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Amphiphobic Septa Enhance the Mechanical Stability of Free-Standing Bilayer Lipid Membranes

  • Daichi Yamaura
    Daichi Yamaura
    Laboratory for Nanoelectronics and Spintronics, Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
  • Daisuke Tadaki
    Daisuke Tadaki
    Laboratory for Nanoelectronics and Spintronics, Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
  • Shun Araki
    Shun Araki
    Laboratory for Nanoelectronics and Spintronics, Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
    More by Shun Araki
  • Miyu Yoshida
    Miyu Yoshida
    Laboratory for Nanoelectronics and Spintronics, Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
    More by Miyu Yoshida
  • Kohei Arata
    Kohei Arata
    Laboratory for Nanoelectronics and Spintronics, Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
    More by Kohei Arata
  • Takeshi Ohori
    Takeshi Ohori
    Laboratory for Nanoelectronics and Spintronics, Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
  • Ken-ichi Ishibashi
    Ken-ichi Ishibashi
    Hang-Ichi Corporation, 1-7-315 Honcho, Naka-ku, Yokohama, Kanagawa 231-0005, Japan
  • Miki Kato
    Miki Kato
    Laboratory for Nanoelectronics and Spintronics, Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
    More by Miki Kato
  • Teng Ma
    Teng Ma
    Advanced Institute for Materials Research, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
    More by Teng Ma
  • Ryusuke Miyata
    Ryusuke Miyata
    Laboratory for Nanoelectronics and Spintronics, Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
  • Hideaki Yamamoto
    Hideaki Yamamoto
    Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, 6-3 Aramaki-Aza-Aoba, Aoba-ku, Sendai, Miyagi 980-8578, Japan
  • Ryugo Tero
    Ryugo Tero
    Department of Environmental and Life Sciences, Toyohashi University of Technology, Toyohashi, Aichi 441-8580, Japan
    More by Ryugo Tero
  • Masao Sakuraba
    Masao Sakuraba
    Laboratory for Nanoelectronics and Spintronics, Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
  • Toshio Ogino
    Toshio Ogino
    The Instrumental Analysis Center, Yokohama National University, Tokiwadai 79-5, Hodogaya-ku, Yokohama, Kanagawa 240-8501, Japan
    More by Toshio Ogino
  • Michio Niwano
    Michio Niwano
    Kansei Fukushi Research Institute, Tohoku Fukushi University, 6-149-1 Kunimi-ga-oka, Aoba-ku, Sendai, Miyagi 989-3201, Japan
  • , and 
  • Ayumi Hirano-Iwata*
    Ayumi Hirano-Iwata
    Laboratory for Nanoelectronics and Spintronics, Research Institute of Electrical Communication  and  Advanced Institute for Materials Research, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan
    *Email: [email protected]
Cite this: Langmuir 2018, 34, 19, 5615–5622
Publication Date (Web):April 17, 2018
https://doi.org/10.1021/acs.langmuir.8b00747
Copyright © 2018 American Chemical Society

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    Abstract

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    Artificial bilayer lipid membranes (BLMs) provide well-defined systems for investigating the fundamental properties of membrane proteins, including ion channels, and for screening the effect of drugs that act on them. However, the application of this technique is limited due to the low stability and low reconstitution efficiency of the process. We previously reported on improving the stability of BLM based on the fabrication of microapertures having a tapered edge in SiO2/Si3N4 septa and efficient ion channel incorporation based on vesicle fusion accelerated by a centrifugal force. Although the BLM stability and incorporation probability were dramatically improved when these approaches were used, some BLMs were ruptured when subjected to a centrifugal force. To further improve the BLM stability, we investigated the effect of modifying the surface of the SiO2/Si3N4 septa on the stability of BLM suspended in the septa. The modified surfaces were characterized in terms of hydrophobicity, lipophobicity, and surface roughness. Diffusion coefficients of the lipid monolayers formed on the modified surfaces were also determined. Highly fluidic lipid monolayers were formed on the amphiphobic substrates that had been modified with long-chain perfluorocarbons. Free-standing BLMs formed in amphiphobic septa showed a much higher mechanical stability, including tolerance to water movement and applied centrifugal forces with and without proteoliposomes, than those formed in the septa that had been modified with a short alkyl chain. These results demonstrate that highly stable BLMs are formed when the surface of the septa has amphiphobic properties. Because highly fluidic lipid monolayers that are formed on the septa seamlessly connect with BLMs in a free-standing region, the high fluidity of the lipids contributes to decreasing potential damage to BLMs when mechanical stresses are applied. This approach to improve the BLM stability increases the experimental efficiency of the BLM systems and will contribute to the development of high-throughput platforms for functional assays of ion channel proteins.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.8b00747.

    • Additional description on the structure of the silane coupling agents, detailed experimental procedures, XPS spectra of the PFDS- and PFTS-modified surfaces, and fractional fluorescence recovery vs. time of lipid monolayers on the OTS-, PFDDS-, FPDS-, and PFTS-modified surfaces (PDF)

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    Cited By

    This article is cited by 16 publications.

