Limosilactobacillus reuteri ATCC 6475 metabolites upregulate the serotonin transporter in the intestinal epithelium
In: Beneficial Microbes
Authors:
,
,
,
,
,
,
,
,
, and
M. Engevik
M. Engevik
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Department of Regenerative Medicine & Cell Biology, Medical University of South Carolina, 173 Ashely Ave, BSB 626, Charleston, SC 29425, USA.
Search for other papers by M. Engevik in
Current site
Google Scholar
Department of Regenerative Medicine & Cell Biology, Medical University of South Carolina, 173 Ashely Ave, BSB 626, Charleston, SC 29425, USA.
Search for other papers by M. Engevik in
Current site
Google Scholar
W. Ruan
W. Ruan
Department of Pediatrics, Baylor College of Medicine, 6701 Fannin Street, Houston, TX 77030, USA.
Section of Gastroenterology, Hepatology, and Nutrition, Texas Children’s Hospital, 6701 Fannin St, Houston, TX 77030, USA.
Search for other papers by W. Ruan in
Current site
Google Scholar
Section of Gastroenterology, Hepatology, and Nutrition, Texas Children’s Hospital, 6701 Fannin St, Houston, TX 77030, USA.
Search for other papers by W. Ruan in
Current site
Google Scholar
C. Visuthranukul
C. Visuthranukul
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Pediatric Nutrition Research Unit, Department of Pediatrics, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
Search for other papers by C. Visuthranukul in
Current site
Google Scholar
Pediatric Nutrition Research Unit, Department of Pediatrics, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
Search for other papers by C. Visuthranukul in
Current site
Google Scholar
Z. Shi
Z. Shi
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by Z. Shi in
Current site
Google Scholar
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by Z. Shi in
Current site
Google Scholar
K.A. Engevik
K.A. Engevik
Department of Molecular Virology & Microbiology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 7703, USA.
Search for other papers by K.A. Engevik in
Current site
Google Scholar
Search for other papers by K.A. Engevik in
Current site
Google Scholar
A.C. Engevik
A.C. Engevik
Departments of Surgery, Vanderbilt University Medical Center, 1211 Medical Center Dr, Nashville, TN 37232, USA.
Search for other papers by A.C. Engevik in
Current site
Google Scholar
Search for other papers by A.C. Engevik in
Current site
Google Scholar
R. Fultz
R. Fultz
Department of Neuroscience, Cell Biology, and Anatomy, University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555-0625, USA.
Search for other papers by R. Fultz in
Current site
Google Scholar
Search for other papers by R. Fultz in
Current site
Google Scholar
D.A. Schady
D.A. Schady
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by D.A. Schady in
Current site
Google Scholar
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by D.A. Schady in
Current site
Google Scholar
J.K. Spinler
J.K. Spinler
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by J.K. Spinler in
Current site
Google Scholar
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by J.K. Spinler in
Current site
Google Scholar
J. Versalovic
J. Versalovic
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by J. Versalovic in
Current site
Google Scholar
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by J. Versalovic in
Current site
Google Scholar
The serotonin transporter (SERT) readily takes up serotonin (5-HT), thereby regulating the availability of 5-HT within the intestine. In the absence of SERT, 5-HT remains in the interstitial space and has the potential to aberrantly activate the many 5-HT receptors distributed on the epithelium, immune cells and enteric neurons. Perturbation of SERT is common in many gastrointestinal disorders as well as mouse models of colitis. Select commensal microbes regulate intestinal SERT levels, but the mechanism of this regulation is poorly understood. Additionally, ethanol upregulates SERT in the brain and dendritic cells, but its effects in the intestine have never been examined. We report that the intestinal commensal microbe Limosilactobacillus (previously classified as Lactobacillus) reuteri ATCC PTA 6475 secretes 83.4 mM ethanol. Consistent with the activity of L. reuteri alcohol dehydrogenases, we found that L. reuteri tolerated various levels of ethanol. Application of L. reuteri conditioned media or exogenous ethanol to human colonic T84 cells was found to upregulate SERT at the level of mRNA. A 4-(4-(dimethylamino) phenyl)-1-methylpyridinium (APP+) uptake assay confirmed the functional activity of SERT. These findings were mirrored in mouse colonic organoids, where L. reuteri metabolites and ethanol were found to upregulate SERT at the apical membrane. Finally, in a trinitrobenzene sulphonic acid model of acute colitis, we observed that mice treated with L. reuteri maintained SERT at the colon membrane compared with mice receiving phosphate buffered saline vehicle control. These data suggest that L. reuteri metabolites, including ethanol, can upregulate SERT and may be beneficial for maintaining intestinal homeostasis with respect to serotonin signalling.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
Akiba, Y., Inoue, T., Kaji, I., Higashiyama, M., Narimatsu, K., Iwamoto, K., Watanabe, M., Guth, P.H., Engel, E., Kuwahara, A. and Kaunitz, J.D., 2015. Short-chain fatty acid sensing in rat duodenum. Journal of Physiology 593: 585-599. https://doi.org/10.1113/jphysiol.2014.280792
-
Amirov, N. and Trubitsyna, I.E., 1981. [Role of serotonin in the pathogenesis of ulcer development]. Biulleten Eksperimentalnoi Biologii i Meditsiny 92: 23-26.
'[Role of serotonin in the pathogenesis of ulcer development] ' () 92 Biulleten Eksperimentalnoi Biologii i Meditsiny : 23 -26.
-
Arskold, E., Lohmeier-Vogel, E., Cao, R., Roos, S., Radstrom, P. and van Niel, E.W., 2008. Phosphoketolase pathway dominates in Lactobacillus reuteri ATCC 55730 containing dual pathways for glycolysis. Journal of Bacteriology 190: 206-212. https://doi.org/10.1128/JB.01227-07
-
Atkinson, J.P., Sullivan, T.J., Kelly, J.P. and Parker, C.W., 1977. Stimulation by alcohols of cyclic AMP metabolism in human leukocytes. Possible role of cyclic AMP in the anti-inflammatory effects of ethanol. Journal of Clinical Investigation 60: 284-294. https://doi.org/10.1172/JCI108776
-
Babu, D.K., Diaz, A., Samikkannu, T., Rao, K.V., Saiyed, Z.M., Rodriguez, J.W. and Nair, M.P., 2009. Upregulation of serotonin transporter by alcohol in human dendritic cells: possible implication in neuroimmune deregulation. Alcoholism, Clinical and Experimental Research 33: 1731-1738. https://doi.org/10.1111/j.1530-0277.2009.01010.x
-
Baganz, N.L. and Blakely, R.D., 2013. A dialogue between the immune system and brain, spoken in the language of serotonin. ACS Chemical Neuroscience 4: 48-63. https://doi.org/10.1021/cn300186b
-
Bellini, M., Rappelli, L., Blandizzi, C., Costa, F., Stasi, C., Colucci, R., Giannaccini, G., Marazziti, D., Betti, L., Baroni, S., Mumolo, M.G., Marchi, S. and Del Tacca, M., 2003. Platelet serotonin transporter in patients with diarrhea-predominant irritable bowel syndrome both before and after treatment with alosetron. American Journal of Gastroenterology 98: 2705-2711. https://doi.org/10.1111/j.1572-0241.2003.08669.x
-
Bellono, N.W., Bayrer, J.R., Leitch, D.B., Castro, J., Zhang, C., O’Donnell, T.A., Brierley, S.M., Ingraham, H.A. and Julius, D., 2017. Enterochromaffin cells are gut chemosensors that couple to sensory neural pathways. Cell 170: 185-198 e116. https://doi.org/10.1016/j.cell.2017.05.034
-
Bertrand, P.P. and Bertrand, R.L., 2010. Serotonin release and uptake in the gastrointestinal tract. Autonomic Neuroscience 153: 47-57. https://doi.org/10.1016/j.autneu.2009.08.002
-
Bertrand, P.P., Barajas-Espinosa, A., Neshat, S., Bertrand, R.L. and Lomax, A.E., 2010. Analysis of real-time serotonin (5-HT) availability during experimental colitis in mouse. American Journal of Physiology – Gastrointestinal and Liver Physiology 298: G446-G455. https://doi.org/10.1152/ajpgi.00318.2009
-
Bischoff, S.C., Mailer, R., Pabst, O., Weier, G., Sedlik, W., Li, Z., Chen, J.J., Murphy, D.L. and Gershon, M.D., 2009. Role of serotonin in intestinal inflammation: knockout of serotonin reuptake transporter exacerbates 2,4,6-trinitrobenzene sulfonic acid colitis in mice. American Journal of Physiology – Gastrointestinal and Liver Physiology 296: G685-G695. https://doi.org/10.1152/ajpgi.90685.2008
-
Blakely, R.D., Berson, H.E., Fremeau, R.T., Jr., Caron, M.G., Peek, M.M., Prince, H.K. and Bradley, C.C., 1991. Cloning and expression of a functional serotonin transporter from rat brain. Nature 354: 66-70. https://doi.org/10.1038/354066a0
-
Blomberg, L., Henriksson, A. and Conway, P.L., 1993. Inhibition of adhesion of Escherichia coli K88 to piglet ileal mucus by Lactobacillus spp. Applied and Environmental Microbiology 59: 34-39.
