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Acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium Cutibacterium acnes

Cutibacterium acnes is a pathogenic bacterium that cause inflammatory diseases of the skin and intervertebral discs. The immune activation induced by C. acnes requires multiple cellular responses in the host. Silkworm, an invertebrate, generates melanin by phenoloxidase upon recognizing bacterial or...

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Autores principales: Matsumoto, Yasuhiko, Sato, Eri, Sugita, Takashi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9512201/
https://www.ncbi.nlm.nih.gov/pubmed/36155485
http://dx.doi.org/10.1371/journal.pone.0271420
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author Matsumoto, Yasuhiko
Sato, Eri
Sugita, Takashi
author_facet Matsumoto, Yasuhiko
Sato, Eri
Sugita, Takashi
author_sort Matsumoto, Yasuhiko
collection PubMed
description Cutibacterium acnes is a pathogenic bacterium that cause inflammatory diseases of the skin and intervertebral discs. The immune activation induced by C. acnes requires multiple cellular responses in the host. Silkworm, an invertebrate, generates melanin by phenoloxidase upon recognizing bacterial or fungal components. Therefore, the melanization reaction can be used as an indicator of innate immune activation. A silkworm infection model was developed for evaluating the virulence of C. acnes, but a system for evaluating the induction of innate immunity by C. acnes using melanization as an indicator has not yet been established. Here we demonstrated that C. acnes rapidly causes melanization of the silkworm hemolymph. On the other hand, Staphylococcus aureus, a gram-positive bacterium identical to C. acnes, does not cause immediate melanization. Even injection of heat-killed C. acnes cells caused melanization of the silkworm hemolymph. DNase, RNase, and protease treatment of the heat-treated C. acnes cells did not decrease the silkworm hemolymph melanization. Treatment with peptidoglycan-degrading enzymes, such as lysostaphin and lysozyme, however, decreased the induction of melanization by the heat-treated C. acnes cells. These findings suggest that silkworm hemolymph melanization may be a useful indicator to evaluate innate immune activation by C. acnes and that C. acnes peptidoglycans are involved in the induction of innate immunity in silkworms.
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spelling pubmed-95122012022-09-27 Acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium Cutibacterium acnes Matsumoto, Yasuhiko Sato, Eri Sugita, Takashi PLoS One Research Article Cutibacterium acnes is a pathogenic bacterium that cause inflammatory diseases of the skin and intervertebral discs. The immune activation induced by C. acnes requires multiple cellular responses in the host. Silkworm, an invertebrate, generates melanin by phenoloxidase upon recognizing bacterial or fungal components. Therefore, the melanization reaction can be used as an indicator of innate immune activation. A silkworm infection model was developed for evaluating the virulence of C. acnes, but a system for evaluating the induction of innate immunity by C. acnes using melanization as an indicator has not yet been established. Here we demonstrated that C. acnes rapidly causes melanization of the silkworm hemolymph. On the other hand, Staphylococcus aureus, a gram-positive bacterium identical to C. acnes, does not cause immediate melanization. Even injection of heat-killed C. acnes cells caused melanization of the silkworm hemolymph. DNase, RNase, and protease treatment of the heat-treated C. acnes cells did not decrease the silkworm hemolymph melanization. Treatment with peptidoglycan-degrading enzymes, such as lysostaphin and lysozyme, however, decreased the induction of melanization by the heat-treated C. acnes cells. These findings suggest that silkworm hemolymph melanization may be a useful indicator to evaluate innate immune activation by C. acnes and that C. acnes peptidoglycans are involved in the induction of innate immunity in silkworms. Public Library of Science 2022-09-26 /pmc/articles/PMC9512201/ /pubmed/36155485 http://dx.doi.org/10.1371/journal.pone.0271420 Text en © 2022 Matsumoto 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
Matsumoto, Yasuhiko
Sato, Eri
Sugita, Takashi
Acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium Cutibacterium acnes
title Acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium Cutibacterium acnes
title_full Acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium Cutibacterium acnes
title_fullStr Acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium Cutibacterium acnes
title_full_unstemmed Acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium Cutibacterium acnes
title_short Acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium Cutibacterium acnes
title_sort acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium cutibacterium acnes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9512201/
https://www.ncbi.nlm.nih.gov/pubmed/36155485
http://dx.doi.org/10.1371/journal.pone.0271420
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