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Insect fungal pathogens secrete a cell wall-associated glucanase that acts to help avoid recognition by the host immune system

Fungal insect pathogens have evolved diverse mechanisms to evade host immune recognition and defense responses. However, identification of fungal factors involved in host immune evasion during cuticular penetration and subsequent hemocoel colonization remains limited. Here, we report that the entomo...

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Autores principales: Wang, Huifang, Lu, Zhuoyue, Keyhani, Nemat O., Deng, Juan, Zhao, Xin, Huang, Shuaishuai, Luo, Zhibing, Jin, Kai, Zhang, Yongjun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441804/
https://www.ncbi.nlm.nih.gov/pubmed/37556475
http://dx.doi.org/10.1371/journal.ppat.1011578
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author Wang, Huifang
Lu, Zhuoyue
Keyhani, Nemat O.
Deng, Juan
Zhao, Xin
Huang, Shuaishuai
Luo, Zhibing
Jin, Kai
Zhang, Yongjun
author_facet Wang, Huifang
Lu, Zhuoyue
Keyhani, Nemat O.
Deng, Juan
Zhao, Xin
Huang, Shuaishuai
Luo, Zhibing
Jin, Kai
Zhang, Yongjun
author_sort Wang, Huifang
collection PubMed
description Fungal insect pathogens have evolved diverse mechanisms to evade host immune recognition and defense responses. However, identification of fungal factors involved in host immune evasion during cuticular penetration and subsequent hemocoel colonization remains limited. Here, we report that the entomopathogenic fungus Beauveria bassiana expresses an endo-β-1,3-glucanase (BbEng1) that functions in helping cells evade insect immune recognition/ responses. BbEng1 was specifically expressed during infection, in response to host cuticle and hemolymph, and in the presence of osmotic or oxidative stress. BbEng1 was localized to the fungal cell surface/ cell wall, where it acts to remodel the cell wall pathogen associated molecular patterns (PAMPs) that can trigger host defenses, thus facilitating fungal cell evasion of host immune defenses. BbEng1 was secreted where it could bind to fungal cells. Cell wall β-1,3-glucan levels were unchanged in ΔBbEng1 cells derived from in vitro growth media, but was elevated in hyphal bodies, whereas glucan levels were reduced in most cell types derived from the BbEng1 overexpressing strain (BbEng1(OE)). The BbEng1(OE) strain proliferated more rapidly in the host hemocoel and displayed higher virulence as compared to the wild type parent. Overexpression of their respective Eng1 homologs or of BbEng1 in the insect fungal pathogens, Metarhizium robertsii and M. acridum also resulted in increased virulence. Our data support a mechanism by which BbEng1 helps the fungal pathogen to evade host immune surveillance by decreasing cell wall glucan PAMPs, promoting successful fungal mycosis.
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spelling pubmed-104418042023-08-22 Insect fungal pathogens secrete a cell wall-associated glucanase that acts to help avoid recognition by the host immune system Wang, Huifang Lu, Zhuoyue Keyhani, Nemat O. Deng, Juan Zhao, Xin Huang, Shuaishuai Luo, Zhibing Jin, Kai Zhang, Yongjun PLoS Pathog Research Article Fungal insect pathogens have evolved diverse mechanisms to evade host immune recognition and defense responses. However, identification of fungal factors involved in host immune evasion during cuticular penetration and subsequent hemocoel colonization remains limited. Here, we report that the entomopathogenic fungus Beauveria bassiana expresses an endo-β-1,3-glucanase (BbEng1) that functions in helping cells evade insect immune recognition/ responses. BbEng1 was specifically expressed during infection, in response to host cuticle and hemolymph, and in the presence of osmotic or oxidative stress. BbEng1 was localized to the fungal cell surface/ cell wall, where it acts to remodel the cell wall pathogen associated molecular patterns (PAMPs) that can trigger host defenses, thus facilitating fungal cell evasion of host immune defenses. BbEng1 was secreted where it could bind to fungal cells. Cell wall β-1,3-glucan levels were unchanged in ΔBbEng1 cells derived from in vitro growth media, but was elevated in hyphal bodies, whereas glucan levels were reduced in most cell types derived from the BbEng1 overexpressing strain (BbEng1(OE)). The BbEng1(OE) strain proliferated more rapidly in the host hemocoel and displayed higher virulence as compared to the wild type parent. Overexpression of their respective Eng1 homologs or of BbEng1 in the insect fungal pathogens, Metarhizium robertsii and M. acridum also resulted in increased virulence. Our data support a mechanism by which BbEng1 helps the fungal pathogen to evade host immune surveillance by decreasing cell wall glucan PAMPs, promoting successful fungal mycosis. Public Library of Science 2023-08-09 /pmc/articles/PMC10441804/ /pubmed/37556475 http://dx.doi.org/10.1371/journal.ppat.1011578 Text en © 2023 Wang 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
Wang, Huifang
Lu, Zhuoyue
Keyhani, Nemat O.
Deng, Juan
Zhao, Xin
Huang, Shuaishuai
Luo, Zhibing
Jin, Kai
Zhang, Yongjun
Insect fungal pathogens secrete a cell wall-associated glucanase that acts to help avoid recognition by the host immune system
title Insect fungal pathogens secrete a cell wall-associated glucanase that acts to help avoid recognition by the host immune system
title_full Insect fungal pathogens secrete a cell wall-associated glucanase that acts to help avoid recognition by the host immune system
title_fullStr Insect fungal pathogens secrete a cell wall-associated glucanase that acts to help avoid recognition by the host immune system
title_full_unstemmed Insect fungal pathogens secrete a cell wall-associated glucanase that acts to help avoid recognition by the host immune system
title_short Insect fungal pathogens secrete a cell wall-associated glucanase that acts to help avoid recognition by the host immune system
title_sort insect fungal pathogens secrete a cell wall-associated glucanase that acts to help avoid recognition by the host immune system
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441804/
https://www.ncbi.nlm.nih.gov/pubmed/37556475
http://dx.doi.org/10.1371/journal.ppat.1011578
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