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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Main Authors: Yasuhiko Matsumoto, Eri Sato, Takashi Sugita
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0271420
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author Yasuhiko Matsumoto
Eri Sato
Takashi Sugita
author_facet Yasuhiko Matsumoto
Eri Sato
Takashi Sugita
author_sort Yasuhiko Matsumoto
collection DOAJ
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 doaj.art-0ff8d6fe642e4874a26f532025274e252022-12-22T03:49:07ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-01179e027142010.1371/journal.pone.0271420Acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium Cutibacterium acnes.Yasuhiko MatsumotoEri SatoTakashi SugitaCutibacterium 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.https://doi.org/10.1371/journal.pone.0271420
spellingShingle Yasuhiko Matsumoto
Eri Sato
Takashi Sugita
Acute melanization of silkworm hemolymph by peptidoglycans of the human commensal bacterium Cutibacterium acnes.
PLoS ONE
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
url https://doi.org/10.1371/journal.pone.0271420
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