Consumption of indigestible saccharides and administration of Bifidobacterium pseudolongum reduce mucosal serotonin in murine colonic mucosa
SCFA increase serotonin (5-hydroxytryptamine, 5-HT) synthesis and content in the colon in vitro and ex vivo, but little is known in vivo. We tested whether dietary indigestible saccharides, utilised as a substrate to produce SCFA by gut microbiota, would increase colonic 5-HT content in mice. Male C...
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Veröffentlicht in: | British journal of nutrition 2022-02, Vol.127 (4), p.513-525 |
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creator | Tatsuoka, Misa Osaki, Yosuke Ohsaka, Fumina Tsuruta, Takeshi Kadota, Yoshihiro Tochio, Takumi Hino, Shingo Morita, Tatsuya Sonoyama, Kei |
description | SCFA increase serotonin (5-hydroxytryptamine, 5-HT) synthesis and content in the colon in vitro and ex vivo, but little is known in vivo. We tested whether dietary indigestible saccharides, utilised as a substrate to produce SCFA by gut microbiota, would increase colonic 5-HT content in mice. Male C57BL/6J mice were fed a purified diet and water supplemented with 4 % (w/v) 1-kestose (KES) for 2 weeks. Colonic 5-HT content and enterochromaffin (EC) cell numbers were lower in mice supplemented with KES than those without supplementation, while monoamine oxidase A activity and mRNA levels of tryptophan hydroxylase 1 (Tph1), chromogranin A (Chga), Slc6a4 and monoamine oxidase A (Maoa) genes in the colonic mucosa, serum 5-HT concentration and total 5-HT content in the colonic contents did not differ between groups. Caecal acetate concentration and Bifidobacterium pseudolongum population were higher in KES-supplemented mice. Similar trends were observed in mice supplemented with other indigestible saccharides, that is, fructo-oligosaccharides, inulin and raffinose. Intragastric administration of live B. pseudolongum (108 colony-forming units/d) for 2 weeks reduced colonic 5-HT content and EC cell numbers. These results suggest that changes in synthesis, reuptake, catabolism and overflow of 5-HT in the colonic mucosa are not involved in the reduction of colonic 5-HT content by dietary indigestible saccharides in mice. We propose that gut microbes including B. pseudolongum could contribute to the reduction of 5-HT content in the colonic mucosa via diminishing EC cells. |
doi_str_mv | 10.1017/S0007114521001306 |
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We tested whether dietary indigestible saccharides, utilised as a substrate to produce SCFA by gut microbiota, would increase colonic 5-HT content in mice. Male C57BL/6J mice were fed a purified diet and water supplemented with 4 % (w/v) 1-kestose (KES) for 2 weeks. Colonic 5-HT content and enterochromaffin (EC) cell numbers were lower in mice supplemented with KES than those without supplementation, while monoamine oxidase A activity and mRNA levels of tryptophan hydroxylase 1 (Tph1), chromogranin A (Chga), Slc6a4 and monoamine oxidase A (Maoa) genes in the colonic mucosa, serum 5-HT concentration and total 5-HT content in the colonic contents did not differ between groups. Caecal acetate concentration and Bifidobacterium pseudolongum population were higher in KES-supplemented mice. Similar trends were observed in mice supplemented with other indigestible saccharides, that is, fructo-oligosaccharides, inulin and raffinose. Intragastric administration of live B. pseudolongum (108 colony-forming units/d) for 2 weeks reduced colonic 5-HT content and EC cell numbers. These results suggest that changes in synthesis, reuptake, catabolism and overflow of 5-HT in the colonic mucosa are not involved in the reduction of colonic 5-HT content by dietary indigestible saccharides in mice. We propose that gut microbes including B. pseudolongum could contribute to the reduction of 5-HT content in the colonic mucosa via diminishing EC cells.