Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression.

BACKGROUND: We previously showed that evaluation of anti-inflammatory activities of lactic acid bacteria in porcine intestinal epithelial (PIE) cells is useful for selecting potentially immunobiotic strains. OBJECTIVE: The aims of the present study were: i) to select potentially immunomodulatory bif...

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Main Authors: Yohsuke Tomosada, Julio Villena, Kozue Murata, Eriko Chiba, Tomoyuki Shimazu, Hisashi Aso, Noriyuki Iwabuchi, Jin-zhong Xiao, Tadao Saito, Haruki Kitazawa
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3608626?pdf=render
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author Yohsuke Tomosada
Julio Villena
Kozue Murata
Eriko Chiba
Tomoyuki Shimazu
Hisashi Aso
Noriyuki Iwabuchi
Jin-zhong Xiao
Tadao Saito
Haruki Kitazawa
author_facet Yohsuke Tomosada
Julio Villena
Kozue Murata
Eriko Chiba
Tomoyuki Shimazu
Hisashi Aso
Noriyuki Iwabuchi
Jin-zhong Xiao
Tadao Saito
Haruki Kitazawa
author_sort Yohsuke Tomosada
collection DOAJ
description BACKGROUND: We previously showed that evaluation of anti-inflammatory activities of lactic acid bacteria in porcine intestinal epithelial (PIE) cells is useful for selecting potentially immunobiotic strains. OBJECTIVE: The aims of the present study were: i) to select potentially immunomodulatory bifidobacteria that beneficially modulate the Toll-like receptor (TLR)-4-triggered inflammatory response in PIE cells and; ii) to gain insight into the molecular mechanisms involved in the anti-inflammatory effect of immunobiotics by evaluating the role of TLR2 and TLR negative regulators in the modulation of proinflammatory cytokine production and activation of mitogen-activated protein kinase (MAPK) and nuclear factor-κB (NF-κB) pathways in PIE cells. RESULTS: Bifidobacteria longum BB536 and B. breve M-16V strains significantly downregulated levels of interleukin (IL)-8, monocyte chemotactic protein (MCP)-1 and IL-6 in PIE cells challenged with heat-killed enterotoxigenic Escherichia coli. Moreover, BB536 and M-16V strains attenuated the proinflammatory response by modulating the NF-κB and MAPK pathways. In addition, our findings provide evidence for a key role for the ubiquitin-editing enzyme A20 in the anti-inflammatory effect of immunobiotic bifidobacteria in PIE cells. CONCLUSIONS: We show new data regarding the mechanism involved in the anti-inflammatory effect of immunobiotics. Several strains with immunoregulatory capabilities used a common mechanism to induce tolerance in PIE cells. Immunoregulatory strains interacted with TLR2, upregulated the expression of A20 in PIE cells, and beneficially modulated the subsequent TLR4 activation by reducing the activation of MAPK and NF-κB pathways and the production of proinflammatory cytokines. We also show that the combination of TLR2 activation and A20 induction can be used as biomarkers to screen and select potential immunoregulatory bifidobacteria strains.
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spelling doaj.art-dc6bcc2c20fd42a0adead1a40acbc7e82022-12-22T01:29:42ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0183e5925910.1371/journal.pone.0059259Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression.Yohsuke TomosadaJulio VillenaKozue MurataEriko ChibaTomoyuki ShimazuHisashi AsoNoriyuki IwabuchiJin-zhong XiaoTadao SaitoHaruki KitazawaBACKGROUND: We previously showed that evaluation of anti-inflammatory activities of lactic acid bacteria in porcine intestinal epithelial (PIE) cells is useful for selecting potentially immunobiotic strains. OBJECTIVE: The aims of the present study were: i) to select potentially immunomodulatory bifidobacteria that beneficially modulate the Toll-like receptor (TLR)-4-triggered inflammatory response in PIE cells and; ii) to gain insight into the molecular mechanisms involved in the anti-inflammatory effect of immunobiotics by evaluating the role of TLR2 and TLR negative regulators in the modulation of proinflammatory cytokine production and activation of mitogen-activated protein kinase (MAPK) and nuclear factor-κB (NF-κB) pathways in PIE cells. RESULTS: Bifidobacteria longum BB536 and B. breve M-16V strains significantly downregulated levels of interleukin (IL)-8, monocyte chemotactic protein (MCP)-1 and IL-6 in PIE cells challenged with heat-killed enterotoxigenic Escherichia coli. Moreover, BB536 and M-16V strains attenuated the proinflammatory response by modulating the NF-κB and MAPK pathways. In addition, our findings provide evidence for a key role for the ubiquitin-editing enzyme A20 in the anti-inflammatory effect of immunobiotic bifidobacteria in PIE cells. CONCLUSIONS: We show new data regarding the mechanism involved in the anti-inflammatory effect of immunobiotics. Several strains with immunoregulatory capabilities used a common mechanism to induce tolerance in PIE cells. Immunoregulatory strains interacted with TLR2, upregulated the expression of A20 in PIE cells, and beneficially modulated the subsequent TLR4 activation by reducing the activation of MAPK and NF-κB pathways and the production of proinflammatory cytokines. We also show that the combination of TLR2 activation and A20 induction can be used as biomarkers to screen and select potential immunoregulatory bifidobacteria strains.http://europepmc.org/articles/PMC3608626?pdf=render
spellingShingle Yohsuke Tomosada
Julio Villena
Kozue Murata
Eriko Chiba
Tomoyuki Shimazu
Hisashi Aso
Noriyuki Iwabuchi
Jin-zhong Xiao
Tadao Saito
Haruki Kitazawa
Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression.
PLoS ONE
title Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression.
title_full Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression.
title_fullStr Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression.
title_full_unstemmed Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression.
title_short Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression.
title_sort immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin editing enzyme a20 expression
url http://europepmc.org/articles/PMC3608626?pdf=render
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