'Inhibition of adhesion of Escherichia coli K88 to piglet ileal mucus by Lactobacillus spp ' () 59 Applied and Environmental Microbiology : 34 -39.
-
Bode, C., Vollmer, E., Hug, J. and Bode, J.C., 1991. Increased permeability of the gut to polyethylene glycol and dextran in rats fed alcohol. Annals of the New York Academy of Sciences 625: 837-840. https://doi.org/10.1111/j.1749-6632.1991.tb33931.x
-
Bohle, L.A., Brede, D.A., Diep, D.B., Holo, H. and Nes, I.F., 2010. Specific degradation of the mucus adhesion-promoting protein (MapA) of Lactobacillus reuteri to an antimicrobial peptide. Applied and Environmental Microbiology 76: 7306-7309. https://doi.org/10.1128/AEM.01423-10
-
Broer, S. and Gether, U., 2012. The solute carrier 6 family of transporters. British Journal of Pharmacology 167: 256-278. https://doi.org/10.1111/j.1476-5381.2012.01975.x
-
Brownstein, M.J. and Hoffman, B.J., 1994. Neurotransmitter transporters. Recent Progress in Hormone Research 49: 27-42.
'Neurotransmitter transporters ' () 49 Recent Progress in Hormone Research : 27 -42.
-
Cao, Y.N., Feng, L.J., Liu, Y.Y., Jiang, K., Zhang, M.J., Gu, Y.X., Wang, B.M., Gao, J., Wang, Z.L. and Wang, Y.M., 2018a. Effect of Lactobacillus rhamnosus GG supernatant on serotonin transporter expression in rats with post-infectious irritable bowel syndrome. World Journal of Gastroenterology 24: 338-350. https://doi.org/10.3748/wjg.v24.i3.338
-
Cao, Y.N., Feng, L.J., Wang, B.M., Jiang, K., Li, S., Xu, X., Wang, W.Q., Zhao, J.W. and Wang, Y.M., 2018b. Lactobacillus acidophilus and Bifidobacterium longum supernatants upregulate the serotonin transporter expression in intestinal epithelial cells. Saudi Journal of Gastroenterology 24: 59-66. https://doi.org/10.4103/sjg.SJG_333_17
-
Carasi, P., Ambrosis, N.M., De Antoni, G.L., Bressollier, P., Urdaci, M.C. and Serradell Mde, L., 2014. Adhesion properties of potentially probiotic Lactobacillus kefiri to gastrointestinal mucus. Journal of Dairy Research 81: 16-23. https://doi.org/10.1017/S0022029913000526
-
Chang-Graham, A.L., Danhof, H.A., Engevik, M.A., Tomaro-Duchesneau, C., Karandikar, U.C., Estes, M.K., Versalovic, J., Britton, R.A. and Hyser, J.M., 2019. Human intestinal enteroids with inducible neurogenin-3 expression as a novel model of gut hormone secretion. Cellular and Molecular Gastroenterology and Hepatology 8: 209-229. https://doi.org/10.1016/j.jcmgh.2019.04.010
-
Chen, J.J., Li, Z., Pan, H., Murphy, D.L., Tamir, H., Koepsell, H. and Gershon, M.D., 2001. Maintenance of serotonin in the intestinal mucosa and ganglia of mice that lack the high-affinity serotonin transporter: Abnormal intestinal motility and the expression of cation transporters. Journal of Neuroscience 21: 6348-6361.
'Maintenance of serotonin in the intestinal mucosa and ganglia of mice that lack the high-affinity serotonin transporter: Abnormal intestinal motility and the expression of cation transporters ' () 21 Journal of Neuroscience : 6348 -6361.
-
Chen, J.X., Pan, H., Rothman, T.P., Wade, P.R. and Gershon, M.D., 1998. Guinea pig 5-HT transporter: cloning, expression, distribution, and function in intestinal sensory reception. American Journal of Physiology 275: G433-448.
'Guinea pig 5-HT transporter: cloning, expression, distribution, and function in intestinal sensory reception ' () 275 American Journal of Physiology : G433 -448.
-
Chen, M., Gao, L., Chen, P., Feng, D., Jiang, Y., Chang, Y., Jin, J., Chu, F.F. and Gao, Q., 2016. Serotonin-exacerbated DSS-induced colitis is associated with increase in MMP-3 and MMP-9 expression in the mouse colon. Mediators of Inflammation 2016: 5359768. https://doi.org/10.1155/2016/5359768
-
Clarke, G., Cryan, J.F., Dinan, T.G. and Quigley, E.M., 2012. Review article: probiotics for the treatment of irritable bowel syndrome-focus on lactic acid bacteria. Alimentary Pharmacology and Therapeutics 35: 403-413. https://doi.org/10.1111/j.1365-2036.2011.04965.x
-
Coates, M.D., Mahoney, C.R., Linden, D.R., Sampson, J.E., Chen, J., Blaszyk, H., Crowell, M.D., Sharkey, K.A., Gershon, M.D., Mawe, G.M. and Moses, P.L., 2004. Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome. Gastroenterology 126: 1657-1664.
'Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome ' () 126 Gastroenterology : 1657 -1664.
-
Coconnier, M.H., Klaenhammer, T.R., Kerneis, S., Bernet, M.F. and Servin, A.L., 1992. Protein-mediated adhesion of Lactobacillus acidophilus BG2FO4 on human enterocyte and mucus-secreting cell lines in culture. Applied and Environmental Microbiology 58: 2034-2039.
'Protein-mediated adhesion of Lactobacillus acidophilus BG2FO4 on human enterocyte and mucus-secreting cell lines in culture ' () 58 Applied and Environmental Microbiology : 2034 -2039.