</description><identifier>ISSN: 0007-1145</identifier><identifier>EISSN: 1475-2662</identifier><identifier>DOI: 10.1017/S0007114521001306</identifier><identifier>PMID: 33849681</identifier><language>eng</language><publisher>Cambridge, UK: Cambridge University Press</publisher><subject>Acetic acid ; Acids ; Amine oxidase (flavin-containing) ; Animals ; Bifidobacterium ; Bifidobacterium pseudolongum ; Carbohydrates ; Catabolism ; Colon ; Colon - metabolism ; Diet ; Drinking water ; Fermentation ; Fructooligosaccharides ; Intestinal microflora ; Intestinal Mucosa - metabolism ; Laboratory animals ; Male ; Manufacturers ; Mice ; Mice, Inbred C57BL ; Microbiota ; Molecular Nutrition ; Monoamine Oxidase - metabolism ; mRNA ; Mucosa ; Nutrition ; Oligosaccharides ; Overflow ; Oxidase ; Raffinose ; Reduction ; Saccharides ; Serotonin ; Serotonin - metabolism ; Substrates ; Synthesis ; Tryptophan ; Tryptophan hydroxylase ; Water purification</subject><ispartof>British journal of nutrition, 2022-02, Vol.127 (4), p.513-525</ispartof><rights>The Author(s), 2021. Published by Cambridge University Press on behalf of The Nutrition Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c483t-87918cdf5e452c230c28133c2256676f8781564a4b9f635af7cbf02abffe04503</citedby><cites>FETCH-LOGICAL-c483t-87918cdf5e452c230c28133c2256676f8781564a4b9f635af7cbf02abffe04503</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.cambridge.org/core/product/identifier/S0007114521001306/type/journal_article$$EHTML$$P50$$Gcambridge$$H</linktohtml><link.rule.ids>164,314,776,780,27901,27902,55603</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33849681$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tatsuoka, Misa</creatorcontrib><creatorcontrib>Osaki, Yosuke</creatorcontrib><creatorcontrib>Ohsaka, Fumina</creatorcontrib><creatorcontrib>Tsuruta, Takeshi</creatorcontrib><creatorcontrib>Kadota, Yoshihiro</creatorcontrib><creatorcontrib>Tochio, Takumi</creatorcontrib><creatorcontrib>Hino, Shingo</creatorcontrib><creatorcontrib>Morita, Tatsuya</creatorcontrib><creatorcontrib>Sonoyama, Kei</creatorcontrib><title>Consumption of indigestible saccharides and administration of Bifidobacterium pseudolongum reduce mucosal serotonin in murine colonic mucosa</title><title>British journal of nutrition</title><addtitle>Br J Nutr</addtitle><description>SCFA increase serotonin (5-hydroxytryptamine, 5-HT) synthesis and content in the colon in vitro and ex vivo, but little is known in vivo. We tested whether dietary indigestible saccharides, utilised as a substrate to produce SCFA by gut microbiota, would increase colonic 5-HT content in mice. Male C57BL/6J mice were fed a purified diet and water supplemented with 4 % (w/v) 1-kestose (KES) for 2 weeks. Colonic 5-HT content and enterochromaffin (EC) cell numbers were lower in mice supplemented with KES than those without supplementation, while monoamine oxidase A activity and mRNA levels of tryptophan hydroxylase 1 (Tph1), chromogranin A (Chga), Slc6a4 and monoamine oxidase A (Maoa) genes in the colonic mucosa, serum 5-HT concentration and total 5-HT content in the colonic contents did not differ between groups. Caecal acetate concentration and Bifidobacterium pseudolongum population were higher in KES-supplemented mice. Similar trends were observed in mice supplemented with other indigestible saccharides, that is, fructo-oligosaccharides, inulin and raffinose. Intragastric administration of live B. pseudolongum (108 colony-forming units/d) for 2 weeks reduced colonic 5-HT content and EC cell numbers. These results suggest that changes in synthesis, reuptake, catabolism and overflow of 5-HT in the colonic mucosa are not involved in the reduction of colonic 5-HT content by dietary indigestible saccharides in mice. We propose that gut microbes including B. pseudolongum could contribute to the reduction of 5-HT content in the colonic mucosa via diminishing EC cells.