Skip to main content Accessibility help
×
Home
Hostname: page-component-8bbf57454-nshs2 Total loading time: 0.351 Render date: 2022-01-22T09:02:26.774Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

Consumption of indigestible saccharides and administration of Bifidobacterium pseudolongum reduce mucosal serotonin in murine colonic mucosa

Published online by Cambridge University Press:  14 April 2021

Misa Tatsuoka
Affiliation:
Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Sapporo, Japan
Yosuke Osaki
Affiliation:
Graduate School of Life Science, Hokkaido University, Sapporo 060-8589, Sapporo, Japan
Fumina Ohsaka
Affiliation:
Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Sapporo, Japan
Takeshi Tsuruta
Affiliation:
Graduate School of Environmental and Life Science, Okayama University, Okayama 700-8530, Okayama, Japan
Yoshihiro Kadota
Affiliation:
B Food Science, Co. Ltd., Chita 478-0046, Chita, Japan
Takumi Tochio
Affiliation:
B Food Science, Co. Ltd., Chita 478-0046, Chita, Japan
Shingo Hino
Affiliation:
College of Agriculture, Academic Institute, Shizuoka University, Shizuoka 422-8529, Shizuoka, Japan
Tatsuya Morita
Affiliation:
College of Agriculture, Academic Institute, Shizuoka University, Shizuoka 422-8529, Shizuoka, Japan
Kei Sonoyama*
Affiliation:
Research Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Sapporo, Japan
*
* Corresponding author: Kei Sonoyama, email ksnym@chem.agr.hokudai.ac.jp

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.

Type
Full Papers
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

These authors contributed equally to this work.