-
Committee, N.N.R., Michail, S., Sylvester, F., Fuchs, G. and Issenman, R., 2006. Clinical efficacy of probiotics: review of the evidence with focus on children. Journal of Pediatric Gastroenterology and Nutrition 43: 550-557. https://doi.org/10.1097/01.mpg.0000239990.35517.bf
-
Costedio, M.M., Coates, M.D., Danielson, A.B., Buttolph, T.R., 3rd, Blaszyk, H.J., Mawe, G.M. and Hyman, N.H., 2008. Serotonin signaling in diverticular disease. Journal of Gastrointestinal Surgery 12: 1439-1445. https://doi.org/10.1007/s11605-008-0536-5
-
Daws, L.C., Montanez, S., Munn, J.L., Owens, W.A., Baganz, N.L., Boyce-Rustay, J.M., Millstein, R.A., Wiedholz, L.M., Murphy, D.L. and Holmes, A., 2006. Ethanol inhibits clearance of brain serotonin by a serotonin transporter-independent mechanism. Journal of Neuroscience 26: 6431-6438. https://doi.org/10.1523/JNEUROSCI.4050-05.2006
-
Elamin, E.E., Masclee, A.A., Dekker, J. and Jonkers, D.M., 2013. Ethanol metabolism and its effects on the intestinal epithelial barrier. Nutrition Reviews 71: 483-499. https://doi.org/10.1111/nure.12027
-
Elshaghabee, F.M., Bockelmann, W., Meske, D., de Vrese, M., Walte, H.G., Schrezenmeir, J. and Heller, K.J., 2016. Ethanol production by selected intestinal microorganisms and lactic acid bacteria growing under different nutritional conditions. Frontiers in Microbiology 7: 47. https://doi.org/10.3389/fmicb.2016.00047
-
Engevik, M.A., Aihara, E., Montrose, M.H., Shull, G.E., Hassett, D.J. and Worrell, R.T., 2013a. Loss of NHE3 alters gut microbiota composition and influences Bacteroides thetaiotaomicron growth. American Journal of Physiology – Gastrointestinal and Liver Physiology 305: G697-G711. https://doi.org/10.1152/ajpgi.00184.2013
-
Engevik, M.A., Engevik, K.A., Yacyshyn, M.B., Wang, J., Hassett, D.J., Darien, B., Yacyshyn, B.R. and Worrell, R.T., 2015. Human Clostridium difficile infection: inhibition of NHE3 and microbiota profile. American Journal of Physiology – Gastrointestinal and Liver Physiology 308: G497-G509. https://doi.org/10.1152/ajpgi.00090.2014
-
Engevik, M.A., Faletti, C.J., Paulmichl, M., Worrell, R.T., 2013b. Prebiotic properties of galursan HF 7K on mouse gut microbiota. Cellular Physiology and Biochemistry 32: 96-110.
'Prebiotic properties of galursan HF 7K on mouse gut microbiota ' () 32 Cellular Physiology and Biochemistry : 96 -110.
-
Engevik, M.A., Hickerson, A., Shull, G.E., Worrell, R.T., 2013c. Acidic conditions in the NHE2-/- mouse intestine result in an altered mucosa-associated bacterial population with changes in mucus oligosaccharides. Cellular Physiology and Biochemistry 32: 111-128.
'Acidic conditions in the NHE2-/- mouse intestine result in an altered mucosa-associated bacterial population with changes in mucus oligosaccharides ' () 32 Cellular Physiology and Biochemistry : 111 -128.
-
Engevik, M.A., Luck, B., Visuthranukul, C., Ihekweazu, F.D., Engevik, A.C., Shi, Z., Danhof, H.A., Chang-Graham, A., Hall, A., Endres, B.T., Haidacher, S.J., Horvath, T.D., Haag, A.M., Devaraj, S., Garey, K.W., Britton, R.A., Hyser, J.M., Shroyer, N.F. and Versalovic, J., 2020. Human-derived Bifidobacterium dentium modulates the mammalian serotonergic system and gut-brain axis. Cellular and Molecular Gastroenterology and Hepatology. https://doi.org/10.1016/j.jcmgh.2020.08.002
-
Engevik, M.A., Morra, C.N., Roth, D., Engevik, K., Spinler, J.K., Devaraj, S., Crawford, S.E., Estes, M.K., Kalkum, M. and Versalovic, J., 2019. Microbial metabolic capacity for intestinal folate production and modulation of host folate receptors. Frontiers in Microbiology 10: 2305. https://doi.org/10.3389/fmicb.2019.02305
-
Engevik, M.A., Ruan, W., Esparza, M., Fultz, R., Shi, Z., Engevik, K.A., Engevik, A.C., Ihekweazu, F.D., Visuthranukul, C., Venable, S., Schady, D.A. and Versalovic, J., 2021. Immunomodulation of dendritic cells by Lactobacillus reuteri surface components and metabolites. Physiol Rep 9: e14719. https://doi.org/10.14814/phy2.14719
-
Esmaili, A., Nazir, S.F., Borthakur, A., Yu, D., Turner, J.R., Saksena, S., Singla, A., Hecht, G.A., Alrefai, W.A. and Gill, R.K., 2009. Enteropathogenic Escherichia coli infection inhibits intestinal serotonin transporter function and expression. Gastroenterology 137: 2074-2083. https://doi.org/10.1053/j.gastro.2009.09.002
-
Fang, T.J., Guo, J.T., Lin, M.K., Lee, M.S., Chen, Y.L. and Lin, W.H., 2019. Protective effects of Lactobacillus plantarum against chronic alcohol-induced liver injury in the murine model. Applied Microbiology and Biotechnology 103: 8597-8608. https://doi.org/10.1007/s00253-019-10122-8
-
Farmer, S.G. and Laniyonu, A.A., 1984. Effects of p-chlorophenylalanine on the sensitivity of rat intestine to agonists and on intestinal 5-hydroxytryptamine levels during Nippostrongylus brasiliensis infection. British Journal of Pharmacology 82: 883-889.
'Effects of p-chlorophenylalanine on the sensitivity of rat intestine to agonists and on intestinal 5-hydroxytryptamine levels during Nippostrongylus brasiliensis infection ' () 82 British Journal of Pharmacology : 883 -889.
-
Fernando, E.H., Dicay, M., Stahl, M., Gordon, M.H., Vegso, A., Baggio, C., Alston, L., Lopes, F., Baker, K., Hirota, S., McKay, D.M., Vallance, B. and MacNaughton, W.K., 2017. A simple, cost-effective method for generating murine colonic 3D enteroids and 2D monolayers for studies of primary epithelial cell function. American Journal of Physiology – Gastrointestinal and Liver Physiology 313: G467-G475. https://doi.org/10.1152/ajpgi.00152.2017
-
Foley, K.F., Pantano, C., Ciolino, A. and Mawe, G.M., 2007. IFN-gamma and TNF-alpha decrease serotonin transporter function and expression in Caco2 cells. American Journal of Physiology – Gastrointestinal and Liver Physiology 292: G779-G784. https://doi.org/10.1152/ajpgi.00470.2006
-
Forsyth, C.B., Farhadi, A., Jakate, S.M., Tang, Y., Shaikh, M. and Keshavarzian, A., 2009. Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 43: 163-172. https://doi.org/10.1016/j.alcohol.2008.12.009
-
Fukumoto, S., Tatewaki, M., Yamada, T., Fujimiya, M., Mantyh, C., Voss, M., Eubanks, S., Harris, M., Pappas, T.N. and Takahashi, T., 2003. Short-chain fatty acids stimulate colonic transit via intraluminal 5-HT release in rats. American Journal of Physiology – Regulatory Integrative and Comparative Physiology 284: R1269-R1276. https://doi.org/10.1152/ajpregu.00442.2002
-
Gershon, M.D., 2013. 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract. Current Opinion in Endocrinology, Diabetes, and Obesity 20: 14-21. https://doi.org/10.1097/MED.0b013e32835bc703
-
Gershon, M.D. and Sherman, D.L., 1982. Identification of and interactions between noradrenergic and serotonergic neurites in the myenteric plexus. Journal of Comparative Neurology 204: 407-421. https://doi.org/10.1002/cne.902040411
-
Gershon, M.D. and Tack, J., 2007. The serotonin signaling system: from basic understanding to drug development for functional GI disorders. Gastroenterology 132: 397-414. https://doi.org/10.1053/j.gastro.2006.11.002
-
Gershon, M.D., Sherman, D.L. and Pintar, J.E., 1990. Type-specific localization of monoamine oxidase in the enteric nervous system: relationship to 5-hydroxytryptamine, neuropeptides, and sympathetic nerves. Journal of Comparative Neurology 301: 191-213. https://doi.org/10.1002/cne.903010205
-
Ghia, J.E., Li, N., Wang, H., Collins, M., Deng, Y., El-Sharkawy, R.T., Cote, F., Mallet, J. and Khan, W.I., 2009. Serotonin has a key role in pathogenesis of experimental colitis. Gastroenterology 137: 1649-1660. https://doi.org/10.1053/j.gastro.2009.08.041
-
Gill, R.K., Pant, N., Saksena, S., Singla, A., Nazir, T.M., Vohwinkel, L., Turner, J.R., Goldstein, J., Alrefai, W.A. and Dudeja, P.K., 2008. Function, expression, and characterization of the serotonin transporter in the native human intestine. American Journal of Physiology – Gastrointestinal and Liver Physiology 294: G254-G262. https://doi.org/10.1152/ajpgi.00354.2007
-
Gill, R.K., Saksena, S., Tyagi, S., Alrefai, W.A., Malakooti, J., Sarwar, Z., Turner, J.R., Ramaswamy, K. and Dudeja, P.K., 2005. Serotonin inhibits Na+/H+ exchange activity via 5-HT4 receptors and activation of PKC alpha in human intestinal epithelial cells. Gastroenterology 128: 962-974.