</description><subject>Acetic acid</subject><subject>Acids</subject><subject>Amine oxidase (flavin-containing)</subject><subject>Animals</subject><subject>Bifidobacterium</subject><subject>Bifidobacterium pseudolongum</subject><subject>Carbohydrates</subject><subject>Catabolism</subject><subject>Colon</subject><subject>Colon - metabolism</subject><subject>Diet</subject><subject>Drinking water</subject><subject>Fermentation</subject><subject>Fructooligosaccharides</subject><subject>Intestinal microflora</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Laboratory animals</subject><subject>Male</subject><subject>Manufacturers</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Microbiota</subject><subject>Molecular Nutrition</subject><subject>Monoamine Oxidase - metabolism</subject><subject>mRNA</subject><subject>Mucosa</subject><subject>Nutrition</subject><subject>Oligosaccharides</subject><subject>Overflow</subject><subject>Oxidase</subject><subject>Raffinose</subject><subject>Reduction</subject><subject>Saccharides</subject><subject>Serotonin</subject><subject>Serotonin - metabolism</subject><subject>Substrates</subject><subject>Synthesis</subject><subject>Tryptophan</subject><subject>Tryptophan hydroxylase</subject><subject>Water purification</subject><issn>0007-1145</issn><issn>1475-2662</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNp1kc9uFDEMxiMEotvCA3BBkbhwmRInmSR7LCtoK1XiAJxHmfxZUs0k22Ry6Dvw0GTULZWKOFiW458_x_oQegfkHAjIT98JIRKA9xQIAUbEC7QBLvuOCkFfos3a7tb-CTot5baVCsj2NTphTPGtULBBv3cpljoflpAiTh6HaMPelSWMk8NFG_NL52BdwTparO0cYihL1o_45-CDTaM2i8uhzvhQXLVpSnHfiuxsNQ7P1aSiJ1xcTkuKIbYl7TGH6LBZ2WCOzBv0yuupuLfHfIZ-fv3yY3fV3Xy7vN5d3HSGK7Z0Sm5BGet71y43lBFDFTBmKO2FkMIrqaAXXPNx6wXrtZdm9ITq0XtHeE_YGfr4oHvI6a62a4c5FOOmSUeXahloD1Ry4II29MMz9DbVHNvvBioobUHkSsEDZXIqJTs_HHKYdb4fgAyrVcM_VrWZ90flOs7O_p149KYB7Ciq57GZsHdPu_8v-wcJxZ_d</recordid><startdate>20220228</startdate><enddate>20220228</enddate><creator>Tatsuoka, Misa</creator><creator>Osaki, Yosuke</creator><creator>Ohsaka, Fumina</creator><creator>Tsuruta, Takeshi</creator><creator>Kadota, Yoshihiro</creator><creator>Tochio, Takumi</creator><creator>Hino, Shingo</creator><creator>Morita, Tatsuya</creator><creator>Sonoyama, Kei</creator><general>Cambridge University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QP</scope><scope>7RV</scope><scope>7T5</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8C1</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AN0</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope></search><sort><creationdate>20220228</creationdate><title>Consumption of indigestible saccharides and administration of Bifidobacterium pseudolongum reduce mucosal serotonin in murine colonic mucosa</title><author>Tatsuoka, Misa ; Osaki, Yosuke ; Ohsaka, Fumina ; Tsuruta, Takeshi ; Kadota, Yoshihiro ; Tochio, Takumi ; Hino, Shingo ; Morita, Tatsuya ; Sonoyama, Kei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c483t-87918cdf5e452c230c28133c2256676f8781564a4b9f635af7cbf02abffe04503</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Acetic acid</topic><topic>Acids</topic><topic>Amine oxidase (flavin-containing)</topic><topic>Animals</topic><topic>Bifidobacterium</topic><topic>Bifidobacterium pseudolongum</topic><topic>Carbohydrates</topic><topic>Catabolism</topic><topic>Colon</topic><topic>Colon - metabolism</topic><topic>Diet</topic><topic>Drinking water</topic><topic>Fermentation</topic><topic>Fructooligosaccharides</topic><topic>Intestinal microflora</topic><topic>Intestinal Mucosa - metabolism</topic><topic>Laboratory animals</topic><topic>Male</topic><topic>Manufacturers</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Microbiota</topic><topic>Molecular Nutrition</topic><topic>Monoamine Oxidase - metabolism</topic><topic>mRNA</topic><topic>Mucosa</topic><topic>Nutrition</topic><topic>Oligosaccharides</topic><topic>Overflow</topic><topic>Oxidase</topic><topic>Raffinose</topic><topic>Reduction</topic><topic>Saccharides</topic><topic>Serotonin</topic><topic>Serotonin - metabolism</topic><topic>Substrates</topic><topic>Synthesis</topic><topic>Tryptophan</topic><topic>Tryptophan hydroxylase</topic><topic>Water