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Motility provides specific adhesion patterns and improves Listeria monocytogenes invasion into human HEp-2 cells

Listeria monocytogenes is motile at 22°C and non-motile at 37°C. In contrast, expression of L. monocytogenes virulence factors is low at 22°C and up-regulated at 37°C. Here, we studied a character of L. monocytogenes near surface swimming (NSS) motility and its effects on adhesion patterns and invas...

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Autores principales: Abdulkadieva, Mariam M., Sysolyatina, Elena V., Vasilieva, Elena V., Litvinenko, Veronika V., Kalinin, Egor V., Zhukhovitsky, Vladimir G., Shevlyagina, Natalia V., Andreevskaya, Svetlana G., Stanishevskyi, Yaroslav M., Vasiliev, Mikhail M., Petrov, Oleg F., Ermolaeva, Svetlana A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10470941/
https://www.ncbi.nlm.nih.gov/pubmed/37651463
http://dx.doi.org/10.1371/journal.pone.0290842
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author Abdulkadieva, Mariam M.
Sysolyatina, Elena V.
Vasilieva, Elena V.
Litvinenko, Veronika V.
Kalinin, Egor V.
Zhukhovitsky, Vladimir G.
Shevlyagina, Natalia V.
Andreevskaya, Svetlana G.
Stanishevskyi, Yaroslav M.
Vasiliev, Mikhail M.
Petrov, Oleg F.
Ermolaeva, Svetlana A.
author_facet Abdulkadieva, Mariam M.
Sysolyatina, Elena V.
Vasilieva, Elena V.
Litvinenko, Veronika V.
Kalinin, Egor V.
Zhukhovitsky, Vladimir G.
Shevlyagina, Natalia V.
Andreevskaya, Svetlana G.
Stanishevskyi, Yaroslav M.
Vasiliev, Mikhail M.
Petrov, Oleg F.
Ermolaeva, Svetlana A.
author_sort Abdulkadieva, Mariam M.
collection PubMed
description Listeria monocytogenes is motile at 22°C and non-motile at 37°C. In contrast, expression of L. monocytogenes virulence factors is low at 22°C and up-regulated at 37°C. Here, we studied a character of L. monocytogenes near surface swimming (NSS) motility and its effects on adhesion patterns and invasion into epithelial cells. L. monocytogenes and its saprophytic counterpart L. innocua both grown at 22°C showed similar NSS characteristics including individual velocities, trajectory lengths, residence times, and an asymmetric distribution of velocity directions. Similar NSS patterns correlated with similar adhesion patterns. Motile bacteria, including both pathogenic and saprophytic species, showed a preference for adhering to the periphery of epithelial HEp-2 cells. In contrast, non-motile bacteria were evenly distributed across the cell surface, including areas over the nucleus. However, the uneven distribution of motile bacteria did not enhance the invasion into HEp-2 cells unless virulence factor production was up-regulated by the transient shift of the culture to 37°C. Motile L. monocytogenes grown overnight at 22°C and then shifted to 37°C for 2 h expressed invasion factors at the same level and invaded human cells up to five times more efficiently comparatively with non-motile bacteria grown overnight at 37°C. Taken together, obtained results demonstrated that (i) NSS motility and correspondent peripheral location over the cell surface did not depend on L. monocytogenes virulence traits; (ii) motility improved L. monocytogenes invasion into human HEp-2 cells within a few hours after the transition from the ambient temperature to the human body temperature.
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spelling pubmed-104709412023-09-01 Motility provides specific adhesion patterns and improves Listeria monocytogenes invasion into human HEp-2 cells Abdulkadieva, Mariam M. Sysolyatina, Elena V. Vasilieva, Elena V. Litvinenko, Veronika V. Kalinin, Egor V. Zhukhovitsky, Vladimir G. Shevlyagina, Natalia V. Andreevskaya, Svetlana G. Stanishevskyi, Yaroslav M. Vasiliev, Mikhail M. Petrov, Oleg F. Ermolaeva, Svetlana A. PLoS One Research Article Listeria monocytogenes is motile at 22°C and non-motile at 37°C. In contrast, expression of L. monocytogenes virulence factors is low at 22°C and up-regulated at 37°C. Here, we studied a character of L. monocytogenes near surface swimming (NSS) motility and its effects on adhesion patterns and invasion into epithelial cells. L. monocytogenes and its saprophytic counterpart L. innocua both grown at 22°C showed similar NSS characteristics including individual velocities, trajectory lengths, residence times, and an asymmetric distribution of velocity directions. Similar NSS patterns correlated with similar adhesion patterns. Motile bacteria, including both pathogenic and saprophytic species, showed a preference for adhering to the periphery of epithelial HEp-2 cells. In contrast, non-motile bacteria were evenly distributed across the cell surface, including areas over the nucleus. However, the uneven distribution of motile bacteria did not enhance the invasion into HEp-2 cells unless virulence factor production was up-regulated by the transient shift of the culture to 37°C. Motile L. monocytogenes grown overnight at 22°C and then shifted to 37°C for 2 h expressed invasion factors at the same level and invaded human cells up to five times more efficiently comparatively with non-motile bacteria grown overnight at 37°C. Taken together, obtained results demonstrated that (i) NSS motility and correspondent peripheral location over the cell surface did not depend on L. monocytogenes virulence traits; (ii) motility improved L. monocytogenes invasion into human HEp-2 cells within a few hours after the transition from the ambient temperature to the human body temperature. Public Library of Science 2023-08-31 /pmc/articles/PMC10470941/ /pubmed/37651463 http://dx.doi.org/10.1371/journal.pone.0290842 Text en © 2023 Abdulkadieva et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Abdulkadieva, Mariam M.
Sysolyatina, Elena V.
Vasilieva, Elena V.
Litvinenko, Veronika V.
Kalinin, Egor V.
Zhukhovitsky, Vladimir G.
Shevlyagina, Natalia V.
Andreevskaya, Svetlana G.
Stanishevskyi, Yaroslav M.
Vasiliev, Mikhail M.
Petrov, Oleg F.
Ermolaeva, Svetlana A.
Motility provides specific adhesion patterns and improves Listeria monocytogenes invasion into human HEp-2 cells
title Motility provides specific adhesion patterns and improves Listeria monocytogenes invasion into human HEp-2 cells
title_full Motility provides specific adhesion patterns and improves Listeria monocytogenes invasion into human HEp-2 cells
title_fullStr Motility provides specific adhesion patterns and improves Listeria monocytogenes invasion into human HEp-2 cells
title_full_unstemmed Motility provides specific adhesion patterns and improves Listeria monocytogenes invasion into human HEp-2 cells
title_short Motility provides specific adhesion patterns and improves Listeria monocytogenes invasion into human HEp-2 cells
title_sort motility provides specific adhesion patterns and improves listeria monocytogenes invasion into human hep-2 cells
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10470941/
https://www.ncbi.nlm.nih.gov/pubmed/37651463
http://dx.doi.org/10.1371/journal.pone.0290842
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