'Serotonin inhibits Na+/H+ exchange activity via 5-HT4 receptors and activation of PKC alpha in human intestinal epithelial cells ' () 128 Gastroenterology : 962 -974.
-
Goldin, B.R. and Gorbach, S.L., 2008. Clinical indications for probiotics: an overview. Clinical Infectious Diseases 46 Suppl 2: S96-100; discussion S144-151. https://doi.org/10.1086/523333
-
Gu, Z., Wu, Y., Wang, Y., Sun, H., You, Y., Piao, C., Liu, J. and Wang, Y., 2020. Lactobacillus rhamnosus granules dose-dependently balance intestinal microbiome disorders and ameliorate chronic alcohol-induced liver injury. Journal of Medicinal Food 23: 114-124. https://doi.org/10.1089/jmf.2018.4357
-
Guglielmetti, S., Mora, D., Gschwender, M. and Popp, K., 2011. Randomised clinical trial: Bifidobacterium bifidum MIMBb75 significantly alleviates irritable bowel syndrome and improves quality of life – a double-blind, placebo-controlled study. Alimentary Pharmacology and Therapeutics 33: 1123-1132. https://doi.org/10.1111/j.1365-2036.2011.04633.x
-
Hata, T., Asano, Y., Yoshihara, K., Kimura-Todani, T., Miyata, N., Zhang, X.T., Takakura, S., Aiba, Y., Koga, Y. and Sudo, N., 2017. Regulation of gut luminal serotonin by commensal microbiota in mice. PLoS ONE 12: e0180745. https://doi.org/10.1371/journal.pone.0180745
-
Haub, S., Kanuri, G., Volynets, V., Brune, T., Bischoff, S.C. and Bergheim, I., 2010a. Serotonin reuptake transporter (SERT) plays a critical role in the onset of fructose-induced hepatic steatosis in mice. American Journal of Physiology – Gastrointestinal and Liver Physiology 298: G335-G344. https://doi.org/10.1152/ajpgi.00088.2009
-
Haub, S., Ritze, Y., Bergheim, I., Pabst, O., Gershon, M.D. and Bischoff, S.C., 2010b. Enhancement of intestinal inflammation in mice lacking interleukin 10 by deletion of the serotonin reuptake transporter. Neurogastroenterology and Motility 22: 826-834, e229. https://doi.org/10.1111/j.1365-2982.2010.01479.x
-
He, B., Hoang, T.K., Tian, X., Taylor, C.M., Blanchard, E., Luo, M., Bhattacharjee, M.B., Freeborn, J., Park, S., Couturier, J., Lindsey, J.W., Tran, D.Q., Rhoads, J.M. and Liu, Y., 2019. Lactobacillus reuteri reduces the severity of experimental autoimmune encephalomyelitis in mice by modulating gut microbiota. Frontiers in Immunology 10: 385. https://doi.org/10.3389/fimmu.2019.00385
-
He, B., Hoang, T.K., Wang, T., Ferris, M., Taylor, C.M., Tian, X., Luo, M., Tran, D.Q., Zhou, J., Tatevian, N., Luo, F., Molina, J.G., Blackburn, M.R., Gomez, T.H., Roos, S., Rhoads, J.M. and Liu, Y., 2017. Resetting microbiota by Lactobacillus reuteri inhibits T reg deficiency-induced autoimmunity via adenosine A2A receptors. Journal of Experimental Medicine 214: 107-123. https://doi.org/10.1084/jem.20160961
-
Henriksson, A. and Conway, P.L., 1996. Adhesion of Lactobacillus fermentum 104-S to porcine stomach mucus. Current Microbiology 33: 31-34.
'Adhesion of Lactobacillus fermentum 104-S to porcine stomach mucus ' () 33 Current Microbiology : 31 -34.
-
Hoffman, B.J., Mezey, E. and Brownstein, M.J., 1991. Cloning of a serotonin transporter affected by antidepressants. Science 254: 579-580.
'Cloning of a serotonin transporter affected by antidepressants ' () 254 Science : 579 -580.
-
Hoffman, J.M., Tyler, K., MacEachern, S.J., Balemba, O.B., Johnson, A.C., Brooks, E.M., Zhao, H., Swain, G.M., Moses, P.L., Galligan, J.J., Sharkey, K.A., Greenwood-Van Meerveld, B. and Mawe, G.M., 2012. Activation of colonic mucosal 5-HT(4) receptors accelerates propulsive motility and inhibits visceral hypersensitivity. Gastroenterology 142: 844-854 e844. https://doi.org/10.1053/j.gastro.2011.12.041
-
Holford, N.H., 1987. Clinical pharmacokinetics of ethanol. Clinical Pharmacokinetics 13: 273-292. https://doi.org/10.2165/00003088-198713050-00001
-
Jacobsen, C.N., Rosenfeldt Nielsen, V., Hayford, A.E., Moller, P.L., Michaelsen, K.F., Paerregaard, A., Sandstrom, B., Tvede, M. and Jakobsen, M., 1999. Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Applied and Environmental Microbiology 65: 4949-4956.
'Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans ' () 65 Applied and Environmental Microbiology : 4949 -4956.
-
Jensen, H., Roos, S., Jonsson, H., Rud, I., Grimmer, S., van Pijkeren, J.P., Britton, R.A. and Axelsson, L., 2014. Role of Lactobacillus reuteri cell and mucus-binding protein A (CmbA) in adhesion to intestinal epithelial cells and mucus in vitro. Microbiology 160: 671-681. https://doi.org/10.1099/mic.0.073551-0
-
Jonsson, H., Strom, E. and Roos, S., 2001. Addition of mucin to the growth medium triggers mucus-binding activity in different strains of Lactobacillus reuteri in vitro. FEMS Microbiology Letters 204: 19-22.
'Addition of mucin to the growth medium triggers mucus-binding activity in different strains of Lactobacillus reuteri in vitro ' () 204 FEMS Microbiology Letters : 19 -22.
