IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43892-x.html
   My bibliography  Save this article

Nonuniversal impact of cholesterol on membranes mobility, curvature sensing and elasticity

Author

Listed:
  • Matthias Pöhnl

    (Friedrich-Alexander-Universität Erlangen-Nürnberg)

  • Marius F. W. Trollmann

    (Friedrich-Alexander-Universität Erlangen-Nürnberg
    Erlangen National High Perfomance Computing Center (NHR@FAU))

  • Rainer A. Böckmann

    (Friedrich-Alexander-Universität Erlangen-Nürnberg
    Erlangen National High Perfomance Computing Center (NHR@FAU))

Abstract

Biological membranes, composed mainly of phospholipids and cholesterol, play a vital role as cellular barriers. They undergo localized reshaping in response to environmental cues and protein interactions, with the energetics of deformations crucial for exerting biological functions. This study investigates the non-universal role of cholesterol on the structure and elasticity of saturated and unsaturated lipid membranes. Our study uncovers a highly cooperative relationship between thermal membrane bending and local cholesterol redistribution, with cholesterol showing a strong preference for the compressed membrane leaflet. Remarkably, in unsaturated membranes, increased cholesterol mobility enhances cooperativity, resulting in membrane softening despite membrane thickening and lipid compression caused by cholesterol. These findings elucidate the intricate interplay between thermodynamic forces and local molecular interactions that govern collective properties of membranes.

