<named-content content-type="genus-species">Bacteroides fragilis</named-content> Strain ZY-312 Defense against <named-content content-type="genus-species">Cronobacter sakazakii</named-content>-Induced Necrotizing Enterocolitis <italic toggle="yes">In Vitro</italic> and in a Neonatal Rat Model

ABSTRACT Cronobacter sakazakii is an important pathogen associated with the development of necrotizing enterocolitis (NEC), infant sepsis, and meningitis. Several randomized prospective clinical trials demonstrated that oral probiotics could decrease the incidence of NEC. Previously, we isolated and...

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Autores principales:	Hongying Fan, Zhenhui Chen, Ruqin Lin, Yangyang Liu, Xianbo Wu, Santhosh Puthiyakunnon, Ye Wang, Bo Zhu, Qiwei Zhang, Yang Bai, Fachao Zhi
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	apoptosis Bacteroides fragilis Cronobacter sakazakii inflammasomes necrotizing enterocolitis pyroptosis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2746e2807e214482ac141d2a8b47b1a1
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spelling	oai:doaj.org-article:2746e2807e214482ac141d2a8b47b1a12021-12-02T18:39:47Z<named-content content-type="genus-species">Bacteroides fragilis</named-content> Strain ZY-312 Defense against <named-content content-type="genus-species">Cronobacter sakazakii</named-content>-Induced Necrotizing Enterocolitis <italic toggle="yes">In Vitro</italic> and in a Neonatal Rat Model10.1128/mSystems.00305-192379-5077https://doaj.org/article/2746e2807e214482ac141d2a8b47b1a12019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00305-19https://doaj.org/toc/2379-5077ABSTRACT Cronobacter sakazakii is an important pathogen associated with the development of necrotizing enterocolitis (NEC), infant sepsis, and meningitis. Several randomized prospective clinical trials demonstrated that oral probiotics could decrease the incidence of NEC. Previously, we isolated and characterized a novel probiotic, Bacteroides fragilis strain ZY-312. However, it remains unclear how ZY-312 protects the host from the effects of C. sakazakii infection. To understand the underlying mechanisms triggering the probiotic effects, we tested the hypothesis that there was cross talk between probiotics/probiotics-modulated microbiota and the local immune system, governed by the permeability of the intestinal mucosa, using in vitro and in vivo models for the intestinal permeability. The probiotic effects of ZY-312 on intestinal epithelial cells were first examined, and the results revealed that ZY-312 inhibited C. sakazakii invasion, C. sakazakii-induced dual cell death (pyroptosis and apoptosis), and epithelial barrier dysfunction in vitro and in vivo. The presence of ZY-312 also resulted in decreased expression of an inflammasome (NOD-like receptor family member pyrin domain-containing protein 3 [NLRP3]), caspase-3, and serine protease caspase-1 in a neonatal rat model. Furthermore, ZY-312 significantly modulated the compositions of the intestinal bacterial communities and decreased the relative abundances of Proteobacteria and Gammaproteobacteria but increased the relative abundances of Bacteroides and Bacillus in neonatal rats. In conclusion, our findings have shown for the first time that the probiotic B. fragilis ZY-312 suppresses C. sakazakii-induced NEC by modulating the proinflammatory response and dual cell death (apoptosis and pyroptosis). IMPORTANCE Cronobacter sakazakii is an opportunistic pathogenic bacterium that can cause necrotizing enterocolitis (NEC). However, the mechanism of pathogenicity of C. sakazakii is largely unknown. Here we have now demonstrated that apoptotic and pyroptotic stimuli are effectors of C. sakazakii-induced NEC. Previously, we isolated a novel probiotic strain candidate from fecal samples from healthy infants and characterized it as Bacteroides fragilis strain ZY-312. Functional characterization reveals that ZY-312 inhibited C. sakazakii invasion, restoring epithelial barrier dysfunction, decreasing the expression of inflammatory cytokines, and reducing dual cell death (pyroptosis and apoptosis). Furthermore, the presence of ZY-132 was sufficient to hinder the adverse reaction seen with C. sakazakii in a C. sakazakii-induced NEC model. Taking the results together, our study demonstrated the utility of ZY-312 as a promising probiotic agent for the prevention of NEC.Hongying FanZhenhui ChenRuqin LinYangyang LiuXianbo WuSanthosh PuthiyakunnonYe WangBo ZhuQiwei ZhangYang BaiFachao ZhiAmerican Society for MicrobiologyarticleapoptosisBacteroides fragilisCronobacter sakazakiiinflammasomesnecrotizing enterocolitispyroptosisMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	apoptosis Bacteroides fragilis Cronobacter sakazakii inflammasomes necrotizing enterocolitis pyroptosis Microbiology QR1-502
spellingShingle	apoptosis Bacteroides fragilis Cronobacter sakazakii inflammasomes necrotizing enterocolitis pyroptosis Microbiology QR1-502 Hongying Fan Zhenhui Chen Ruqin Lin Yangyang Liu Xianbo Wu Santhosh Puthiyakunnon Ye Wang Bo Zhu Qiwei Zhang Yang Bai Fachao Zhi <named-content content-type="genus-species">Bacteroides fragilis</named-content> Strain ZY-312 Defense against <named-content content-type="genus-species">Cronobacter sakazakii</named-content>-Induced Necrotizing Enterocolitis <italic toggle="yes">In Vitro</italic> and in a Neonatal Rat Model
