Programmable Lipid Bilayer Tension–Control Apparatus for Quantitative Mechanobiology

The biological membrane is not just a platform for information processing but also a field of mechanics. The lipid bilayer that constitutes the membrane is an elastic body, generating stress upon deformation, while the membrane protein embedded therein deforms the bilayer through structural changes. Among membrane-protein interplays, various channel species act as tension-current converters for signal transduction, serving as elementary processes in mechanobiology. However, in situ studies in chaotically complex cell membranes are challenging, and characterizing the tension dependency of mechanosensitive channels remains semiquantitative owing to technical limitations. Here, we developed a programmable membrane tension-control apparatus on a lipid bilayer system. This synthetic membrane system [contact bubble bilayer (CBB)] uses pressure to drive bilayer tension changes via the Young-Laplace principle, whereas absolute bilayer tension is monitored in real-time through image analysis of the bubble geometry via the Young principle. Consequently, the mechanical nature of the system permits the implementation of closed-loop feedback control of bilayer tension (tension-clamp CBB), maintaining a constant tension for minutes and allowing stepwise tension changes within a hundred milliseconds in the tension range of 0.8 to 15 mN·m<sup>-1</sup>. We verified the system performance by examining the single-channel behavior of tension-dependent KcsA and TREK-1 potassium channels under scheduled tension time courses prescribed via visual interfaces. The result revealed steady-state activity and dynamic responses to the step tension changes, which are essential to the biophysical characterization of the channels. The apparatus explores a frontier for quantitative mechanobiology studies and promotes the development of a tension-operating experimental robot.

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Publication Details

Journal
ACS Nano
Published
2024-10-22
DOI
https://doi.org/10.1021/acsnano.4c09017
Citations
6
Primary Topic
Lipid Membrane Structure and Behavior
Type
article
Field-Weighted Citation Impact
1.40

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article

Programmable Lipid Bilayer Tension–Control Apparatus for Quantitative Mechanobiology

Yuka Matsuki, Takahisa Maki, Masayuki Iwamoto, Shigetoshi Oiki et al.
6 citations
ACS Nano
Lipid Membrane Structure and Behavior
1.40
article

Programmable Lipid Bilayer Tension–Control Apparatus for Quantitative Mechanobiology

Yuka Matsuki, Takahisa Maki, Masayuki Iwamoto, Shigetoshi Oiki, Toshiyuki Yoshida, Masako Takashima
article en
6 citations

Abstract

The biological membrane is not just a platform for information processing but also a field of mechanics. The lipid bilayer that constitutes the membrane is an elastic body, generating stress upon deformation, while the membrane protein embedded therein deforms the bilayer through structural changes. Among membrane-protein interplays, various channel species act as tension-current converters for signal transduction, serving as elementary processes in mechanobiology. However, in situ studies in chaotically complex cell membranes are challenging, and characterizing the tension dependency of mechanosensitive channels remains semiquantitative owing to technical limitations. Here, we developed a programmable membrane tension-control apparatus on a lipid bilayer system. This synthetic membrane system [contact bubble bilayer (CBB)] uses pressure to drive bilayer tension changes via the Young-Laplace principle, whereas absolute bilayer tension is monitored in real-time through image analysis of the bubble geometry via the Young principle. Consequently, the mechanical nature of the system permits the implementation of closed-loop feedback control of bilayer tension (tension-clamp CBB), maintaining a constant tension for minutes and allowing stepwise tension changes within a hundred milliseconds in the tension range of 0.8 to 15 mN·m<sup>-1</sup>. We verified the system performance by examining the single-channel behavior of tension-dependent KcsA and TREK-1 potassium channels under scheduled tension time courses prescribed via visual interfaces. The result revealed steady-state activity and dynamic responses to the step tension changes, which are essential to the biophysical characterization of the channels. The apparatus explores a frontier for quantitative mechanobiology studies and promotes the development of a tension-operating experimental robot.

ACS NanoVol. 18(44)
University of Fukui (JP), Laboratoire d’Imagerie Biomédicale (FR)
University of Fukui, Japan Society for the Promotion of Science
Openalex Percentile: Top 18%
Lipid Membrane Structure and Behavior
1.40
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