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Small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp

Small antibacterial effectors, including lysozymes, lectins, and antimicrobial peptides, are key regulators of intestinal immunity. However, whether there is coordination among them during regulation is an interesting, but largely unknown, issue. In the present study, we revealed that small effector...

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Autores principales: Liu, Ping-Ping, Wei, Zhe, Cheng, Zi-Hua, Wang, Xian-Wei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9683584/
https://www.ncbi.nlm.nih.gov/pubmed/36417479
http://dx.doi.org/10.1371/journal.ppat.1010967
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author Liu, Ping-Ping
Wei, Zhe
Cheng, Zi-Hua
Wang, Xian-Wei
author_facet Liu, Ping-Ping
Wei, Zhe
Cheng, Zi-Hua
Wang, Xian-Wei
author_sort Liu, Ping-Ping
collection PubMed
description Small antibacterial effectors, including lysozymes, lectins, and antimicrobial peptides, are key regulators of intestinal immunity. However, whether there is coordination among them during regulation is an interesting, but largely unknown, issue. In the present study, we revealed that small effectors synergistically regulate peptidoglycan-derived intestinal immunity in the kuruma shrimp, Marsupenaeus japonicus. A C-type lysozyme (LysC) was screened as a responsive factor for the intestine-bacteria interaction. LysC functions to restrict intestinal bacteria, mainly by cleaving Photobacterium damselae peptidoglycan to generate muropeptides which are powerful stimulators that induce anti-lipopolysaccharides factor B1 (AlfB1), an effective bactericidal peptide. The muropeptides also induce a C-type lectin (Ctl24), which recognizes peptidoglycan and coats bacteria. By counteracting LysC-mediated muropeptide release and AlfB1’s bactericidal activity, Ctl24 prevents the continuous elimination of intestinal bacteria. Therefore, this study demonstrates a mechanism by which small immune effectors coordinate to achieve intestinal homeostasis, and provides new insights into peptidoglycan-derived intestinal immunity in invertebrates.
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spelling pubmed-96835842022-11-24 Small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp Liu, Ping-Ping Wei, Zhe Cheng, Zi-Hua Wang, Xian-Wei PLoS Pathog Research Article Small antibacterial effectors, including lysozymes, lectins, and antimicrobial peptides, are key regulators of intestinal immunity. However, whether there is coordination among them during regulation is an interesting, but largely unknown, issue. In the present study, we revealed that small effectors synergistically regulate peptidoglycan-derived intestinal immunity in the kuruma shrimp, Marsupenaeus japonicus. A C-type lysozyme (LysC) was screened as a responsive factor for the intestine-bacteria interaction. LysC functions to restrict intestinal bacteria, mainly by cleaving Photobacterium damselae peptidoglycan to generate muropeptides which are powerful stimulators that induce anti-lipopolysaccharides factor B1 (AlfB1), an effective bactericidal peptide. The muropeptides also induce a C-type lectin (Ctl24), which recognizes peptidoglycan and coats bacteria. By counteracting LysC-mediated muropeptide release and AlfB1’s bactericidal activity, Ctl24 prevents the continuous elimination of intestinal bacteria. Therefore, this study demonstrates a mechanism by which small immune effectors coordinate to achieve intestinal homeostasis, and provides new insights into peptidoglycan-derived intestinal immunity in invertebrates. Public Library of Science 2022-11-23 /pmc/articles/PMC9683584/ /pubmed/36417479 http://dx.doi.org/10.1371/journal.ppat.1010967 Text en © 2022 Liu 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
Liu, Ping-Ping
Wei, Zhe
Cheng, Zi-Hua
Wang, Xian-Wei
Small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp
title Small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp
title_full Small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp
title_fullStr Small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp
title_full_unstemmed Small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp
title_short Small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp
title_sort small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9683584/
https://www.ncbi.nlm.nih.gov/pubmed/36417479
http://dx.doi.org/10.1371/journal.ppat.1010967
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