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Multiscale compression-induced restructuring of stacked lipid bilayers: From buckling delamination to molecular packing
Lipid membranes in nature adapt and reconfigure to changes in composition, temperature, humidity, and mechanics. For instance, the oscillating mechanical forces on lung cells and alveoli influence membrane synthesis and structure during breathing. However, despite advances in the understanding of li...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9733850/ https://www.ncbi.nlm.nih.gov/pubmed/36490254 http://dx.doi.org/10.1371/journal.pone.0275079 |
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author | Porras-Gómez, Marilyn Kim, Hyunchul Dronadula, Mohan Teja Kambar, Nurila Metellus, Christopher J. B. Aluru, Narayana R. van der Zande, Arend Leal, Cecília |
author_facet | Porras-Gómez, Marilyn Kim, Hyunchul Dronadula, Mohan Teja Kambar, Nurila Metellus, Christopher J. B. Aluru, Narayana R. van der Zande, Arend Leal, Cecília |
author_sort | Porras-Gómez, Marilyn |
collection | PubMed |
description | Lipid membranes in nature adapt and reconfigure to changes in composition, temperature, humidity, and mechanics. For instance, the oscillating mechanical forces on lung cells and alveoli influence membrane synthesis and structure during breathing. However, despite advances in the understanding of lipid membrane phase behavior and mechanics of tissue, there is a critical knowledge gap regarding the response of lipid membranes to micromechanical forces. Most studies of lipid membrane mechanics use supported lipid bilayer systems missing the structural complexity of pulmonary lipids in alveolar membranes comprising multi-bilayer interconnected stacks. Here, we elucidate the collective response of the major component of pulmonary lipids to strain in the form of multi-bilayer stacks supported on flexible elastomer substrates. We utilize X-ray diffraction, scanning probe microscopy, confocal microscopy, and molecular dynamics simulation to show that lipid multilayered films both in gel and fluid states evolve structurally and mechanically in response to compression at multiple length scales. Specifically, compression leads to increased disorder of lipid alkyl chains comparable to the effect of cholesterol on gel phases as a direct result of the formation of nanoscale undulations in the lipid multilayers, also inducing buckling delamination and enhancing multi-bilayer alignment. We propose this cooperative short- and long-range reconfiguration of lipid multilayered films under compression constitutes a mechanism to accommodate stress and substrate topography. Our work raises fundamental insights regarding the adaptability of complex lipid membranes to mechanical stimuli. This is critical to several technologies requiring mechanically reconfigurable surfaces such as the development of electronic devices interfacing biological materials. |
format | Online Article Text |
id | pubmed-9733850 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-97338502022-12-10 Multiscale compression-induced restructuring of stacked lipid bilayers: From buckling delamination to molecular packing Porras-Gómez, Marilyn Kim, Hyunchul Dronadula, Mohan Teja Kambar, Nurila Metellus, Christopher J. B. Aluru, Narayana R. van der Zande, Arend Leal, Cecília PLoS One Research Article Lipid membranes in nature adapt and reconfigure to changes in composition, temperature, humidity, and mechanics. For instance, the oscillating mechanical forces on lung cells and alveoli influence membrane synthesis and structure during breathing. However, despite advances in the understanding of lipid membrane phase behavior and mechanics of tissue, there is a critical knowledge gap regarding the response of lipid membranes to micromechanical forces. Most studies of lipid membrane mechanics use supported lipid bilayer systems missing the structural complexity of pulmonary lipids in alveolar membranes comprising multi-bilayer interconnected stacks. Here, we elucidate the collective response of the major component of pulmonary lipids to strain in the form of multi-bilayer stacks supported on flexible elastomer substrates. We utilize X-ray diffraction, scanning probe microscopy, confocal microscopy, and molecular dynamics simulation to show that lipid multilayered films both in gel and fluid states evolve structurally and mechanically in response to compression at multiple length scales. Specifically, compression leads to increased disorder of lipid alkyl chains comparable to the effect of cholesterol on gel phases as a direct result of the formation of nanoscale undulations in the lipid multilayers, also inducing buckling delamination and enhancing multi-bilayer alignment. We propose this cooperative short- and long-range reconfiguration of lipid multilayered films under compression constitutes a mechanism to accommodate stress and substrate topography. Our work raises fundamental insights regarding the adaptability of complex lipid membranes to mechanical stimuli. This is critical to several technologies requiring mechanically reconfigurable surfaces such as the development of electronic devices interfacing biological materials. Public Library of Science 2022-12-09 /pmc/articles/PMC9733850/ /pubmed/36490254 http://dx.doi.org/10.1371/journal.pone.0275079 Text en © 2022 Porras-Gómez et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Porras-Gómez, Marilyn Kim, Hyunchul Dronadula, Mohan Teja Kambar, Nurila Metellus, Christopher J. B. Aluru, Narayana R. van der Zande, Arend Leal, Cecília Multiscale compression-induced restructuring of stacked lipid bilayers: From buckling delamination to molecular packing |
title | Multiscale compression-induced restructuring of stacked lipid bilayers: From buckling delamination to molecular packing |
title_full | Multiscale compression-induced restructuring of stacked lipid bilayers: From buckling delamination to molecular packing |
title_fullStr | Multiscale compression-induced restructuring of stacked lipid bilayers: From buckling delamination to molecular packing |
title_full_unstemmed | Multiscale compression-induced restructuring of stacked lipid bilayers: From buckling delamination to molecular packing |
title_short | Multiscale compression-induced restructuring of stacked lipid bilayers: From buckling delamination to molecular packing |
title_sort | multiscale compression-induced restructuring of stacked lipid bilayers: from buckling delamination to molecular packing |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9733850/ https://www.ncbi.nlm.nih.gov/pubmed/36490254 http://dx.doi.org/10.1371/journal.pone.0275079 |
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