description	ABSTRACT Cronobacter sakazakii is an important pathogen associated with the development of necrotizing enterocolitis (NEC), infant sepsis, and meningitis. Several randomized prospective clinical trials demonstrated that oral probiotics could decrease the incidence of NEC. Previously, we isolated and characterized a novel probiotic, Bacteroides fragilis strain ZY-312. However, it remains unclear how ZY-312 protects the host from the effects of C. sakazakii infection. To understand the underlying mechanisms triggering the probiotic effects, we tested the hypothesis that there was cross talk between probiotics/probiotics-modulated microbiota and the local immune system, governed by the permeability of the intestinal mucosa, using in vitro and in vivo models for the intestinal permeability. The probiotic effects of ZY-312 on intestinal epithelial cells were first examined, and the results revealed that ZY-312 inhibited C. sakazakii invasion, C. sakazakii-induced dual cell death (pyroptosis and apoptosis), and epithelial barrier dysfunction in vitro and in vivo. The presence of ZY-312 also resulted in decreased expression of an inflammasome (NOD-like receptor family member pyrin domain-containing protein 3 [NLRP3]), caspase-3, and serine protease caspase-1 in a neonatal rat model. Furthermore, ZY-312 significantly modulated the compositions of the intestinal bacterial communities and decreased the relative abundances of Proteobacteria and Gammaproteobacteria but increased the relative abundances of Bacteroides and Bacillus in neonatal rats. In conclusion, our findings have shown for the first time that the probiotic B. fragilis ZY-312 suppresses C. sakazakii-induced NEC by modulating the proinflammatory response and dual cell death (apoptosis and pyroptosis). IMPORTANCE Cronobacter sakazakii is an opportunistic pathogenic bacterium that can cause necrotizing enterocolitis (NEC). However, the mechanism of pathogenicity of C. sakazakii is largely unknown. Here we have now demonstrated that apoptotic and pyroptotic stimuli are effectors of C. sakazakii-induced NEC. Previously, we isolated a novel probiotic strain candidate from fecal samples from healthy infants and characterized it as Bacteroides fragilis strain ZY-312. Functional characterization reveals that ZY-312 inhibited C. sakazakii invasion, restoring epithelial barrier dysfunction, decreasing the expression of inflammatory cytokines, and reducing dual cell death (pyroptosis and apoptosis). Furthermore, the presence of ZY-132 was sufficient to hinder the adverse reaction seen with C. sakazakii in a C. sakazakii-induced NEC model. Taking the results together, our study demonstrated the utility of ZY-312 as a promising probiotic agent for the prevention of NEC.
format	article
author	Hongying Fan Zhenhui Chen Ruqin Lin Yangyang Liu Xianbo Wu Santhosh Puthiyakunnon Ye Wang Bo Zhu Qiwei Zhang Yang Bai Fachao Zhi
author_facet	Hongying Fan Zhenhui Chen Ruqin Lin Yangyang Liu Xianbo Wu Santhosh Puthiyakunnon Ye Wang Bo Zhu Qiwei Zhang Yang Bai Fachao Zhi
author_sort	Hongying Fan
title	<named-content content-type="genus-species">Bacteroides fragilis</named-content> Strain ZY-312 Defense against <named-content content-type="genus-species">Cronobacter sakazakii</named-content>-Induced Necrotizing Enterocolitis <italic toggle="yes">In Vitro</italic> and in a Neonatal Rat Model
title_short	<named-content content-type="genus-species">Bacteroides fragilis</named-content> Strain ZY-312 Defense against <named-content content-type="genus-species">Cronobacter sakazakii</named-content>-Induced Necrotizing Enterocolitis <italic toggle="yes">In Vitro</italic> and in a Neonatal Rat Model
title_full	<named-content content-type="genus-species">Bacteroides fragilis</named-content> Strain ZY-312 Defense against <named-content content-type="genus-species">Cronobacter sakazakii</named-content>-Induced Necrotizing Enterocolitis <italic toggle="yes">In Vitro</italic> and in a Neonatal Rat Model
title_fullStr	<named-content content-type="genus-species">Bacteroides fragilis</named-content> Strain ZY-312 Defense against <named-content content-type="genus-species">Cronobacter sakazakii</named-content>-Induced Necrotizing Enterocolitis <italic toggle="yes">In Vitro</italic> and in a Neonatal Rat Model
title_full_unstemmed	<named-content content-type="genus-species">Bacteroides fragilis</named-content> Strain ZY-312 Defense against <named-content content-type="genus-species">Cronobacter sakazakii</named-content>-Induced Necrotizing Enterocolitis <italic toggle="yes">In Vitro</italic> and in a Neonatal Rat Model
title_sort	<named-content content-type="genus-species">bacteroides fragilis</named-content> strain zy-312 defense against <named-content content-type="genus-species">cronobacter sakazakii</named-content>-induced necrotizing enterocolitis <italic toggle="yes">in vitro</italic> and in a neonatal rat model
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/2746e2807e214482ac141d2a8b47b1a1
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<named-content content-type="genus-species">Bacteroides fragilis</named-content> Strain ZY-312 Defense against <named-content content-type="genus-species">Cronobacter sakazakii</named-content>-Induced Necrotizing Enterocolitis <italic toggle="yes">In Vitro</italic> and in a Neonatal Rat Model

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