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Title: Shiga Toxin Induces Lipid Compression: A Mechanism for Generating Membrane Curvature

Abstract

We report biomembranes are hard to compress laterally, and membrane area compressibility has not been associated with biological processes. Using X-ray surface scattering, we observed that bacterial Shiga toxin compresses lipid packing in a gel phase monolayer upon binding to its cellular receptor, the glycolipid Gb3. This toxin-induced reorganization of lipid packing reached beyond the immediate membrane patch that the protein was bound to, and linkers separating the Gb3 carbohydrate and ceramide moieties modulated the toxin’s capacity to compress the membrane. Within a natural membrane, asymmetric compression of the toxin-bound leaflet could provide a mechanism to initiate narrow membrane bending, as observed upon toxin entry into cells. Such lipid compression and long-range membrane reorganization by glycolipid-binding proteins represent novel concepts in membrane biology that have direct implications for the construction of endocytic pits in clathrin-independent endocytosis.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3];  [4];  [4];  [5]
+ Show Author Affiliations
  1. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States); National Science Foundation (NSF), Alexandria, VA (United States); Univ. of New Mexico, Albuquerque, NM (United States)
  3. Univ. of New Mexico, Albuquerque, NM (United States)
  4. PSL Research Univ., Paris (France)
  5. Los Alamos National Lab. (LANL), Los Alamos, NM (United States); PSL Research Univ., Paris (France)
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States); Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1868228
Report Number(s):
LA-UR-21-22929
Journal ID: ISSN 1530-6984
Grant/Contract Number:  
89233218CNA000001; AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Nano Letters
Additional Journal Information:
Journal Volume: 19; Journal Issue: 10; Journal ID: ISSN 1530-6984
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; biomembrane; Shiga toxin; membrane curvature; endocytosis

Citation Formats

Watkins, Erik B., Majewski, Jaroslaw, Chi, Eva Y., Gao, Haifei, Florent, Jean-Claude, and Johannes, Ludger. Shiga Toxin Induces Lipid Compression: A Mechanism for Generating Membrane Curvature. United States: N. p., 2019. Web. doi:10.1021/acs.nanolett.9b03001.
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Watkins, Erik B., Majewski, Jaroslaw, Chi, Eva Y., Gao, Haifei, Florent, Jean-Claude, & Johannes, Ludger. Shiga Toxin Induces Lipid Compression: A Mechanism for Generating Membrane Curvature. United States. https://doi.org/10.1021/acs.nanolett.9b03001
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Watkins, Erik B., Majewski, Jaroslaw, Chi, Eva Y., Gao, Haifei, Florent, Jean-Claude, and Johannes, Ludger. Fri . "Shiga Toxin Induces Lipid Compression: A Mechanism for Generating Membrane Curvature". United States. https://doi.org/10.1021/acs.nanolett.9b03001. https://www.osti.gov/servlets/purl/1868228.
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@article{osti_1868228,
title = {Shiga Toxin Induces Lipid Compression: A Mechanism for Generating Membrane Curvature},
author = {Watkins, Erik B. and Majewski, Jaroslaw and Chi, Eva Y. and Gao, Haifei and Florent, Jean-Claude and Johannes, Ludger},
abstractNote = {We report biomembranes are hard to compress laterally, and membrane area compressibility has not been associated with biological processes. Using X-ray surface scattering, we observed that bacterial Shiga toxin compresses lipid packing in a gel phase monolayer upon binding to its cellular receptor, the glycolipid Gb3. This toxin-induced reorganization of lipid packing reached beyond the immediate membrane patch that the protein was bound to, and linkers separating the Gb3 carbohydrate and ceramide moieties modulated the toxin’s capacity to compress the membrane. Within a natural membrane, asymmetric compression of the toxin-bound leaflet could provide a mechanism to initiate narrow membrane bending, as observed upon toxin entry into cells. Such lipid compression and long-range membrane reorganization by glycolipid-binding proteins represent novel concepts in membrane biology that have direct implications for the construction of endocytic pits in clathrin-independent endocytosis.},
doi = {10.1021/acs.nanolett.9b03001},
journal = {Nano Letters},
number = 10,
volume = 19,
place = {United States},
year = {Fri Sep 20 00:00:00 EDT 2019},
month = {Fri Sep 20 00:00:00 EDT 2019}
}
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Journal Article:
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Publisher's Version of Record
https://doi.org/10.1021/acs.nanolett.9b03001
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