purification</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tatsuoka, Misa</creatorcontrib><creatorcontrib>Osaki, Yosuke</creatorcontrib><creatorcontrib>Ohsaka, Fumina</creatorcontrib><creatorcontrib>Tsuruta, Takeshi</creatorcontrib><creatorcontrib>Kadota, Yoshihiro</creatorcontrib><creatorcontrib>Tochio, Takumi</creatorcontrib><creatorcontrib>Hino, Shingo</creatorcontrib><creatorcontrib>Morita, Tatsuya</creatorcontrib><creatorcontrib>Sonoyama, Kei</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Immunology Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Public Health Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>British Nursing Database</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Research Library (Corporate)</collection><collection>Nursing & Allied Health Premium</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><jtitle>British journal of nutrition</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tatsuoka, Misa</au><au>Osaki, Yosuke</au><au>Ohsaka, Fumina</au><au>Tsuruta, Takeshi</au><au>Kadota, Yoshihiro</au><au>Tochio, Takumi</au><au>Hino, Shingo</au><au>Morita, Tatsuya</au><au>Sonoyama, Kei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Consumption of indigestible saccharides and administration of Bifidobacterium pseudolongum reduce mucosal serotonin in murine colonic mucosa</atitle><jtitle>British journal of nutrition</jtitle><addtitle>Br J Nutr</addtitle><date>2022-02-28</date><risdate>2022</risdate><volume>127</volume><issue>4</issue><spage>513</spage><epage>525</epage><pages>513-525</pages><issn>0007-1145</issn><eissn>1475-2662</eissn><abstract>SCFA increase serotonin (5-hydroxytryptamine, 5-HT) synthesis and content in the colon in vitro and ex vivo, but little is known in vivo. We tested whether dietary indigestible saccharides, utilised as a substrate to produce SCFA by gut microbiota, would increase colonic 5-HT content in mice. Male C57BL/6J mice were fed a purified diet and water supplemented with 4 % (w/v) 1-kestose (KES) for 2 weeks. Colonic 5-HT content and enterochromaffin (EC) cell numbers were lower in mice supplemented with KES than those without supplementation, while monoamine oxidase A activity and mRNA levels of tryptophan hydroxylase 1 (Tph1), chromogranin A (Chga), Slc6a4 and monoamine oxidase A (Maoa) genes in the colonic mucosa, serum 5-HT concentration and total 5-HT content in the colonic contents did not differ between groups. Caecal acetate concentration and Bifidobacterium pseudolongum population were higher in KES-supplemented mice. Similar trends were observed in mice supplemented with other indigestible saccharides, that is, fructo-oligosaccharides, inulin and raffinose. Intragastric administration of live B. pseudolongum (108 colony-forming units/d) for 2 weeks reduced colonic 5-HT content and EC cell numbers. These results suggest that changes in synthesis, reuptake, catabolism and overflow of 5-HT in the colonic mucosa are not involved in the reduction of colonic 5-HT content by dietary indigestible saccharides in mice. We propose that gut microbes including B. pseudolongum could contribute to the reduction of 5-HT content in the colonic mucosa via diminishing EC cells.</abstract><cop>Cambridge, UK</cop><pub>Cambridge University Press</pub><pmid>33849681</pmid><doi>10.1017/S0007114521001306</doi><tpages>13</tpages></addata></record> |
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subjects | Acetic acid Acids Amine oxidase (flavin-containing) Animals Bifidobacterium Bifidobacterium pseudolongum Carbohydrates Catabolism Colon Colon - metabolism Diet Drinking water Fermentation Fructooligosaccharides Intestinal microflora Intestinal Mucosa - metabolism Laboratory animals Male Manufacturers Mice Mice, Inbred C57BL Microbiota Molecular Nutrition Monoamine Oxidase - metabolism mRNA Mucosa Nutrition Oligosaccharides Overflow Oxidase Raffinose Reduction Saccharides Serotonin Serotonin - metabolism Substrates Synthesis Tryptophan Tryptophan hydroxylase Water purification |
title | Consumption of indigestible saccharides and administration of Bifidobacterium pseudolongum reduce mucosal serotonin in murine colonic mucosa |
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