Mechanism of protection of transepithelial barrier function by Lactobacillus salivarius: strain dependence and attenuation by bacteriocin production

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TY  - JOUR
  - Miyauchi, E,O'Callaghan, J,Butto, LF,Hurley, G,Melgar, S,Tanabe, S,Shanahan, F,Nally, K,O'Toole, PW
  - 2012
  - January
  - American Journal of Physiology - Gastrointestinal and Liver Physiology
  - Mechanism of protection of transepithelial barrier function by Lactobacillus salivarius: strain dependence and attenuation by bacteriocin production
  - Validated
  - ()
  - lactobacilli barrier integrity ERK transepithelial resistance tight junction INFLAMMATORY-BOWEL-DISEASE EPITHELIAL TIGHT JUNCTION HYDROGEN-PEROXIDE OXIDATIVE STRESS TNF-ALPHA INTESTINAL BARRIER CLAUDIN-2 EXPRESSION HELICOBACTER-PYLORI ULCERATIVE-COLITIS PROTEIN EXPRESSION
  - 303
  - 1029
  - 1041
  - Enhanced barrier function is one mechanism whereby commensals and probiotic bacteria limit translocation of foreign antigens or pathogens in the gut. However, barrier protection is not exhibited by all probiotic or commensals and the strain-specific molecules involved remain to be clarified. We evaluated the effects of 33 individual Lactobacillus salivarius strains on the hydrogen peroxide (H2O2)induced barrier impairment in human epithelial Caco-2 cells. These strains showed markedly different effects on H2O2-induced reduction in transepithelial resistance (TER). The effective strains such as UCC118 and CCUG38008 attenuated H2O2-induced disassembly and relocalization of tight junction proteins, but the ineffective strain AH43324 did not. Strains UCC118 and CCUG38008 induced phosphorylation of extracellular signal-regulated kinase (ERK) in Caco-2 cells, and the ERK inhibitor U0126 attenuated the barrier-protecting effect of these strains. In contrast, the AH43324 strain induced phosphorylation of Akt and p38, which was associated with an absence of a protective effect. Global transcriptome analysis of UCC118 and AH43324 revealed that some genes in a bacteriocin gene cluster were upregulated in AH43324 under TER assay conditions. A bacteriocin-negative UCC118 mutant displayed significantly greater suppressive effect on H2O2-induced reduction in TER compared with wild-type UCC118. The wild-type strain augmented H2O2-induced phosphorylation of Akt and p38, whereas a bacteriocin-negative UCC118 mutant did not. These observations indicate that L. salivarius strains are widely divergent in their capacity for barrier protection, and this is underpinned by differences in the activation of intracellular signaling pathways. Furthermore, bacteriocin production appears to have an attenuating influence on lactobacillus-mediated barrier protection.
  - DOI 10.1152/ajpgi.00003.2012
DA  - 2012/01
ER  - 
@article{V190495672,
   = {Miyauchi,  E and O'Callaghan,  J and Butto,  LF and Hurley,  G and Melgar,  S and Tanabe,  S and Shanahan,  F and Nally,  K and O'Toole,  PW },
   = {2012},
   = {January},
   = {American Journal of Physiology - Gastrointestinal and Liver Physiology},
   = {Mechanism of protection of transepithelial barrier function by Lactobacillus salivarius: strain dependence and attenuation by bacteriocin production},
   = {Validated},
   = {()},
   = {lactobacilli barrier integrity ERK transepithelial resistance tight junction INFLAMMATORY-BOWEL-DISEASE EPITHELIAL TIGHT JUNCTION HYDROGEN-PEROXIDE OXIDATIVE STRESS TNF-ALPHA INTESTINAL BARRIER CLAUDIN-2 EXPRESSION HELICOBACTER-PYLORI ULCERATIVE-COLITIS PROTEIN EXPRESSION},
   = {303},
  pages = {1029--1041},
