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Dual Inhibitory Activity of Petroselinic Acid Enriched in Fennel Against Porphyromonas gingivalis

Increasing evidence has shown that a major periodontal pathobiont, Porphyromonas gingivalis, triggers oral dysbiosis leading to deterioration not only of periodontal health, but also of several systemic conditions. In the present study we identified remarkable anti-P. gingivalis activity of Foenicul...

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Autores principales: Yoshino, Nanami, Ikeda, Tsuyoshi, Nakao, Ryoma
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9161081/
https://www.ncbi.nlm.nih.gov/pubmed/35663901
http://dx.doi.org/10.3389/fmicb.2022.816047
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author Yoshino, Nanami
Ikeda, Tsuyoshi
Nakao, Ryoma
author_facet Yoshino, Nanami
Ikeda, Tsuyoshi
Nakao, Ryoma
author_sort Yoshino, Nanami
collection PubMed
description Increasing evidence has shown that a major periodontal pathobiont, Porphyromonas gingivalis, triggers oral dysbiosis leading to deterioration not only of periodontal health, but also of several systemic conditions. In the present study we identified remarkable anti-P. gingivalis activity of Foeniculum vulgare (fennel), an herbal plant used in Asian cuisine as well as in traditional medicine, by screening of 92 extracts prepared from 23 edible plants. The n-hexane-extracted fennel (HEF) showed a rapid lethal action toward P. gingivalis, while it was rather ineffective with a wide range of other oral commensal bacterial species. Morphological analysis using both high-speed atomic force microscopy and field emission scanning electron microscopy revealed that a low concentration of HEF (8 μg/mL) resulted in formation of protruding nanostructures composed of outer membrane vesicle (OMV)-like particles, while a high concentration of HEF (64 μg/mL) induced bacteriolysis with overproduction of OMVs with unusual surface properties. Interestingly, HEF treatment resulted in deprivation of two outer membrane transporter proteins, RagA and RagB, which is essential for nutrient acquisition in P. gingivalis, by extracellularly releasing RagA/RagB-enriched OMVs. Furthermore, HEF showed gingipain-inhibitory activity toward both arginine-specific (Rgps) and lysine-specific (Kgp) gingipains, resulting in blocking oral epithelial cell rounding and the subsequent detachment from culture dishes. Finally, we isolated petroselinic acid as a major bactericide as well as a gingipain inhibitor through a bioassay-guided fractionation of HEF. Taken together, our findings suggest clinical applicability of HEF and petroselinic acid for periodontitis therapy to eliminate P. gingivalis and its major virulence factors on the basis of the dual anti-P. gingivalis activity, i.e., rapid bacteriolysis and gingipain inhibition.
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spelling pubmed-91610812022-06-03 Dual Inhibitory Activity of Petroselinic Acid Enriched in Fennel Against Porphyromonas gingivalis Yoshino, Nanami Ikeda, Tsuyoshi Nakao, Ryoma Front Microbiol Microbiology Increasing evidence has shown that a major periodontal pathobiont, Porphyromonas gingivalis, triggers oral dysbiosis leading to deterioration not only of periodontal health, but also of several systemic conditions. In the present study we identified remarkable anti-P. gingivalis activity of Foeniculum vulgare (fennel), an herbal plant used in Asian cuisine as well as in traditional medicine, by screening of 92 extracts prepared from 23 edible plants. The n-hexane-extracted fennel (HEF) showed a rapid lethal action toward P. gingivalis, while it was rather ineffective with a wide range of other oral commensal bacterial species. Morphological analysis using both high-speed atomic force microscopy and field emission scanning electron microscopy revealed that a low concentration of HEF (8 μg/mL) resulted in formation of protruding nanostructures composed of outer membrane vesicle (OMV)-like particles, while a high concentration of HEF (64 μg/mL) induced bacteriolysis with overproduction of OMVs with unusual surface properties. Interestingly, HEF treatment resulted in deprivation of two outer membrane transporter proteins, RagA and RagB, which is essential for nutrient acquisition in P. gingivalis, by extracellularly releasing RagA/RagB-enriched OMVs. Furthermore, HEF showed gingipain-inhibitory activity toward both arginine-specific (Rgps) and lysine-specific (Kgp) gingipains, resulting in blocking oral epithelial cell rounding and the subsequent detachment from culture dishes. Finally, we isolated petroselinic acid as a major bactericide as well as a gingipain inhibitor through a bioassay-guided fractionation of HEF. Taken together, our findings suggest clinical applicability of HEF and petroselinic acid for periodontitis therapy to eliminate P. gingivalis and its major virulence factors on the basis of the dual anti-P. gingivalis activity, i.e., rapid bacteriolysis and gingipain inhibition. Frontiers Media S.A. 2022-05-19 /pmc/articles/PMC9161081/ /pubmed/35663901 http://dx.doi.org/10.3389/fmicb.2022.816047 Text en Copyright © 2022 Yoshino, Ikeda and Nakao. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Yoshino, Nanami
Ikeda, Tsuyoshi
Nakao, Ryoma
Dual Inhibitory Activity of Petroselinic Acid Enriched in Fennel Against Porphyromonas gingivalis
title Dual Inhibitory Activity of Petroselinic Acid Enriched in Fennel Against Porphyromonas gingivalis
title_full Dual Inhibitory Activity of Petroselinic Acid Enriched in Fennel Against Porphyromonas gingivalis
title_fullStr Dual Inhibitory Activity of Petroselinic Acid Enriched in Fennel Against Porphyromonas gingivalis
title_full_unstemmed Dual Inhibitory Activity of Petroselinic Acid Enriched in Fennel Against Porphyromonas gingivalis
title_short Dual Inhibitory Activity of Petroselinic Acid Enriched in Fennel Against Porphyromonas gingivalis
title_sort dual inhibitory activity of petroselinic acid enriched in fennel against porphyromonas gingivalis
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9161081/
https://www.ncbi.nlm.nih.gov/pubmed/35663901
http://dx.doi.org/10.3389/fmicb.2022.816047
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