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Escherichia coli Nissle 1917 enhances bioavailability of serotonin in gut tissues through modulation of synthesis and clearance.

Nzakizwanayo J, Dedi C, Standen G, Macfarlane WM, Patel BA, Jones BV - Sci Rep (2015)

Bottom Line: Exposure of tissue to EcN cells, but not MG1655 cells, was found to increase levels of extra-cellular 5-HT.These effects were not observed when tissues were treated with cell-free supernatant from bacterial cultures.Measurement of 5-HT precursors and metabolites indicated EcN also increases intracellular 5-HTP and reduces 5-HIAA.

View Article: PubMed Central - PubMed

Affiliation: School of Pharmacy and Biomolecular Sciences, University of Brighton, Brighton, BN2 4GJ, United Kingdom.

ABSTRACT
Accumulating evidence shows indigenous gut microbes can interact with the human host through modulation of serotonin (5-HT) signaling. Here we investigate the impact of the probiotic Escherichia coli Nissle 1917 (EcN) on 5-HT signalling in gut tissues. Ex-vivo mouse ileal tissue sections were treated with either EcN or the human gut commensal MG1655, and effects on levels of 5-HT, precursors, and metabolites, were evaluated using amperometry and high performance liquid chromatography with electrochemical detection (HPLC-EC). Exposure of tissue to EcN cells, but not MG1655 cells, was found to increase levels of extra-cellular 5-HT. These effects were not observed when tissues were treated with cell-free supernatant from bacterial cultures. In contrast, when supernatant recovered from untreated ileal tissue was pre-incubated with EcN, the derivative cell-free supernatant was able to elevate 5-HT overflow when used to treat fresh ileal tissue. Measurement of 5-HT precursors and metabolites indicated EcN also increases intracellular 5-HTP and reduces 5-HIAA. The former pointed to modulation of tryptophan hydroxylase-1 to enhance 5-HT synthesis, while the latter indicates an impact on clearance into enterocytes through SERT. Taken together, these findings show EcN is able to enhance 5-HT bioavailability in ileal tissues through interaction with compounds secreted from host tissues.

No MeSH data available.


Related in: MedlinePlus

Role of short chain fatty acid production in EcN mediate 5-HT overflow.To determine if the capacity for production of short chain fatty acids (SCFA) was enhanced in EcN compared to MG1655, and relevant to EcN mediated 5-HT overflow, the levels of SCFA generated by each strain during growth in mucosal co-culture was measured. Bacterial cell suspensions in krebs buffer with ileal mucosal scrapings were incubated at 37 °C with 5% CO2 for 1 h, before measurement of SCFA by HPLC. Propionate and butyrate were not detected in this assay but both EcN and MG1655 generate acetate as show in charts. Data show means ± S.E.M. (n = 3). **P ≤ 0.01 ***P ≤ 0.001 Vs KB. KB - Krebs buffer only; EcN – E. coli Nissle 1917; MG1655 – E. coli MG1655
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f3: Role of short chain fatty acid production in EcN mediate 5-HT overflow.To determine if the capacity for production of short chain fatty acids (SCFA) was enhanced in EcN compared to MG1655, and relevant to EcN mediated 5-HT overflow, the levels of SCFA generated by each strain during growth in mucosal co-culture was measured. Bacterial cell suspensions in krebs buffer with ileal mucosal scrapings were incubated at 37 °C with 5% CO2 for 1 h, before measurement of SCFA by HPLC. Propionate and butyrate were not detected in this assay but both EcN and MG1655 generate acetate as show in charts. Data show means ± S.E.M. (n = 3). **P ≤ 0.01 ***P ≤ 0.001 Vs KB. KB - Krebs buffer only; EcN – E. coli Nissle 1917; MG1655 – E. coli MG1655

Mentions: Because the production of short chain fatty acids (SCFA) such as acetate, butyrate and propionate have been shown to stimulate 5-HT release in vivo47, and acetate is a key end product of E. coli growth in glucose containing media such as Krebs buffer, we next assessed the potential for the observed effects to be the result of enhanced SCFA production in EcN compared to MG1655. As expected, neither strain was able to generate detectable levels of butyrate or propionate, but both produced acetate under co-culture conditions with intestinal tissues (Fig. 3). However, under these conditions no significant differences in acetate production were observed between EcN and MG1655, indicating the elevated 5-HT release instigated by EcN was not attributable to acetate production.