-
Karsenty, G. and Gershon, M.D., 2011. The importance of the gastrointestinal tract in the control of bone mass accrual. Gastroenterology 141: 439-442. https://doi.org/10.1053/j.gastro.2011.06.011
-
Kato, K., Mizuno, S., Umesaki, Y., Ishii, Y., Sugitani, M., Imaoka, A., Otsuka, M., Hasunuma, O., Kurihara, R., Iwasaki, A. and Arakawa, Y., 2004. Randomized placebo-controlled trial assessing the effect of bifidobacteria-fermented milk on active ulcerative colitis. Alimentary Pharmacology and Therapeutics 20: 1133-1141. https://doi.org/10.1111/j.1365-2036.2004.02268.x
-
Kato, S., Matsuda, N., Matsumoto, K., Wada, M., Onimaru, N., Yasuda, M., Amagase, K., Horie, S. and Takeuchi, K., 2012. Dual role of serotonin in the pathogenesis of indomethacin-induced small intestinal ulceration: pro-ulcerogenic action via 5-HT3 receptors and anti-ulcerogenic action via 5-HT4 receptors. Pharmacological Research 66: 226-234. https://doi.org/10.1016/j.phrs.2012.06.002
-
Kelai, S., Aissi, F., Lesch, K.P., Cohen-Salmon, C., Hamon, M. and Lanfumey, L., 2003. Alcohol intake after serotonin transporter inactivation in mice. Alcohol 38: 386-389.
'Alcohol intake after serotonin transporter inactivation in mice ' () 38 Alcohol : 386 -389.
-
Keshavarzian, A., Choudhary, S., Holmes, E.W., Yong, S., Banan, A., Jakate, S. and Fields, J.Z., 2001. Preventing gut leakiness by oats supplementation ameliorates alcohol-induced liver damage in rats. Journal of Pharmacology and Experimental Therapeutics 299: 442-448.
'Preventing gut leakiness by oats supplementation ameliorates alcohol-induced liver damage in rats ' () 299 Journal of Pharmacology and Experimental Therapeutics : 442 -448.
-
Keshavarzian, A., Farhadi, A., Forsyth, C.B., Rangan, J., Jakate, S., Shaikh, M., Banan, A. and Fields, J.Z., 2009. Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. Journal of Hepatology 50: 538-547. https://doi.org/10.1016/j.jhep.2008.10.028
-
Khan, W.I., Motomura, Y., Wang, H., El-Sharkawy, R.T., Verdu, E.F., Verma-Gandhu, M., Rollins, B.J. and Collins, S.M., 2006. Critical role of MCP-1 in the pathogenesis of experimental colitis in the context of immune and enterochromaffin cells. American Journal of Physiology – Gastrointestinal and Liver Physiology 291: G803-811. https://doi.org/10.1152/ajpgi.00069.2006
-
Kim, J.J. and Khan, W.I., 2014. 5-HT7 receptor signaling: improved therapeutic strategy in gut disorders. Frontiers in Behavioral Neuroscience 8: 396. https://doi.org/10.3389/fnbeh.2014.00396
-
Kopp-Hoolihan, L., 2001. Prophylactic and therapeutic uses of probiotics: a review. Journal of the American Dietetic Association 101: 229-238; quiz 239-241. https://doi.org/10.1016/S0002-8223(01)00060-8
-
Kristensen, A.S., Andersen, J., Jorgensen, T.N., Sorensen, L., Eriksen, J., Loland, C.J., Stromgaard, K. and Gether, U., 2011. SLC6 neurotransmitter transporters: structure, function, and regulation. Pharmacological Reviews 63: 585-640. https://doi.org/10.1124/pr.108.000869
-
Lambert, J.C., Zhou, Z., Wang, L., Song, Z., McClain, C.J. and Kang, Y.J., 2003. Prevention of alterations in intestinal permeability is involved in zinc inhibition of acute ethanol-induced liver damage in mice. Journal of Pharmacology and Experimental Therapeutics 305: 880-886. https://doi.org/10.1124/jpet.102.047852
-
Latorre, E., Layunta, E., Grasa, L., Castro, M., Pardo, J., Gomollon, F., Alcalde, A.I. and Mesonero, J.E., 2016a. Intestinal serotonin transporter inhibition by Toll-like receptor 2 activation. A feedback modulation. PLoS ONE 11: e0169303. https://doi.org/10.1371/journal.pone.0169303
-
Latorre, E., Pradilla, A., Chueca, B., Pagan, R., Layunta, E., Alcalde, A.I. and Mesonero, J.E., 2016b. Listeria monocytogenes inhibits serotonin transporter in human intestinal Caco-2 cells. Microbial Ecology 72: 730-739. https://doi.org/10.1007/s00248-016-0809-6
-
Li, F., Duan, K., Wang, C., McClain, C. and Feng, W., 2016. Probiotics and alcoholic liver disease: treatment and potential mechanisms. Gastroenterology Research and Practice 2016: 5491465. https://doi.org/10.1155/2016/5491465
-
Li, N., Ghia, J.E., Wang, H., McClemens, J., Cote, F., Suehiro, Y., Mallet, J. and Khan, W.I., 2011a. Serotonin activates dendritic cell function in the context of gut inflammation. American Journal of Pathology 178: 662-671. https://doi.org/10.1016/j.ajpath.2010.10.028
-
Li, Z., Chalazonitis, A., Huang, Y.Y., Mann, J.J., Margolis, K.G., Yang, Q.M., Kim, D.O., Cote, F., Mallet, J. and Gershon, M.D., 2011b. Essential roles of enteric neuronal serotonin in gastrointestinal motility and the development/survival of enteric dopaminergic neurons. Journal of Neuroscience 31: 8998-9009. https://doi.org/10.1523/JNEUROSCI.6684-10.2011
-
Linden, D.R., Chen, J.X., Gershon, M.D., Sharkey, K.A. and Mawe, G.M., 2003. Serotonin availability is increased in mucosa of guinea pigs with TNBS-induced colitis. American Journal of Physiology Gastrointestinal and Liver Physiology 285: G207-216. https://doi.org/10.1152/ajpgi.00488.2002
-
Linden, D.R., Foley, K.F., McQuoid, C., Simpson, J., Sharkey, K.A. and Mawe, G.M., 2005. Serotonin transporter function and expression are reduced in mice with TNBS-induced colitis. Neurogastroenterology and Motility 17: 565-574. https://doi.org/10.1111/j.1365-2982.2005.00673.x
-
Liu, Q., Duan, Z.P., Ha, D.K., Bengmark, S., Kurtovic, J. and Riordan, S.M., 2004. Synbiotic modulation of gut flora: effect on minimal hepatic encephalopathy in patients with cirrhosis. Hepatology 39: 1441-1449. https://doi.org/10.1002/hep.20194
-
Ma, Y.L., Guo, T., Xu, Z.R., You, P. and Ma, J.F., 2006. Effect of Lactobacillus isolates on the adhesion of pathogens to chicken intestinal mucus in vitro. Letters in Applied Microbiology 42: 369-374. https://doi.org/10.1111/j.1472-765X.2006.01844.x
-
Macias-Rodriguez, M.E., Zagorec, M., Ascencio, F., Vazquez-Juarez, R. and Rojas, M., 2009. Lactobacillus fermentum BCS87 expresses mucus- and mucin-binding proteins on the cell surface. Journal of Applied Microbiology 107: 1866-1874. https://doi.org/10.1111/j.1365-2672.2009.04368.x
-
Mackenzie, D.A., Jeffers, F., Parker, M.L., Vibert-Vallet, A., Bongaerts, R.J., Roos, S., Walter, J. and Juge, N., 2010. Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri. Microbiology 156: 3368-3378. https://doi.org/10.1099/mic.0.043265-0
-
Margolis, K.G. and Pothoulakis, C., 2009. Serotonin has a critical role in the pathogenesis of experimental colitis. Gastroenterology 137: 1562-1566. https://doi.org/10.1053/j.gastro.2009.09.027
-
Martel, F., Monteiro, R. and Lemos, C., 2003. Uptake of serotonin at the apical and basolateral membranes of human intestinal epithelial (Caco-2) cells occurs through the neuronal serotonin transporter (SERT). Journal of Pharmacology and Experimental Therapeutics 306: 355-362. https://doi.org/10.1124/jpet.103.049668
-
Martin, R., Miquel, S., Ulmer, J., Kechaou, N., Langella, P. and Bermudez-Humaran, L.G., 2013. Role of commensal and probiotic bacteria in human health: a focus on inflammatory bowel disease. Microbial Cell Factories 12: 71. https://doi.org/10.1186/1475-2859-12-71
-
Mawe, G.M. and Hoffman, J.M., 2013. Serotonin signalling in the gut--functions, dysfunctions and therapeutic targets. Nature Reviews: Gastroenterology and Hepatology 10: 473-486. https://doi.org/10.1038/nrgastro.2013.105
-
Miyoshi, Y., Okada, S., Uchimura, T. and Satoh, E., 2006. A mucus adhesion promoting protein, MapA, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells. Bioscience Biotechnology and Biochemistry 70: 1622-1628. https://doi.org/10.1271/bbb.50688
-
Nakaita, Y., Kaneda, H. and Shigyo, T., 2013. Heat-killed Lactobacillus brevis SBC8803 induces serotonin release from intestinal cells. Food and Nutrition Sciences 4: 767-771.