   = {{Enhanced barrier function is one mechanism whereby commensals and probiotic bacteria limit translocation of foreign antigens or pathogens in the gut. However, barrier protection is not exhibited by all probiotic or commensals and the strain-specific molecules involved remain to be clarified. We evaluated the effects of 33 individual Lactobacillus salivarius strains on the hydrogen peroxide (H2O2)induced barrier impairment in human epithelial Caco-2 cells. These strains showed markedly different effects on H2O2-induced reduction in transepithelial resistance (TER). The effective strains such as UCC118 and CCUG38008 attenuated H2O2-induced disassembly and relocalization of tight junction proteins, but the ineffective strain AH43324 did not. Strains UCC118 and CCUG38008 induced phosphorylation of extracellular signal-regulated kinase (ERK) in Caco-2 cells, and the ERK inhibitor U0126 attenuated the barrier-protecting effect of these strains. In contrast, the AH43324 strain induced phosphorylation of Akt and p38, which was associated with an absence of a protective effect. Global transcriptome analysis of UCC118 and AH43324 revealed that some genes in a bacteriocin gene cluster were upregulated in AH43324 under TER assay conditions. A bacteriocin-negative UCC118 mutant displayed significantly greater suppressive effect on H2O2-induced reduction in TER compared with wild-type UCC118. The wild-type strain augmented H2O2-induced phosphorylation of Akt and p38, whereas a bacteriocin-negative UCC118 mutant did not. These observations indicate that L. salivarius strains are widely divergent in their capacity for barrier protection, and this is underpinned by differences in the activation of intracellular signaling pathways. Furthermore, bacteriocin production appears to have an attenuating influence on lactobacillus-mediated barrier protection.}},
   = {DOI 10.1152/ajpgi.00003.2012},
  source = {IRIS}
}
AUTHORSMiyauchi, E,O'Callaghan, J,Butto, LF,Hurley, G,Melgar, S,Tanabe, S,Shanahan, F,Nally, K,O'Toole, PW
YEAR2012
MONTHJanuary
JOURNAL_CODEAmerican Journal of Physiology - Gastrointestinal and Liver Physiology
TITLEMechanism of protection of transepithelial barrier function by Lactobacillus salivarius: strain dependence and attenuation by bacteriocin production
STATUSValidated
TIMES_CITED()
SEARCH_KEYWORDlactobacilli barrier integrity ERK transepithelial resistance tight junction INFLAMMATORY-BOWEL-DISEASE EPITHELIAL TIGHT JUNCTION HYDROGEN-PEROXIDE OXIDATIVE STRESS TNF-ALPHA INTESTINAL BARRIER CLAUDIN-2 EXPRESSION HELICOBACTER-PYLORI ULCERATIVE-COLITIS PROTEIN EXPRESSION
VOLUME303
ISSUE
START_PAGE1029
END_PAGE1041
ABSTRACTEnhanced barrier function is one mechanism whereby commensals and probiotic bacteria limit translocation of foreign antigens or pathogens in the gut. However, barrier protection is not exhibited by all probiotic or commensals and the strain-specific molecules involved remain to be clarified. We evaluated the effects of 33 individual Lactobacillus salivarius strains on the hydrogen peroxide (H2O2)induced barrier impairment in human epithelial Caco-2 cells. These strains showed markedly different effects on H2O2-induced reduction in transepithelial resistance (TER). The effective strains such as UCC118 and CCUG38008 attenuated H2O2-induced disassembly and relocalization of tight junction proteins, but the ineffective strain AH43324 did not. Strains UCC118 and CCUG38008 induced phosphorylation of extracellular signal-regulated kinase (ERK) in Caco-2 cells, and the ERK inhibitor U0126 attenuated the barrier-protecting effect of these strains. In contrast, the AH43324 strain induced phosphorylation of Akt and p38, which was associated with an absence of a protective effect. Global transcriptome analysis of UCC118 and AH43324 revealed that some genes in a bacteriocin gene cluster were upregulated in AH43324 under TER assay conditions. A bacteriocin-negative UCC118 mutant displayed significantly greater suppressive effect on H2O2-induced reduction in TER compared with wild-type UCC118. The wild-type strain augmented H2O2-induced phosphorylation of Akt and p38, whereas a bacteriocin-negative UCC118 mutant did not. These observations indicate that L. salivarius strains are widely divergent in their capacity for barrier protection, and this is underpinned by differences in the activation of intracellular signaling pathways. Furthermore, bacteriocin production appears to have an attenuating influence on lactobacillus-mediated barrier protection.
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DOI_LINKDOI 10.1152/ajpgi.00003.2012
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