Suggested Citation

  • Matthias Pöhnl & Marius F. W. Trollmann & Rainer A. Böckmann, 2023. "Nonuniversal impact of cholesterol on membranes mobility, curvature sensing and elasticity," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43892-x
    DOI: 10.1038/s41467-023-43892-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43892-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43892-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Kai Simons & Elina Ikonen, 1997. "Functional rafts in cell membranes," Nature, Nature, vol. 387(6633), pages 569-572, June.
    2. Jacopo Frallicciardi & Josef Melcr & Pareskevi Siginou & Siewert J. Marrink & Bert Poolman, 2022. "Membrane thickness, lipid phase and sterol type are determining factors in the permeability of membranes to small solutes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Xuzhong Yang & Chao Lin & Xudong Chen & Shouqin Li & Xueming Li & Bailong Xiao, 2022. "Structure deformation and curvature sensing of PIEZO1 in lipid membranes," Nature, Nature, vol. 604(7905), pages 377-383, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Haoqing Jerry Wang & Yao Wang & Seyed Sajad Mirjavadi & Tomas Andersen & Laura Moldovan & Parham Vatankhah & Blake Russell & Jasmine Jin & Zijing Zhou & Qing Li & Charles D. Cox & Qian Peter Su & Lini, 2024. "Microscale geometrical modulation of PIEZO1 mediated mechanosensing through cytoskeletal redistribution," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Danchin, Antoine, 1999. "From function to sequence, an integrated view of the genome texts," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 273(1), pages 92-98.
    3. Marta Ukleja & Lara Kricks & Gabriel Torrens & Ilaria Peschiera & Ines Rodrigues-Lopes & Marcin Krupka & Julia García-Fernández & Roberto Melero & Rosa Campo & Ana Eulalio & André Mateus & María López, 2024. "Flotillin-mediated stabilization of unfolded proteins in bacterial membrane microdomains," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    4. Sara Baratchi & Habiba Danish & Chanly Chheang & Ying Zhou & Angela Huang & Austin Lai & Manijeh Khanmohammadi & Kylie M. Quinn & Khashayar Khoshmanesh & Karlheinz Peter, 2024. "Piezo1 expression in neutrophils regulates shear-induced NETosis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Arun Shivanandan & Jayakrishnan Unnikrishnan & Aleksandra Radenovic, 2015. "Accounting for Limited Detection Efficiency and Localization Precision in Cluster Analysis in Single Molecule Localization Microscopy," PLOS ONE, Public Library of Science, vol. 10(3), pages 1-15, March.
    6. Jonathan Mount & Grigory Maksaev & Brock T. Summers & James A. J. Fitzpatrick & Peng Yuan, 2022. "Structural basis for mechanotransduction in a potassium-dependent mechanosensitive ion channel," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    7. Haruka Kemmoku & Kanoko Takahashi & Kojiro Mukai & Toshiki Mori & Koichiro M. Hirosawa & Fumika Kiku & Yasunori Uchida & Yoshihiko Kuchitsu & Yu Nishioka & Masaaki Sawa & Takuma Kishimoto & Kazuma Tan, 2024. "Single-molecule localization microscopy reveals STING clustering at the trans-Golgi network through palmitoylation-dependent accumulation of cholesterol," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Daniel P. Arnold & Yaxin Xu & Sho C. Takatori, 2023. "Antibody binding reports spatial heterogeneities in cell membrane organization," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    9. Shilong Yang & Xinwen Miao & Steven Arnold & Boxuan Li & Alan T. Ly & Huan Wang & Matthew Wang & Xiangfu Guo & Medha M. Pathak & Wenting Zhao & Charles D. Cox & Zheng Shi, 2022. "Membrane curvature governs the distribution of Piezo1 in live cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    10. Xinchun Zhou & Jinghe Mao & Junmei Ai & Youping Deng & Mary R Roth & Charles Pound & Jeffrey Henegar & Ruth Welti & Steven A Bigler, 2012. "Identification of Plasma Lipid Biomarkers for Prostate Cancer by Lipidomics and Bioinformatics," PLOS ONE, Public Library of Science, vol. 7(11), pages 1-11, November.
    11. Luis O. Romero & Rebeca Caires & A. Kaitlyn Victor & Juanma Ramirez & Francisco J. Sierra-Valdez & Patrick Walsh & Vincent Truong & Jungsoo Lee & Ugo Mayor & Lawrence T. Reiter & Valeria Vásquez & Jul, 2023. "Linoleic acid improves PIEZO2 dysfunction in a mouse model of Angelman Syndrome," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    12. Jeong Han Lee & Maria C. Perez-Flores & Seojin Park & Hyo Jeong Kim & Yingying Chen & Mincheol Kang & Jennifer Kersigo & Jinsil Choi & Phung N. Thai & Ryan L. Woltz & Dolores Columba Perez-Flores & Gu, 2024. "The Piezo channel is a mechano-sensitive complex component in the mammalian inner ear hair cell," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    13. Yuanyue Shan & Mengmeng Zhang & Meiyu Chen & Xinyi Guo & Ying Li & Mingfeng Zhang & Duanqing Pei, 2024. "Activation mechanisms of dimeric mechanosensitive OSCA/TMEM63 channels," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. Anne M. Kiirikki & Hanne S. Antila & Lara S. Bort & Pavel Buslaev & Fernando Favela-Rosales & Tiago Mendes Ferreira & Patrick F. J. Fuchs & Rebeca Garcia-Fandino & Ivan Gushchin & Batuhan Kav & Norber, 2024. "Overlay databank unlocks data-driven analyses of biomolecules for all," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    15. Talia Zeppelin & Lucy Kate Ladefoged & Steffen Sinning & Xavier Periole & Birgit Schiøtt, 2018. "A direct interaction of cholesterol with the dopamine transporter prevents its out-to-inward transition," PLOS Computational Biology, Public Library of Science, vol. 14(1), pages 1-24, January.
    16. Francisco Andrés Peralta & Mélaine Balcon & Adeline Martz & Deniza Biljali & Federico Cevoli & Benoit Arnould & Antoine Taly & Thierry Chataigneau & Thomas Grutter, 2023. "Optical control of PIEZO1 channels," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    17. D’Emiliano, D. & Casieri, C. & Paci, M. & De Luca, F., 2007. "Detection of ganglioside clustering in DOPC bilayers by 1H-NMR spectroscopy," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 374(1), pages 293-303.
    18. Jingying Zhang & Grigory Maksaev & Peng Yuan, 2023. "Open structure and gating of the Arabidopsis mechanosensitive ion channel MSL10," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    19. Alexander P. Fellows & Ben John & Martin Wolf & Martin Thämer, 2024. "Spiral packing and chiral selectivity in model membranes probed by phase-resolved sum-frequency generation microscopy," Nature Communications, Nature, vol. 15(1), pages 1-10, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43892-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.