'Heat-killed Lactobacillus brevis SBC8803 induces serotonin release from intestinal cells ' () 4 Food and Nutrition Sciences : 767 -771.
-
Narendranath, N.V., Hynes, S.H., Thomas, K.C. and Ingledew, W.M., 1997. Effects of lactobacilli on yeast-catalyzed ethanol fermentations. Applied and Environmental Microbiology 63: 4158-4163. https://doi.org/10.1128/AEM.63.11.4158-4163.1997
-
Nazir, S., Kumar, A., Chatterjee, I., Anbazhagan, A.N., Gujral, T., Priyamvada, S., Saksena, S., Alrefai, W.A., Dudeja, P.K. and Gill, R.K., 2015. Mechanisms of intestinal serotonin transporter (SERT) upregulation by TGF-beta1 induced non-smad pathways. PLoS ONE 10: e0120447. https://doi.org/10.1371/journal.pone.0120447
-
Neufeld, K.M., Kang, N., Bienenstock, J. and Foster, J.A., 2011. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterology and Motility 23: 255-264, e119. https://doi.org/10.1111/j.1365-2982.2010.01620.x
-
Nishino, R., Mikami, K., Takahashi, H., Tomonaga, S., Furuse, M., Hiramoto, T., Aiba, Y., Koga, Y. and Sudo, N., 2013. Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods. Neurogastroenterology and Motility 25: 521-528. https://doi.org/10.1111/nmo.12110
-
Nishiyama, K., Nakamata, K., Ueno, S., Terao, A., Aryantini, N.P., Sujaya, I.N., Fukuda, K., Urashima, T., Yamamoto, Y. and Mukai, T., 2015. Adhesion properties of Lactobacillus rhamnosus mucus-binding factor to mucin and extracellular matrix proteins. Bioscience Biotechnology and Biochemistry 79: 271-279. https://doi.org/10.1080/09168451.2014.972325
-
Nzakizwanayo, J., Dedi, C., Standen, G., Macfarlane, W.M., Patel, B.A. and Jones, B.V., 2015. Escherichia coli Nissle 1917 enhances bioavailability of serotonin in gut tissues through modulation of synthesis and clearance. Scientific Reports 5: 17324. https://doi.org/10.1038/srep17324
-
Oh, J.H., Alexander, L.M., Pan, M., Schueler, K.L., Keller, M.P., Attie, A.D., Walter, J. and van Pijkeren, J.P., 2019. Dietary fructose and microbiota-derived short-chain fatty acids promote bacteriophage production in the gut symbiont Lactobacillus reuteri. Cell Host and Microbe 25: 273-284 e276. https://doi.org/10.1016/j.chom.2018.11.016
-
O’Hara, J.R., Ho, W., Linden, D.R., Mawe, G.M. and Sharkey, K.A., 2004. Enteroendocrine cells and 5-HT availability are altered in mucosa of guinea pigs with TNBS ileitis. American Journal of Physiology – Gastrointestinal and Liver Physiology 287: G998-1007. https://doi.org/10.1152/ajpgi.00090.2004
-
O’Hara, J.R., Skinn, A.C., MacNaughton, W.K., Sherman, P.M. and Sharkey, K.A., 2006. Consequences of Citrobacter rodentium infection on enteroendocrine cells and the enteric nervous system in the mouse colon. Cellular Microbiology 8: 646-660. https://doi.org/10.1111/j.1462-5822.2005.00657.x
-
Oliva, S., Di Nardo, G., Ferrari, F., Mallardo, S., Rossi, P., Patrizi, G., Cucchiara, S. and Stronati, L., 2012. Randomised clinical trial: the effectiveness of Lactobacillus reuteri ATCC 55730 rectal enema in children with active distal ulcerative colitis. Alimentary Pharmacology and Therapeutics 35: 327-334. https://doi.org/10.1111/j.1365-2036.2011.04939.x
-
O’Mahony, L., McCarthy, J., Kelly, P., Hurley, G., Luo, F., Chen, K., O’Sullivan, G.C., Kiely, B., Collins, J.K., Shanahan, F. and Quigley, E.M., 2005. Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 128: 541-551.
'Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles ' () 128 Gastroenterology : 541 -551.
-
O’Sullivan, G.C., Kelly, P., O’Halloran, S., Collins, C., Collins, J.K., Dunne, C. and Shanahan, F., 2005. Probiotics: an emerging therapy. Current Pharmaceutical Design 11: 3-10.
'Probiotics: an emerging therapy ' () 11 Current Pharmaceutical Design : 3 -10.
-
O’Sullivan, M.A. and O’Morain, C.A., 2000. Bacterial supplementation in the irritable bowel syndrome. A randomised double-blind placebo-controlled crossover study. Digestive and Liver Disease 32: 294-301.
'Bacterial supplementation in the irritable bowel syndrome ' () 32 Digestive and Liver Disease : 294 -301.
-
Ouwehand, A.C. and Conway, P.L., 1996. Purification and characterization of a component produced by Lactobacillus fermentum that inhibits the adhesion of K88 expressing Escherichia coli to porcine ileal mucus. Journal of Applied Bacteriology 80: 311-318.
'Purification and characterization of a component produced by Lactobacillus fermentum that inhibits the adhesion of K88 expressing Escherichia coli to porcine ileal mucus ' () 80 Journal of Applied Bacteriology : 311 -318.
-
Parlesak, A., Schafer, C., Schutz, T., Bode, J.C. and Bode, C., 2000. Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. Journal of Hepatology 32: 742-747. https://doi.org/10.1016/s0168-8278(00)80242-1
-
Rabe, C.S., Giri, P.R., Hoffman, P.L. and Tabakoff, B., 1990. Effect of ethanol on cyclic AMP levels in intact PC12 cells. Biochemical Pharmacology 40: 565-571.
'Effect of ethanol on cyclic AMP levels in intact PC12 cells ' () 40 Biochemical Pharmacology : 565 -571.