References

Banskota, S, Ghia, JE & Khan, WI (2019) Serotonin in the gut: blessing or a curse. Biochimie 161, 5664.CrossRefGoogle ScholarPubMed
Mawe, GM & Hoffman, JM (2013) Serotonin signaling in the gastrointestinal tract: functions, dysfunctions, and therapeutic targets. Nat Rev Gastroenterol Hepatol 10, 473486.CrossRefGoogle ScholarPubMed
Spohn, SN & Mawe, GM (2017) Non-conventional features of peripheral serotonin signalling: the gut and beyond. Nat Rev Gastroenterol Hepatol 14, 412420.CrossRefGoogle ScholarPubMed
Sudo, N (2019) Biogenic amines: signals between commensal microbiota and gut physiology. Front Endocrinol 10, 504.CrossRefGoogle ScholarPubMed
Reigstad, CS, Salmonson, CE, Rainey, JF, et al. (2015) Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells. FASEB J 29, 13951403.CrossRefGoogle ScholarPubMed
Yano, JM, Yu, K, Donaldson, GP, et al. (2015) Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161, 264276.CrossRefGoogle ScholarPubMed
Fukumoto, S, Tatewaki, M, Yamada, T, et al. (2003) Short-chain fatty acids stimulate colonic transit via intraluminal 5-HT release in rats. Am J Physiol Regul Integr Comp Physiol 284, R1269R1276.CrossRefGoogle ScholarPubMed
Tsuruta, T, Saito, T, Osaki, Y, et al. (2016) Organoids as an ex vivo model for studying the serotonin system in the murine small intestine and colon epithelium. Biochem Biophys Res Commun 474, 161167.CrossRefGoogle Scholar
Tochio, T, Kitaura, Y, Nakamura, S, et al. (2016) An alteration in the cecal microbiota composition by feeding of 1-kestose results in a marked increase in the cecal butyrate content in rats. PLoS One 11, e0166850.CrossRefGoogle Scholar
Watanabe, A, Kadota, Y, Yokoyama, H, et al. (2019) Experimental determination of the threshold dose for bifidogenic activity of dietary 1-kestose in rats. Foods 9, E4.CrossRefGoogle ScholarPubMed
Ide, K, Shinohara, M, Yamagishi, S, et al. (2020) Kestose supplementation exerts bifidogenic effect within fecal microbiota and increases fecal butyrate concentration in dogs. J Vet Med Sci 82, 18.CrossRefGoogle ScholarPubMed
Tochio, T, Kadota, Y, Tanaka, T, et al. (2018) 1-Kestose, the smallest fructooligosaccharide component, which efficiently stimulates Faecalibacterium prausnitzii as well as bifidobacteria in humans. Foods 7, E140.CrossRefGoogle ScholarPubMed
Endo, A, Hirano, K, Ose, R, et al. (2020) Impact of kestose supplementation on the healthy adult microbiota in in vitro fecal batch cultures. Anaerobe 61, 102076.CrossRefGoogle ScholarPubMed
Udomsopagit, T, Miwa, A, Seki, M, et al. (2020) Intestinal microbiota transplantation reveals the role of microbiota in dietary regulation of RegIIIβ and RegIIIγ expression in mouse intestine. Biochem Biophys Res Commun 529, 6469.CrossRefGoogle ScholarPubMed
Hugenholtz, F & de Vos, WM (2018) Mouse models for human intestinal microbiota research: a critical evaluation. Cell Mol Life Sci 75, 149160.CrossRefGoogle ScholarPubMed
Sasajima, N, Ogasawara, T, Takemura, N, et al. (2010) Role of intestinal Bifidobacterium pseudolongum in dietary fructo-oligosaccharide inhibition of 2,4-dinitrofluorobenzene-induced contact hypersensitivity in mice. Br J Nutr 103, 539548.CrossRefGoogle ScholarPubMed
Sugahara, H, Odamaki, T, Hashikura, N, et al. (2015) Differences in folate production by bifidobacteria of different origins. Biosci Microbiota Food Health 34, 8793.CrossRefGoogle ScholarPubMed
Roy, D (2001) Media for the isolation and enumeration of bifidobacteria in dairy products. Int J Food Microbiol 69, 167182.CrossRefGoogle ScholarPubMed
Morita, T, Kasaoka, S, Ohhashi, A, et al. (1998) Resistant proteins alter cecal short-chain fatty acid profiles in rats fed high amylose cornstarch. J Nutr 128, 11561164.CrossRefGoogle ScholarPubMed
Aoki-Yoshida, A, Saito, S, Tsuruta, T, et al. (2017) Exosomes isolated from sera of mice fed Lactobacillus strains affect inflammatory cytokine production in macrophages in vitro . Biochem Biophys Res Commun 489, 248254.CrossRefGoogle ScholarPubMed
Massironi, S, Zilli, A, Cavalcoli, F, et al. (2016) Chromogranin A and other enteroendocrine markers in inflammatory bowel disease. Neuropeptides 58, 127134.CrossRefGoogle ScholarPubMed
Bustin, SA, Benes, V, Garson, JA, et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55, 611622.CrossRefGoogle ScholarPubMed
Okumura, M, Hamada, A, Ohsaka, F, et al. (2020) Expression of serotonin receptor HTR4 in glucagon-like peptide-1-positive enteroendocrine cells of the murine intestine. Pflügers Arch 472, 15211532.CrossRefGoogle ScholarPubMed
Faul, F, Erdfelder, E, Lang, A-G, et al. (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39, 175191.CrossRefGoogle ScholarPubMed
Friswell, MK, Gika, H, Stratford, IJ, et al. (2010) Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PLoS One 5, e8584.CrossRefGoogle ScholarPubMed
Nair, AB & Jacob, S (2016) A simple practice guide for dose conversion between animals and human. J Basic Clin Pharm 7, 2731.CrossRefGoogle ScholarPubMed
Roberfroid, MB (2005) Introducing inulin-type fructans. Br J Nutr 93, S13S25.CrossRefGoogle ScholarPubMed
Kleessen, B, Sykura, B, Zunft, HJ, et al. (1997) Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. Am J Clin Nutr 65, 13971402.CrossRefGoogle ScholarPubMed
Buddington, RK, Williams, CH, Chen, SC, et al. (1996) Dietary supplement of neosugar alters the fecal flora and decreases activities of some reductive enzymes in human subjects. Am J Clin Nutr 63, 709716.CrossRefGoogle ScholarPubMed
Gershon, MD & Tack, J (2007) The serotonin signaling system: from basic understanding to drug development for functional GI disorders. Gastroenterology 132, 397414.CrossRefGoogle ScholarPubMed
Gavini, F, Delcenserie, V, Kopeinig, K, et al. (2006) Bifidobacterium species isolated from animal feces and from beef and pork meat. J Food Prot 69, 871877.CrossRefGoogle ScholarPubMed
Kwon, YH, Wang, H, Denou, E, et al. (2019) Modulation of gut microbiota composition by serotonin signaling influences intestinal immune response and susceptibility to colitis. Cell Mol Gastroenterol Hepatol 7, 709728.CrossRefGoogle ScholarPubMed
Fung, TC, Vuong, HE, Luna, CDG, et al. (2019) Intestinal serotonin and fluoxetine exposure modulate bacterial colonization in the gut. Nat Microbiol 4, 20642073.CrossRefGoogle Scholar
de Bruïne, AP, Dinjens, WN, Zijlema, JH, et al. (1992) Renewal of enterochromaffin cells in the rat caecum. Anat Rec 233, 7582.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Tatsuoka et al. supplementary material

Tatsuoka et al. supplementary material

Download Tatsuoka et al. supplementary material(PDF)
PDF 650 KB
1
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Consumption of indigestible saccharides and administration of Bifidobacterium pseudolongum reduce mucosal serotonin in murine colonic mucosa
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Consumption of indigestible saccharides and administration of Bifidobacterium pseudolongum reduce mucosal serotonin in murine colonic mucosa
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Consumption of indigestible saccharides and administration of Bifidobacterium pseudolongum reduce mucosal serotonin in murine colonic mucosa
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *