Pediococcus pentosaceus Enhances Host Resistance Against Pathogen by Increasing IL-1β Production: Understanding Probiotic Effectiveness and Administration Duration

Probiotic administration is a potential strategy against enteric pathogen infection in either clinical treatment or animal nutrition industry, but the administration duration of probiotics varied and the underlying mechanisms remain unclear. A strain (YC) affiliated to Pediococcus pentosaceus, a com...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Chengjie Shan, Miao Li, Zhu Liu, Rong Xu, Fang Qiao, Zhen-Yu Du, Mei-Ling Zhang
Formato: article
Lenguaje:EN
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://doaj.org/article/7b066457684a4aab91788b76a2d7ac84
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:7b066457684a4aab91788b76a2d7ac84
record_format dspace
spelling oai:doaj.org-article:7b066457684a4aab91788b76a2d7ac842021-12-01T07:44:16ZPediococcus pentosaceus Enhances Host Resistance Against Pathogen by Increasing IL-1β Production: Understanding Probiotic Effectiveness and Administration Duration1664-322410.3389/fimmu.2021.766401https://doaj.org/article/7b066457684a4aab91788b76a2d7ac842021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fimmu.2021.766401/fullhttps://doaj.org/toc/1664-3224Probiotic administration is a potential strategy against enteric pathogen infection in either clinical treatment or animal nutrition industry, but the administration duration of probiotics varied and the underlying mechanisms remain unclear. A strain (YC) affiliated to Pediococcus pentosaceus, a commonly used probiotic, was isolated from fish gut and the potential role of YC against Aeromonas hydrophila was detected in zebrafish. We found that 3- or 4-week YC administration (YC3W or YC4W) increased the resistance against A. hydrophila while 1- or 2-week treatment (YC1W or YC2W) did not. To determine the possible reason, intestinal microbiota analysis and RNAseq were conducted. The results showed that compared with CON and YC1W, YC4W significantly increased the abundance of short-chain fatty acids (SCFAs) producing bacteria and elevated the gene expression of nlrp3. Higher butyrate content and enhanced expression of IL1β were subsequently found in YC4W. To identify the causal relationship between butyrate and the higher pathogen resistance, different concentrations of sodium butyrate (SB) were supplemented. The results suggested that 10 mmol/kg SB addition mirrored the protective effect of YC4W by increasing the production of IL-1β. Furthermore, the increased IL-1β raised the percentage of intestinal neutrophils, which endued the zebrafish with A. hydrophila resistance. In vivo knockdown of intestinal il1b eliminated the anti-infection effect. Collectively, our data suggested that the molecular mechanism of probiotics determined the administration duration, which is vital for the efficiency of probiotics. Promoting host inflammation by probiotic pretreatment is one potential way for probiotics to provide their protective effects against pathogens.Chengjie ShanMiao LiZhu LiuZhu LiuRong XuFang QiaoZhen-Yu DuMei-Ling ZhangFrontiers Media S.A.articleprobioticpathogen resistanceadministration durationbutyrateNLRP3 inflammasomeImmunologic diseases. AllergyRC581-607ENFrontiers in Immunology, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic probiotic
pathogen resistance
administration duration
butyrate
NLRP3 inflammasome
Immunologic diseases. Allergy
RC581-607
spellingShingle probiotic
pathogen resistance
administration duration
butyrate
NLRP3 inflammasome
Immunologic diseases. Allergy
RC581-607
Chengjie Shan
Miao Li
Zhu Liu
Zhu Liu
Rong Xu
Fang Qiao
Zhen-Yu Du
Mei-Ling Zhang
Pediococcus pentosaceus Enhances Host Resistance Against Pathogen by Increasing IL-1β Production: Understanding Probiotic Effectiveness and Administration Duration
description Probiotic administration is a potential strategy against enteric pathogen infection in either clinical treatment or animal nutrition industry, but the administration duration of probiotics varied and the underlying mechanisms remain unclear. A strain (YC) affiliated to Pediococcus pentosaceus, a commonly used probiotic, was isolated from fish gut and the potential role of YC against Aeromonas hydrophila was detected in zebrafish. We found that 3- or 4-week YC administration (YC3W or YC4W) increased the resistance against A. hydrophila while 1- or 2-week treatment (YC1W or YC2W) did not. To determine the possible reason, intestinal microbiota analysis and RNAseq were conducted. The results showed that compared with CON and YC1W, YC4W significantly increased the abundance of short-chain fatty acids (SCFAs) producing bacteria and elevated the gene expression of nlrp3. Higher butyrate content and enhanced expression of IL1β were subsequently found in YC4W. To identify the causal relationship between butyrate and the higher pathogen resistance, different concentrations of sodium butyrate (SB) were supplemented. The results suggested that 10 mmol/kg SB addition mirrored the protective effect of YC4W by increasing the production of IL-1β. Furthermore, the increased IL-1β raised the percentage of intestinal neutrophils, which endued the zebrafish with A. hydrophila resistance. In vivo knockdown of intestinal il1b eliminated the anti-infection effect. Collectively, our data suggested that the molecular mechanism of probiotics determined the administration duration, which is vital for the efficiency of probiotics. Promoting host inflammation by probiotic pretreatment is one potential way for probiotics to provide their protective effects against pathogens.
format article
author Chengjie Shan
Miao Li
Zhu Liu
Zhu Liu
Rong Xu
Fang Qiao
Zhen-Yu Du
Mei-Ling Zhang
author_facet Chengjie Shan
Miao Li
Zhu Liu
Zhu Liu
Rong Xu
Fang Qiao
Zhen-Yu Du
Mei-Ling Zhang
author_sort Chengjie Shan
title Pediococcus pentosaceus Enhances Host Resistance Against Pathogen by Increasing IL-1β Production: Understanding Probiotic Effectiveness and Administration Duration
title_short Pediococcus pentosaceus Enhances Host Resistance Against Pathogen by Increasing IL-1β Production: Understanding Probiotic Effectiveness and Administration Duration
title_full Pediococcus pentosaceus Enhances Host Resistance Against Pathogen by Increasing IL-1β Production: Understanding Probiotic Effectiveness and Administration Duration
title_fullStr Pediococcus pentosaceus Enhances Host Resistance Against Pathogen by Increasing IL-1β Production: Understanding Probiotic Effectiveness and Administration Duration
title_full_unstemmed Pediococcus pentosaceus Enhances Host Resistance Against Pathogen by Increasing IL-1β Production: Understanding Probiotic Effectiveness and Administration Duration
title_sort pediococcus pentosaceus enhances host resistance against pathogen by increasing il-1β production: understanding probiotic effectiveness and administration duration
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/7b066457684a4aab91788b76a2d7ac84
work_keys_str_mv AT chengjieshan pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT miaoli pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT zhuliu pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT zhuliu pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT rongxu pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT fangqiao pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT zhenyudu pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT meilingzhang pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
_version_ 1718405421044072448