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

Erik B. Watkins; Jaroslaw Majewski; Eva Y. Chi; Haifei Gao; Jean Claude Florent; Ludger Johannes

doi:10.1021/acs.nanolett.9b03001

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

Erik B. Watkins
, Jaroslaw Majewski
, Eva Y. Chi
, Haifei Gao
, Jean Claude Florent
, Ludger Johannes

Research output: Contribution to journal › Article › peer-review

25 Scopus citations

Abstract

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.

Original language	English
Pages (from-to)	7365-7369
Number of pages	5
Journal	Nano Letters
Volume	19
Issue number	10
DOIs	https://doi.org/10.1021/acs.nanolett.9b03001
State	Published - Oct 9 2019
Externally published	Yes

Funding

This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under contract no. DE-AC02-06CH11357. We would also like to acknowledge Dr. Wei Bu for help with the reflectivity and grazing incidence diffraction experiments. Work was supported by grants from the Agence Nationale de la Recherche (ANR-16-CE23-0005-02, ANR-19-CE13-0001-01), Human Frontier Science Program grant RGP0029-2014, European Research Council advanced grant (project 340485), European Union program H2020-MSCA-ITN-2014 BIOPOL, and the Swedish Research Council. NSF provided support for J.M. to contribute to this project through their Independent Research and Development program. Any opinion, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.

Keywords

Biomembrane
Shiga toxin
endocytosis
membrane curvature

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10.1021/acs.nanolett.9b03001

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title = "Shiga Toxin Induces Lipid Compression: A Mechanism for Generating Membrane Curvature",

abstract = "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.",

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author = "Watkins, \{Erik B.\} and Jaroslaw Majewski and Chi, \{Eva Y.\} and Haifei Gao and Florent, \{Jean Claude\} and Ludger Johannes",

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doi = "10.1021/acs.nanolett.9b03001",

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AU - Watkins, Erik B.

AU - Majewski, Jaroslaw

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AU - Gao, Haifei

AU - Florent, Jean Claude

AU - Johannes, Ludger

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AB - 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.

KW - Biomembrane

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KW - endocytosis

KW - membrane curvature

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

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Keywords

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