-
Ramiah, K., van Reenen, C.A. and Dicks, L.M., 2007. Expression of the mucus adhesion genes Mub and MapA, adhesion-like factor EF-Tu and bacteriocin gene plaA of Lactobacillus plantarum 423, monitored with real-time PCR. International Journal of Food Microbiology 116: 405-409. https://doi.org/10.1016/j.ijfoodmicro.2007.02.011
-
Ramiah, K., Van Reenen, C.A. and Dicks, L.M., 2009. Expression of the mucus adhesion gene Mub, surface layer protein Slp and adhesion-like factor EF-TU of Lactobacillus acidophilus ATCC 4356 under digestive stress conditions, as monitored with real-time PCR. Probiotics and Antimicrobial Proteins 1: 91. https://doi.org/10.1007/s12602-009-9009-8
-
Regmi, S.C., Park, S.Y., Ku, S.K. and Kim, J.A., 2014. Serotonin regulates innate immune responses of colon epithelial cells through Nox2-derived reactive oxygen species. Free Radical Biology and Medicine 69: 377-389. https://doi.org/10.1016/j.freeradbiomed.2014.02.003
-
Reigstad, C.S., Salmonson, C.E., Rainey, J.F., 3rd, Szurszewski, J.H., Linden, D.R., Sonnenburg, J.L., Farrugia, G. and Kashyap, P.C., 2015. Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells. FASEB Journal 29: 1395-1403. https://doi.org/10.1096/fj.14-259598
-
Romani Vestman, N., Chen, T., Lif Holgerson, P., Ohman, C. and Johansson, I., 2015. Oral microbiota shift after 12-week supplementation with Lactobacillus reuteri DSM 17938 and PTA 5289; a randomized control trial. PLoS ONE 10: e0125812. https://doi.org/10.1371/journal.pone.0125812
-
Sato, T., Stange, D.E., Ferrante, M., Vries, R.G., Van Es, J.H., Van den Brink, S., Van Houdt, W.J., Pronk, A., Van Gorp, J., Siersema, P.D. and Clevers, H., 2011. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology 141: 1762-1772. https://doi.org/10.1053/j.gastro.2011.07.050
-
Sato, T., Vries, R.G., Snippert, H.J., van de Wetering, M., Barker, N., Stange, D.E., van Es, J.H., Abo, A., Kujala, P., Peters, P.J. and Clevers, H., 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-265. https://doi.org/10.1038/nature07935
-
Shanahan, F., 2009. Therapeutic implications of manipulating and mining the microbiota. Journal of Physiology 587: 4175-4179. https://doi.org/10.1113/jphysiol.2009.174649
-
Shibasaki, M., Inoue, M., Kurokawa, K., Ogou, S. and Ohkuma, S., 2010. Expression of serotonin transporter in mice with ethanol physical dependency. Journal of Pharmacological Sciences 114: 234-237.
'Expression of serotonin transporter in mice with ethanol physical dependency ' () 114 Journal of Pharmacological Sciences : 234 -237.
-
Solis, E., Jr., Zdravkovic, I., Tomlinson, I.D., Noskov, S.Y., Rosenthal, S.J. and De Felice, L.J., 2012. 4-(4-(dimethylamino)phenyl)-1-methylpyridinium (APP+) is a fluorescent substrate for the human serotonin transporter. Journal of Biological Chemistry 287: 8852-8863. https://doi.org/10.1074/jbc.M111.267757
-
Spohn, S.N., Bianco, F., Scott, R.B., Keenan, C.M., Linton, A.A., O’Neill, C.H., Bonora, E., Dicay, M., Lavoie, B., Wilcox, R.L., MacNaughton, W.K., De Giorgio, R., Sharkey, K.A. and Mawe, G.M., 2016. Protective actions of epithelial 5-hydroxytryptamine 4 receptors in normal and inflamed colon. Gastroenterology 151: 933-944, e933. https://doi.org/10.1053/j.gastro.2016.07.032
-
Stansbridge, E.M., Walker, V., Hall, M.A., Smith, S.L., Millar, M.R., Bacon, C. and Chen, S., 1993. Effects of feeding premature infants with Lactobacillus GG on gut fermentation. Archives of Disease in Childhood 69: 488-492. https://doi.org/10.1136/adc.69.5_spec_no.488
-
Szabo, G., Verma, B.K., Fogarasi, M. and Catalano, D.E., 1992. Induction of transforming growth factor-beta and prostaglandin E2 production by ethanol in human monocytes. Journal of Leukocyte Biology 52: 602-610. https://doi.org/10.1002/jlb.52.6.602
-
Tada, Y., Ishihara, S., Kawashima, K., Fukuba, N., Sonoyama, H., Kusunoki, R., Oka, A., Mishima, Y., Oshima, N., Moriyama, I., Yuki, T., Ishikawa, N., Araki, A., Harada, Y., Maruyama, R. and Kinoshita, Y., 2016. Downregulation of serotonin reuptake transporter gene expression in healing colonic mucosa in presence of remaining low-grade inflammation in ulcerative colitis. Journal of Gastroenterology and Hepatology 31: 1443-1452. https://doi.org/10.1111/jgh.13268
-
Takayanagi, S., Hanai, H., Kumagai, J. and Kaneko, E., 1995. Serotonin uptake and its modulation in rat jejunal enterocyte preparation. Journal of Pharmacology and Experimental Therapeutics 272: 1151-1159.
'Serotonin uptake and its modulation in rat jejunal enterocyte preparation ' () 272 Journal of Pharmacology and Experimental Therapeutics : 1151 -1159.
-
Uhlemann, E.R., Robberecht, P. and Gardner, J.D., 1979. Effects of alcohols on the actions of VIP and secretin on acinar cells from guinea pig pancreas. Gastroenterology 76: 917-925.
'Effects of alcohols on the actions of VIP and secretin on acinar cells from guinea pig pancreas ' () 76 Gastroenterology : 917 -925.
-
Van Tassell, M.L. and Miller, M.J., 2011. Lactobacillus adhesion to mucus. Nutrients 3: 613-636. https://doi.org/10.3390/nu3050613
-
Wade, P.R., Chen, J., Jaffe, B., Kassem, I.S., Blakely, R.D. and Gershon, M.D., 1996. Localization and function of a 5-HT transporter in crypt epithelia of the gastrointestinal tract. Journal of Neuroscience 16: 2352-2364.
'Localization and function of a 5-HT transporter in crypt epithelia of the gastrointestinal tract ' () 16 Journal of Neuroscience : 2352 -2364.
-
Wang, Y.M., Ge, X.Z., Wang, W.Q., Wang, T., Cao, H.L., Wang, B.L. and Wang, B.M., 2015. Lactobacillus rhamnosus GG supernatant upregulates serotonin transporter expression in intestinal epithelial cells and mice intestinal tissues. Neurogastroenterology and Motility 27: 1239-1248. https://doi.org/10.1111/nmo.12615
-
Wheatcroft, J., Wakelin, D., Smith, A., Mahoney, C.R., Mawe, G. and Spiller, R., 2005. Enterochromaffin cell hyperplasia and decreased serotonin transporter in a mouse model of postinfectious bowel dysfunction. Neurogastroenterology and Motility 17: 863-870. https://doi.org/10.1111/j.1365-2982.2005.00719.x
-
Wilson, J.N., Ladefoged, L.K., Babinchak, W.M. and Schiott, B., 2014. Binding-induced fluorescence of serotonin transporter ligands: A spectroscopic and structural study of 4-(4-(dimethylamino)phenyl)-1-methylpyridinium (APP(+)) and APP(+) analogues. ACS Chemical Neuroscience 5: 296-304. https://doi.org/10.1021/cn400230x
-
Wolin, M.J., Yerry, S., Miller, T.L., Zhang, Y. and Bank, S., 1998. Changes in production of ethanol, acids and H2 from glucose by the fecal flora of a 16- to 158-d-old breast-fed infant. Journal of Nutrition 128: 85-90. https://doi.org/10.1093/jn/128.1.85
-
Yadav, V.K., Balaji, S., Suresh, P.S., Liu, X.S., Lu, X., Li, Z., Guo, X.E., Mann, J.J., Balapure, A.K., Gershon, M.D., Medhamurthy, R., Vidal, M., Karsenty, G. and Ducy, P., 2010. Pharmacological inhibition of gut-derived serotonin synthesis is a potential bone anabolic treatment for osteoporosis. Nature Medicine 16: 308-312. https://doi.org/10.1038/nm.2098
-
Yammamoto, H., Tanaka, S., Tanaka, A., Hide, I., Seki, T. and Sakai, N., 2013. Long-term exposure of RN46A cells expressing serotonin transporter (SERT) to a cAMP analog up-regulates SERT activity and is accompanied by neural differentiation of the cells. Journal of Pharmacological Sciences 121: 25-38.
