determined by Single-Molecule Fluorescence Spectroscopy
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    Department of Chemical and Biological Engineering, Chalmers University of Technology, 412 96, Göteborg, Sweden
    School of Chemistry, University of Southampton, Highfield, Southampton, SO17 1BJ, United Kingdom
    § Chemistry Branch, Department of Science and Mathematics, Faculty of Petroleum and Mining Engineering, Suez Canal University, Suez, 43721, Egypt
    *Address correspondence to [email protected]
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    ACS Nano

    Cite this: ACS Nano 2013, 7, 1, 308–315
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    https://doi.org/10.1021/nn304010p
    Published December 5, 2012
    Copyright © 2012 American Chemical Society

    Abstract

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    We use single-molecule fluorescence microscopy to monitor individual hybridization reactions between membrane-anchored DNA strands, occurring in nanofluidic lipid monolayer films deposited on Teflon AF substrates. The DNA molecules are labeled with different fluorescent dyes, which make it possible to simultaneously monitor the movements of two different molecular species, thus enabling tracking of both reactants and products. We employ lattice diffusion simulations to determine reaction probabilities upon interaction. The observed hybridization rate of the 40-mer DNA was more than 2-fold higher than that of the 20-mer DNA. Since the lateral diffusion coefficient of the two different constructs is nearly identical, the effective molecule radius determines the overall kinetics. This implies that when two DNA molecules approach each other, hydrogen bonding takes place distal from the place where the DNA is anchored to the surface. Strand closure then propagates bidirectionally through a zipper-like mechanism, eventually bringing the lipid anchors together. Comparison with hybridization rates for corresponding DNA sequences in solution reveals that hybridization rates are lower for the lipid-anchored strands and that the dependence on strand length is stronger.

    Copyright © 2012 American Chemical Society

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    Supporting Information

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    S1. Supporting Information covering oligonucleotide synthesis, bulk hybridization kinetics measurements, and conversion from 2D surface density to 3D concentration. S2. Movie showing the co-migration of two hybridized DNA strands. This material is available free of charge via the Internet at http://pubs.acs.org.

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    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

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    This article is cited by 9 publications.

    1. Xiaobin Huang, Weidong Zhao, Xiangyu Chen, Jinming Li, Haochen Ye, Cancan Li, Xiaomeng Yin, Xinyuan Zhou, Xuezhi Qiao, Zhenjie Xue, Tie Wang. Gold Nanoparticle-Bridge Array to Improve DNA Hybridization Efficiency of SERS Sensors. Journal of the American Chemical Society 2022, 144 (38) , 17533-17539. https://doi.org/10.1021/jacs.2c06623
    2. Pelin Toren, Erol Ozgur, and Mehmet Bayindir . Real-Time and Selective Detection of Single Nucleotide DNA Mutations Using Surface Engineered Microtoroids. Analytical Chemistry 2015, 87 (21) , 10920-10926. https://doi.org/10.1021/acs.analchem.5b02664
    3. Mehrnaz Shaali, Samuel Lara-Avila, Paul Dommersnes, Alar Ainla, Sergey Kubatkin, and Aldo Jesorka . Nanopatterning of Mobile Lipid Monolayers on Electron-Beam-Sculpted Teflon AF Surfaces. ACS Nano 2015, 9 (2) , 1271-1279. https://doi.org/10.1021/nn5050867
    4. Bin Zhao, Ningwei Li, Tianfa Xie, Yousef Bagheri, Chungwen Liang, Puspam Keshri, Yubing Sun, Mingxu You. Quantifying tensile forces at cell–cell junctions with a DNA-based fluorescent probe. Chemical Science 2020, 11 (32) , 8558-8566. https://doi.org/10.1039/D0SC01455A
    5. Yousef Bagheri, Sara Chedid, Fatemeh Shafiei, Bin Zhao, Mingxu You. A quantitative assessment of the dynamic modification of lipid–DNA probes on live cell membranes. Chemical Science 2019, 10 (48) , 11030-11040. https://doi.org/10.1039/C9SC04251B
    6. Mingxu You, Yifan Lyu, Da Han, Liping Qiu, Qiaoling Liu, Tao Chen, Cuichen Sam Wu, Lu Peng, Liqin Zhang, Gang Bao, Weihong Tan. DNA probes for monitoring dynamic and transient molecular encounters on live cell membranes. Nature Nanotechnology 2017, 12 (5) , 453-459. https://doi.org/10.1038/nnano.2017.23
    7. Cong Liu, Judy M. Obliosca, Yen-Liang Liu, Yu-An Chen, Ning Jiang, Hsin-Chih Yeh. 3D single-molecule tracking enables direct hybridization kinetics measurement in solution. Nanoscale 2017, 9 (17) , 5664-5670. https://doi.org/10.1039/C7NR01369H
    8. Steven McGinn, David Bauer, Thomas Brefort, Liqin Dong, Afaf El-Sagheer, Abdou Elsharawy, Geraint Evans, Elin Falk-Sörqvist, Michael Forster, Simon Fredriksson, Peter Freeman, Camilla Freitag, Joachim Fritzsche, Spencer Gibson, Mats Gullberg, Marta Gut, Simon Heath, Isabelle Heath-Brun, Andrew J. Heron, Johannes Hohlbein, Rongqin Ke, Owen Lancaster, Ludovic Le Reste, Giovanni Maglia, Rodolphe Marie, Florence Mauger, Florian Mertes, Marco Mignardi, Lotte Moens, Jelle Oostmeijer, Ruud Out, Jonas Nyvold Pedersen, Fredrik Persson, Vincent Picaud, Dvir Rotem, Nadine Schracke, Jennifer Sengenes, Peer F. Stähler, Björn Stade, David Stoddart, Xia Teng, Colin D. Veal, Nathalie Zahra, Hagan Bayley, Markus Beier, Tom Brown, Cees Dekker, Björn Ekström, Henrik Flyvbjerg, Andre Franke, Simone Guenther, Achillefs N. Kapanidis, Jane Kaye, Anders Kristensen, Hans Lehrach, Jonathan Mangion, Sascha Sauer, Emile Schyns, Jörg Tost, Joop M.L.M. van Helvoort, Pieter J. van der Zaag, Jonas O. Tegenfeldt, Anthony J. Brookes, Kalim Mir, Mats Nilsson, James P. Willcocks, Ivo G. Gut. New technologies for DNA analysis – a review of the READNA Project. New Biotechnology 2016, 33 (3) , 311-330. https://doi.org/10.1016/j.nbt.2015.10.003
    9. Ambadas B. Rode, Tamaki Endoh, Hisae Tateishi-Karimata, Shuntaro Takahashi, Naoki Sugimoto. Real-time monitoring of DNA hybridization kinetics on living cell surfaces. Chemical Communications 2013, 49 (76) , 8444. https://doi.org/10.1039/c3cc42990c

    ACS Nano

    Cite this: ACS Nano 2013, 7, 1, 308–315
    Click to copy citationCitation copied!
    https://doi.org/10.1021/nn304010p
    Published December 5, 2012
    Copyright © 2012 American Chemical Society

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