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Charge Effects Provide Ångström-Level Control of Lipid Bilayer Morphology on Titanium Dioxide Surfaces

  • Dennis J. Michalak
    Dennis J. Michalak
    Department of Physics, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, United States
  • Mathias Lösche
    Mathias Lösche
    Department of Physics, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, United States
    Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, United States
    Center for Neutron Research, National Institute of Standards and Technology, Gaithersburg, Maryland 20899, United States
  • , and 
  • David P. Hoogerheide*
    David P. Hoogerheide
    Center for Neutron Research, National Institute of Standards and Technology, Gaithersburg, Maryland 20899, United States
    *Email: [email protected]
Cite this: Langmuir 2021, 37, 13, 3970–3981
Publication Date (Web):March 24, 2021
https://doi.org/10.1021/acs.langmuir.1c00214
Copyright © 2021 American Chemical Society

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    Abstract

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    Interfaces between molecular organic architectures and oxidic substrates are a central feature of biosensors and applications of biomimetics in science and technology. For phospholipid bilayers, the large range of pH- and ionic strength-dependent surface charge densities adopted by titanium dioxide and other oxidic surfaces leads to a rich landscape of phenomena that provides exquisite control of membrane interactions with such substrates. Using neutron reflectometry measurements, we report sharp, reversible transitions that occur between closely surface-associated and weakly coupled states. We show that these states arise from a complex interplay of the tunable length scale of electrostatic interactions with the length scale arising from other forces that are independent of solution conditions. A generalized free energy potential, with its inputs only derived from established measurements of surface and bilayer properties, quantitatively describes these and previously reported observations concerning the unbinding of bilayers from supporting substrates.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.langmuir.1c00214.

    • Raw data and derived neutron scattering length density profiles that resulted in the data shown in Figures 1 and 2, an evaluation of the differences in free energy based on linearized and non-linear solutions of the Poisson–Boltzmann equation, a rigorous calculation of the free energy landscape of a DOPC membrane on a SiO2-terminated substrate, a semi-quantitative account of the behavior of a DSPC membrane on a surface-grafted PC bilayer in water to account for experimental results published in references (66) and (67), an estimate of the differences in the behavior of a DOPC membrane on TiO2 in Tris and HEPES buffer, and a table of model fit parameters exemplary for a DOPC bilayer on TiO2 at pH 7 and [NaCl] = 150 mM (PDF)

    • Changes of membrane free energy on TiO2 as a function of ionic strength (MP4)

    • POPC bilayer on a carboxylated substrate as a function of ion concentration in the buffer in reference to ref 47 (MP4)

    • Membrane on TiO2 as a function of bilayer surface potential, ψb (MP4)

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    Cited By

    This article is cited by 5 publications.

    1. Moritz S. Muthwill, Maryame Bina, Nicolò Paracini, John Peter Coats, Severin Merget, Saziye Yorulmaz Avsar, Daniel Messmer, Konrad Tiefenbacher, Cornelia G. Palivan. Planar Polymer Membranes Accommodate Functional Self-Assembly of Inserted Resorcinarene Nanocapsules. ACS Applied Materials & Interfaces 2024, 16 (10) , 13291-13304. https://doi.org/10.1021/acsami.3c18687
    2. Mikhail Ivanov, Alexander P. Lyubartsev. Atomistic Molecular Dynamics Simulations of Lipids Near TiO2 Nanosurfaces. The Journal of Physical Chemistry B 2021, 125 (29) , 8048-8059. https://doi.org/10.1021/acs.jpcb.1c04547
    3. Christian A. Reardon-Lochbaum, Ravithree D. Senanayake, Rocio Amaro Marquez, Kha Trinh, Khoi Nguyen L. Hoang, Tobias Rangel Guillen, Catherine J. Murphy, Robert J. Hamers, Joel A. Pedersen, Rigoberto Hernandez. Influence of sensor composition on nanoparticle and protein interaction with supported lipid bilayers. Environmental Science: Nano 2024, 11 (2) , 561-577. https://doi.org/10.1039/D3EN00406F
    4. David P. Hoogerheide, Joseph A. Dura, Brian B. Maranville, Charles F. Majkrzak. Low-background neutron reflectometry from solid/liquid interfaces. Journal of Applied Crystallography 2022, 55 (1) , 58-66. https://doi.org/10.1107/S1600576721011924
    5. David P. Hoogerheide, Tatiana K. Rostovtseva, Sergey M. Bezrukov. Exploring lipid-dependent conformations of membrane-bound α-synuclein with the VDAC nanopore. Biochimica et Biophysica Acta (BBA) - Biomembranes 2021, 1863 (9) , 183643. https://doi.org/10.1016/j.bbamem.2021.183643