Cargando…

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

Detalles Bibliográficos
Autores principales: Shan, Chengjie, Li, Miao, Liu, Zhu, Xu, Rong, Qiao, Fang, Du, Zhen-Yu, Zhang, Mei-Ling
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8662542/
https://www.ncbi.nlm.nih.gov/pubmed/34899717
http://dx.doi.org/10.3389/fimmu.2021.766401
_version_ 1784613459456950272
author Shan, Chengjie
Li, Miao
Liu, Zhu
Xu, Rong
Qiao, Fang
Du, Zhen-Yu
Zhang, Mei-Ling
author_facet Shan, Chengjie
Li, Miao
Liu, Zhu
Xu, Rong
Qiao, Fang
Du, Zhen-Yu
Zhang, Mei-Ling
author_sort Shan, Chengjie
collection PubMed
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 Online
Article
Text
id pubmed-8662542
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-86625422021-12-11 Pediococcus pentosaceus Enhances Host Resistance Against Pathogen by Increasing IL-1β Production: Understanding Probiotic Effectiveness and Administration Duration Shan, Chengjie Li, Miao Liu, Zhu Xu, Rong Qiao, Fang Du, Zhen-Yu Zhang, Mei-Ling Front Immunol Immunology 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. Frontiers Media S.A. 2021-11-26 /pmc/articles/PMC8662542/ /pubmed/34899717 http://dx.doi.org/10.3389/fimmu.2021.766401 Text en Copyright © 2021 Shan, Li, Liu, Xu, Qiao, Du and Zhang https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Shan, Chengjie
Li, Miao
Liu, Zhu
Xu, Rong
Qiao, Fang
Du, Zhen-Yu
Zhang, Mei-Ling
Pediococcus pentosaceus Enhances Host Resistance Against Pathogen by Increasing IL-1β Production: Understanding Probiotic Effectiveness and Administration Duration
title 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_short 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
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8662542/
https://www.ncbi.nlm.nih.gov/pubmed/34899717
http://dx.doi.org/10.3389/fimmu.2021.766401
work_keys_str_mv AT shanchengjie pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT limiao pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT liuzhu pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT xurong pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT qiaofang pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT duzhenyu pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration
AT zhangmeiling pediococcuspentosaceusenhanceshostresistanceagainstpathogenbyincreasingil1bproductionunderstandingprobioticeffectivenessandadministrationduration