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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2018-08-01
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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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