'Long-term exposure of RN46A cells expressing serotonin transporter (SERT) to a cAMP analog up-regulates SERT activity and is accompanied by neural differentiation of the cells ' () 121 Journal of Pharmacological Sciences : 25 -38.
-
Yano, J.M., Yu, K., Donaldson, G.P., Shastri, G.G., Ann, P., Ma, L., Nagler, C.R., Ismagilov, R.F., Mazmanian, S.K. and Hsiao, E.Y., 2015. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161: 264-276. https://doi.org/10.1016/j.cell.2015.02.047
-
Zaunmuller, T., Eichert, M., Richter, H. and Unden, G., 2006. Variations in the energy metabolism of biotechnologically relevant heterofermentative lactic acid bacteria during growth on sugars and organic acids. Applied Microbiology and Biotechnology 72: 421-429. https://doi.org/10.1007/s00253-006-0514-3
-
Zhu, C.B., Carneiro, A.M., Dostmann, W.R., Hewlett, W.A. and Blakely, R.D., 2005. p38 MAPK activation elevates serotonin transport activity via a trafficking-independent, protein phosphatase 2A-dependent process. Journal of Biological Chemistry 280: 15649-15658. https://doi.org/10.1074/jbc.M410858200
-
Zocco, M.A., dal Verme, L.Z., Cremonini, F., Piscaglia, A.C., Nista, E.C., Candelli, M., Novi, M., Rigante, D., Cazzato, I.A., Ojetti, V., Armuzzi, A., Gasbarrini, G. and Gasbarrini, A., 2006. Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Alimentary Pharmacology and Therapeutics 23: 1567-1574. https://doi.org/10.1111/j.1365-2036.2006.02927.x
Supplementary Materials
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 0 | 0 | 0 |
| Full Text Views | 934 | 358 | 17 |
| PDF Views & Downloads | 898 | 318 | 6 |
Limosilactobacillus reuteri ATCC 6475 metabolites upregulate the serotonin transporter in the intestinal epithelium
In: Beneficial Microbes
Authors:
,
,
,
,
,
,
,
,
, and
M. Engevik
M. Engevik
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Department of Regenerative Medicine & Cell Biology, Medical University of South Carolina, 173 Ashely Ave, BSB 626, Charleston, SC 29425, USA.
Search for other papers by M. Engevik in
Current site
Google Scholar
PubMed
Department of Regenerative Medicine & Cell Biology, Medical University of South Carolina, 173 Ashely Ave, BSB 626, Charleston, SC 29425, USA.
Search for other papers by M. Engevik in
Current site
Google Scholar
PubMed
W. Ruan
W. Ruan
Department of Pediatrics, Baylor College of Medicine, 6701 Fannin Street, Houston, TX 77030, USA.
Section of Gastroenterology, Hepatology, and Nutrition, Texas Children’s Hospital, 6701 Fannin St, Houston, TX 77030, USA.
Search for other papers by W. Ruan in
Current site
Google Scholar
PubMed
Section of Gastroenterology, Hepatology, and Nutrition, Texas Children’s Hospital, 6701 Fannin St, Houston, TX 77030, USA.
Search for other papers by W. Ruan in
Current site
Google Scholar
PubMed
C. Visuthranukul
C. Visuthranukul
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Pediatric Nutrition Research Unit, Department of Pediatrics, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
Search for other papers by C. Visuthranukul in
Current site
Google Scholar
PubMed
Pediatric Nutrition Research Unit, Department of Pediatrics, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
Search for other papers by C. Visuthranukul in
Current site
Google Scholar
PubMed
Z. Shi
Z. Shi
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by Z. Shi in
Current site
Google Scholar
PubMed
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by Z. Shi in
Current site
Google Scholar
PubMed
K.A. Engevik
K.A. Engevik
Department of Molecular Virology & Microbiology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 7703, USA.
Search for other papers by K.A. Engevik in
Current site
Google Scholar
PubMed
Search for other papers by K.A. Engevik in
Current site
Google Scholar
PubMed
A.C. Engevik
A.C. Engevik
Departments of Surgery, Vanderbilt University Medical Center, 1211 Medical Center Dr, Nashville, TN 37232, USA.
Search for other papers by A.C. Engevik in
Current site
Google Scholar
PubMed
Search for other papers by A.C. Engevik in
Current site
Google Scholar
PubMed
R. Fultz
R. Fultz
Department of Neuroscience, Cell Biology, and Anatomy, University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555-0625, USA.
Search for other papers by R. Fultz in
Current site
Google Scholar
PubMed
Search for other papers by R. Fultz in
Current site
Google Scholar
PubMed
D.A. Schady
D.A. Schady
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by D.A. Schady in
Current site
Google Scholar
PubMed
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by D.A. Schady in
Current site
Google Scholar
PubMed
J.K. Spinler
J.K. Spinler
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by J.K. Spinler in
Current site
Google Scholar
PubMed
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by J.K. Spinler in
Current site
Google Scholar
PubMed
J. Versalovic
J. Versalovic
Department of Pathology & Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by J. Versalovic in
Current site
Google Scholar
PubMed
Department of Pathology, Texas Children’s Hospital, 6621 Fannin St, Houston, TX 77030, USA.
Search for other papers by J. Versalovic in
Current site
Google Scholar
PubMed
The serotonin transporter (SERT) readily takes up serotonin (5-HT), thereby regulating the availability of 5-HT within the intestine. In the absence of SERT, 5-HT remains in the interstitial space and has the potential to aberrantly activate the many 5-HT receptors distributed on the epithelium, immune cells and enteric neurons. Perturbation of SERT is common in many gastrointestinal disorders as well as mouse models of colitis. Select commensal microbes regulate intestinal SERT levels, but the mechanism of this regulation is poorly understood. Additionally, ethanol upregulates SERT in the brain and dendritic cells, but its effects in the intestine have never been examined. We report that the intestinal commensal microbe Limosilactobacillus (previously classified as Lactobacillus) reuteri ATCC PTA 6475 secretes 83.4 mM ethanol. Consistent with the activity of L. reuteri alcohol dehydrogenases, we found that L. reuteri tolerated various levels of ethanol. Application of L. reuteri conditioned media or exogenous ethanol to human colonic T84 cells was found to upregulate SERT at the level of mRNA. A 4-(4-(dimethylamino) phenyl)-1-methylpyridinium (APP+) uptake assay confirmed the functional activity of SERT. These findings were mirrored in mouse colonic organoids, where L. reuteri metabolites and ethanol were found to upregulate SERT at the apical membrane. Finally, in a trinitrobenzene sulphonic acid model of acute colitis, we observed that mice treated with L. reuteri maintained SERT at the colon membrane compared with mice receiving phosphate buffered saline vehicle control. These data suggest that L. reuteri metabolites, including ethanol, can upregulate SERT and may be beneficial for maintaining intestinal homeostasis with respect to serotonin signalling.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 0 | 0 | 0 |
| Full Text Views | 934 | 358 | 17 |
| PDF Views & Downloads | 898 | 318 | 6 |