Escherichia coli Nissle 1917 enhances bioavailability of serotonin in gut tissues through modulation of synthesis and clearance.

Nzakizwanayo J, Dedi C, Standen G, Macfarlane WM, Patel BA, Jones BV - Sci Rep (2015)

Role of short chain fatty acid production in EcN mediate 5-HT overflow.To determine if the capacity for production of short chain fatty acids (SCFA) was enhanced in EcN compared to MG1655, and relevant to EcN mediated 5-HT overflow, the levels of SCFA generated by each strain during growth in mucosal co-culture was measured. Bacterial cell suspensions in krebs buffer with ileal mucosal scrapings were incubated at 37 °C with 5% CO2 for 1 h, before measurement of SCFA by HPLC. Propionate and butyrate were not detected in this assay but both EcN and MG1655 generate acetate as show in charts. Data show means ± S.E.M. (n = 3). **P ≤ 0.01 ***P ≤ 0.001 Vs KB. KB - Krebs buffer only; EcN – E. coli Nissle 1917; MG1655 – E. coli MG1655
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4663480&req=5

f3: Role of short chain fatty acid production in EcN mediate 5-HT overflow.To determine if the capacity for production of short chain fatty acids (SCFA) was enhanced in EcN compared to MG1655, and relevant to EcN mediated 5-HT overflow, the levels of SCFA generated by each strain during growth in mucosal co-culture was measured. Bacterial cell suspensions in krebs buffer with ileal mucosal scrapings were incubated at 37 °C with 5% CO2 for 1 h, before measurement of SCFA by HPLC. Propionate and butyrate were not detected in this assay but both EcN and MG1655 generate acetate as show in charts. Data show means ± S.E.M. (n = 3). **P ≤ 0.01 ***P ≤ 0.001 Vs KB. KB - Krebs buffer only; EcN – E. coli Nissle 1917; MG1655 – E. coli MG1655
Mentions: Because the production of short chain fatty acids (SCFA) such as acetate, butyrate and propionate have been shown to stimulate 5-HT release in vivo47, and acetate is a key end product of E. coli growth in glucose containing media such as Krebs buffer, we next assessed the potential for the observed effects to be the result of enhanced SCFA production in EcN compared to MG1655. As expected, neither strain was able to generate detectable levels of butyrate or propionate, but both produced acetate under co-culture conditions with intestinal tissues (Fig. 3). However, under these conditions no significant differences in acetate production were observed between EcN and MG1655, indicating the elevated 5-HT release instigated by EcN was not attributable to acetate production.

Bottom Line: Exposure of tissue to EcN cells, but not MG1655 cells, was found to increase levels of extra-cellular 5-HT.These effects were not observed when tissues were treated with cell-free supernatant from bacterial cultures.Measurement of 5-HT precursors and metabolites indicated EcN also increases intracellular 5-HTP and reduces 5-HIAA.

View Article: PubMed Central - PubMed

Affiliation: School of Pharmacy and Biomolecular Sciences, University of Brighton, Brighton, BN2 4GJ, United Kingdom.

ABSTRACT
Accumulating evidence shows indigenous gut microbes can interact with the human host through modulation of serotonin (5-HT) signaling. Here we investigate the impact of the probiotic Escherichia coli Nissle 1917 (EcN) on 5-HT signalling in gut tissues. Ex-vivo mouse ileal tissue sections were treated with either EcN or the human gut commensal MG1655, and effects on levels of 5-HT, precursors, and metabolites, were evaluated using amperometry and high performance liquid chromatography with electrochemical detection (HPLC-EC). Exposure of tissue to EcN cells, but not MG1655 cells, was found to increase levels of extra-cellular 5-HT. These effects were not observed when tissues were treated with cell-free supernatant from bacterial cultures. In contrast, when supernatant recovered from untreated ileal tissue was pre-incubated with EcN, the derivative cell-free supernatant was able to elevate 5-HT overflow when used to treat fresh ileal tissue. Measurement of 5-HT precursors and metabolites indicated EcN also increases intracellular 5-HTP and reduces 5-HIAA. The former pointed to modulation of tryptophan hydroxylase-1 to enhance 5-HT synthesis, while the latter indicates an impact on clearance into enterocytes through SERT. Taken together, these findings show EcN is able to enhance 5-HT bioavailability in ileal tissues through interaction with compounds secreted from host tissues.

No MeSH data available.


Related in: MedlinePlus