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    2. Azusa Oshima, Hiroshi Nakashima, Koji Sumitomo. Evaluation of Lateral Diffusion of Lipids in Continuous Membranes between Freestanding and Supported Areas by Fluorescence Recovery after Photobleaching. Langmuir 2019, 35 (36) , 11725-11734. https://doi.org/10.1021/acs.langmuir.9b01595
    3. Won Bae Han, Dong-Hyun Kang, Tae Song Kim. 3D Artificial Cell Membranes as Versatile Platforms for Biological Applications. BioChip Journal 2022, 16 (3) , 215-226. https://doi.org/10.1007/s13206-022-00066-z
    4. Hironori Kageyama, Teng Ma, Madoka Sato, Maki Komiya, Daisuke Tadaki, Ayumi Hirano-Iwata. New Aspects of Bilayer Lipid Membranes for the Analysis of Ion Channel Functions. Membranes 2022, 12 (9) , 863. https://doi.org/10.3390/membranes12090863
    5. Inga Gabriunaite, Ausra Valiuniene, Simonas Ramanavicius, Arunas Ramanavicius. Biosensors Based on Bio-Functionalized Semiconducting Metal Oxides. Critical Reviews in Analytical Chemistry 2022, 21 , 1-16. https://doi.org/10.1080/10408347.2022.2088226
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    7. Kazuto Ogishi, Toshihisa Osaki, Yuya Morimoto, Shoji Takeuchi. 3D printed microfluidic devices for lipid bilayer recordings. Lab on a Chip 2022, 22 (5) , 890-898. https://doi.org/10.1039/D1LC01077H
    8. Minako Hirano, Masahisa Tomita, Chikako Takahashi, Nobuyuki Kawashima, Toru Ide. Development of an automated system to measure ion channel currents using a surface-modified gold probe. Scientific Reports 2021, 11 (1) https://doi.org/10.1038/s41598-021-97237-z
    9. Teng Ma, Madoka Sato, Maki Komiya, Xingyao Feng, Daisuke Tadaki, Ayumi Hirano-Iwata. Advances in Artificial Bilayer Lipid Membranes as a Novel Biosensing Platform: From Drug-screening to Self-assembled Devices. Chemistry Letters 2021, 50 (3) , 418-425. https://doi.org/10.1246/cl.200764
    10. Ryusuke Miyata, Daisuke Tadaki, Daichi Yamaura, Shun Araki, Madoka Sato, Maki Komiya, Teng Ma, Hideaki Yamamoto, Michio Niwano, Ayumi Hirano-Iwata. Parallel Recordings of Transmembrane hERG Channel Currents Based on Solvent-Free Lipid Bilayer Microarray. Micromachines 2021, 12 (1) , 98. https://doi.org/10.3390/mi12010098
    11. Maki Komiya, Miki Kato, Daisuke Tadaki, Teng Ma, Hideaki Yamamoto, Ryugo Tero, Yuzuru Tozawa, Michio Niwano, Ayumi Hirano‐Iwata. Advances in Artificial Cell Membrane Systems as a Platform for Reconstituting Ion Channels. The Chemical Record 2020, 20 (7) , 730-742. https://doi.org/10.1002/tcr.201900094
    12. Yasutaka Tomioka, Shogo Takashima, Masataka Moriya, Hiroshi Shimada, Fumihiko Hirose, Ayumi Hirano-Iwata, Yoshinao Mizugaki. Capacitance extraction method for a free-standing bilayer lipid membrane formed over an aperture in a nanofabricated silicon chip. Japanese Journal of Applied Physics 2020, 59 (SI) , SIIK02. https://doi.org/10.35848/1347-4065/ab79f0
    13. Kenta Imai, Tomoko Horio, Toshiaki Hattori, Kazuaki Sawada, Ryugo Tero. Lipid bilayer formation on an ion image sensor and measurement of time response of potential dependency on ion concentration. Japanese Journal of Applied Physics 2019, 58 (SD) , SDDK06. https://doi.org/10.7567/1347-4065/ab088a
    14. Yasutaka Tomioka, Shogo Takashima, Masataka Moriya, Hiroshi Shimada, Fumihiko Hirose, Ayumi Hirano-Iwata, Yoshinao Mizugaki. Equivalent circuit model modified for free-standing bilayer lipid membranes beyond 1 TΩ. Japanese Journal of Applied Physics 2019, 58 (SD) , SDDK02. https://doi.org/10.7567/1347-4065/ab088c
    15. Maki KOMIYA, Teng MA, Daisuke TADAKI, Ayumi HIRANO-IWATA. Development of an Analytical System for Ion Channel Proteins Based on Artificial Bilayer Lipid Membranes —Screening of Drug Components that Haveing Side Effects on hERG Channels for Personalized Medicine—. BUNSEKI KAGAKU 2018, 67 (12) , 749-760. https://doi.org/10.2116/bunsekikagaku.67.749
    16. Daisuke TADAKI, Daichi YAMAURA, Xingyao FENG, Ayumi HIRANO-IWATA. Evaluation Methods for Drug Side Effects Using Artificial Cell Membranes in Microfabricated Silicon Chips. Seibutsu Butsuri 2018, 58 (6) , 324-327. https://doi.org/10.2142/biophys.58.324

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