Differential interactions of bacterial lipopolysaccharides with lipid membranes: implications for TRPA1-mediated chemosensation

Abstract Bacterial lipopolysaccharides (LPS) activate the TRPA1 cation channels in sensory neurons, leading to acute pain and inflammation in mice and to aversive behaviors in fruit flies. However, the precise mechanisms underlying this effect remain elusive. Here we assessed the hypothesis that TRP...

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Main Authors: Justyna B. Startek, Karel Talavera, Thomas Voets, Yeranddy A. Alpizar
Format: Article
Language:English
Published: Nature Publishing Group 2018-08-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-018-30534-2
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spelling doaj-01f0e445cd9540058b3e232f789a390d2020-12-08T04:33:16ZengNature Publishing GroupScientific Reports2045-23222018-08-018111110.1038/s41598-018-30534-2Differential interactions of bacterial lipopolysaccharides with lipid membranes: implications for TRPA1-mediated chemosensationJustyna B. Startek0Karel Talavera1Thomas Voets2Yeranddy A. Alpizar3Laboratory of Ion Channel Research, Department of Cellular and Molecular Medicine. KU Leuven; VIB Center for Brain & Disease ResearchLaboratory of Ion Channel Research, Department of Cellular and Molecular Medicine. KU Leuven; VIB Center for Brain & Disease ResearchLaboratory of Ion Channel Research, Department of Cellular and Molecular Medicine. KU Leuven; VIB Center for Brain & Disease ResearchLaboratory of Ion Channel Research, Department of Cellular and Molecular Medicine. KU Leuven; VIB Center for Brain & Disease ResearchAbstract Bacterial lipopolysaccharides (LPS) activate the TRPA1 cation channels in sensory neurons, leading to acute pain and inflammation in mice and to aversive behaviors in fruit flies. However, the precise mechanisms underlying this effect remain elusive. Here we assessed the hypothesis that TRPA1 is activated by mechanical perturbations induced upon LPS insertion in the plasma membrane. We asked whether the effects of different LPS on TRPA1 relate to their ability to induce mechanical alterations in artificial and cellular membranes. We found that LPS from E. coli, but not from S. minnesota, activates TRPA1. We then assessed the effects of these LPS on lipid membranes using dyes whose fluorescence properties change upon alteration of the local lipid environment. E. coli LPS was more effective than S. minnesota LPS in shifting Laurdan’s emission spectrum towards lower wavelengths, increasing the fluorescence anisotropy of diphenylhexatriene and reducing the fluorescence intensity of merocyanine 540. These data indicate that E. coli LPS induces stronger changes in the local lipid environment than S. minnesota LPS, paralleling its distinct ability to activate TRPA1. Our findings indicate that LPS activate TRPA1 by producing mechanical perturbations in the plasma membrane and suggest that TRPA1-mediated chemosensation may result from primary mechanosensory mechanisms.https://doi.org/10.1038/s41598-018-30534-2
collection DOAJ
language English
format Article
sources DOAJ
author Justyna B. Startek
Karel Talavera
Thomas Voets
Yeranddy A. Alpizar
spellingShingle Justyna B. Startek
Karel Talavera
Thomas Voets
Yeranddy A. Alpizar
Differential interactions of bacterial lipopolysaccharides with lipid membranes: implications for TRPA1-mediated chemosensation
Scientific Reports
author_facet Justyna B. Startek
Karel Talavera
Thomas Voets
Yeranddy A. Alpizar
author_sort Justyna B. Startek
title Differential interactions of bacterial lipopolysaccharides with lipid membranes: implications for TRPA1-mediated chemosensation
title_short Differential interactions of bacterial lipopolysaccharides with lipid membranes: implications for TRPA1-mediated chemosensation
title_full Differential interactions of bacterial lipopolysaccharides with lipid membranes: implications for TRPA1-mediated chemosensation
title_fullStr Differential interactions of bacterial lipopolysaccharides with lipid membranes: implications for TRPA1-mediated chemosensation
title_full_unstemmed Differential interactions of bacterial lipopolysaccharides with lipid membranes: implications for TRPA1-mediated chemosensation
title_sort differential interactions of bacterial lipopolysaccharides with lipid membranes: implications for trpa1-mediated chemosensation
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2018-08-01
description Abstract Bacterial lipopolysaccharides (LPS) activate the TRPA1 cation channels in sensory neurons, leading to acute pain and inflammation in mice and to aversive behaviors in fruit flies. However, the precise mechanisms underlying this effect remain elusive. Here we assessed the hypothesis that TRPA1 is activated by mechanical perturbations induced upon LPS insertion in the plasma membrane. We asked whether the effects of different LPS on TRPA1 relate to their ability to induce mechanical alterations in artificial and cellular membranes. We found that LPS from E. coli, but not from S. minnesota, activates TRPA1. We then assessed the effects of these LPS on lipid membranes using dyes whose fluorescence properties change upon alteration of the local lipid environment. E. coli LPS was more effective than S. minnesota LPS in shifting Laurdan’s emission spectrum towards lower wavelengths, increasing the fluorescence anisotropy of diphenylhexatriene and reducing the fluorescence intensity of merocyanine 540. These data indicate that E. coli LPS induces stronger changes in the local lipid environment than S. minnesota LPS, paralleling its distinct ability to activate TRPA1. Our findings indicate that LPS activate TRPA1 by producing mechanical perturbations in the plasma membrane and suggest that TRPA1-mediated chemosensation may result from primary mechanosensory mechanisms.
url https://doi.org/10.1038/s41598-018-30534-2
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