Effect of the probiotic Lactobacillus plantarum IS-10506 on BDNF and 5HT stimulation: role of intestinal microbiota on the gut-brain axis

Reza Ranuh, Alpha Fardah Athiyyah, Andy Darma, Vitria Prasetyo Risky, Wibi Riawan, Ingrid S Surono, Subijanto Marto Sudarmo, Reza Ranuh, Alpha Fardah Athiyyah, Andy Darma, Vitria Prasetyo Risky, Wibi Riawan, Ingrid S Surono, Subijanto Marto Sudarmo

Abstract

Background and objectives: Microbial communities residing in the gut play a major role in the communication between the gut and the brain through neural, immune, and hormonal routes. Changes in abundance of beneficial intestinal bacteria can affect health of individuals. Conversely, drugs, disease, diet and other factors can alter the gut microbiome. However, there is limited information on the effect of exogenous factors on gut microbiota. In this study, we investigated whether a beneficial bacterium, the probiotic Lactobacillus plantarum IS-10506, can stimulate the gut-brain axis using Wistar rats.

Materials and methods: The animals were divided into two groups: one received L. plantarum IS strain 10506 supplementation, while the control group received no treatment. Activation of the gut-brain axis was evaluated by immunohistochemical analysis of intestinal and brain serotonin (5-HT) and brain neurotrophin (NT), serotonin transporter (5-HTT), and brain-derived neurotrophic factor (BDNF) levels.

Results: The results showed that BDNF (p< 0.000), NT (p< 0.000007), and 5-HTT (p< 0.000007) expression was upregulated in the brain along with intestinal 5-HT (p< 0.000) level in rats treated with L. plantarum strain IS-10506 relative to the control group.

Conclusion: The probiotic L. plantarum IS-10506 stimulates the gut-brain axis and can potentially promote brain development and function.

Keywords: Brain-derived neurotrophic factor; Gut–brain axis; Probiotic Lactobacillus plantarum IS 10506; Serotonin.

Figures

Fig. 1.
Fig. 1.
Representative image of intestinal 5-HT expression in control rats, as detected by immunohistochemistry (400× magnification).
Fig. 2.
Fig. 2.
Representative image of intestinal 5-HT in rats treated with L. plantarum IS-19596 (400× magnification).
Fig. 3.
Fig. 3.
Quantitative analysis of intestinal 5-HT levels in L. plantarum IS-10506 treated and control rats. Data represent mean ± SE (n = 10/group).
Fig. 4.
Fig. 4.
Representative image of brain BDNF expression in control rats, as detected by immunohistochemistry (400× magnification).
Fig. 5.
Fig. 5.
Representative image of brain BDNF expression in rats treated with L. plantarum IS-10506 (400× magnification).
Fig. 6.
Fig. 6.
Quantitative analysis of intestinal BDNF levels in L. plantarum IS-10506 treated and control rats. Data represent mean ± SE (n = 10/group).
Fig. 7.
Fig. 7.
Representative image of brain 5-HTT expression in control rats, as detected by immunohistochemistry (400× magnification).
Fig. 8.
Fig. 8.
Representative image of brain 5-HTT expression in rats treated with L. plantarum IS-10506 (400× magnification).
Fig. 9.
Fig. 9.
Quantitative analysis of brain 5-HTT levels in L. plantarum IS-10506 treated and control rats. Data represent mean ± SE (n = 10/group).
Fig. 10.
Fig. 10.
Representative image of brain NT expression in control rats, as detected by immunohistochemistry (400× magnification).
Fig. 11.
Fig. 11.
Representative image of brain NT expression in rats treated with L. plantarum IS-10506 (400× magnification).
Fig. 12.
Fig. 12.
Quantitative analysis of brain NT levels in L. plantarum IS-10506 treated and control rats. Data represent mean ± SE (n = 10/group).

References

    1. Carabotti M, Scirocco A, Antonietta M, Severi C. The gut-brain axis : interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol 2015; 28:203–209.
    1. Cao H, Liu X, An Y, Zhou G, Liu Y, Xu M. Dysbiosis contributes to chronic constipation development via regulation of serotonin transporter in the intestine. Sci Rep 2017;7:10322.
    1. Chen JJ, Li Z, Pan H, Murphy DL, Tamir H, Koepsell H, et al. 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. J Neurosci 2001;21:6348–6361.
    1. Foster JA, Rinaman L, Cryan JF. Stress & the gut-brain axis: Regulation by the microbiome. Neurobiol Stress 2017;7:124–136.
    1. Farzi A, Fröhlich EE, Holzer P. Gut microbiota and the neuroendocrine system. Neurotherapeutics 2018;15:5–22.
    1. Dinan TG, Cryan JF. The microbiome-gut-brain axis in health and disease. Gastroenterol Clin North Am 2017;46:77–89.
    1. Cerdó T, Ruíz A, Suárez A, Campoy C. Probiotic, pebiotic, and brain development. Nutrients 2017;9(11):E1247.
    1. Popova NK, Naumenko VS. 5-HT 1A receptor as a key player in the brain 5-HT system. Rev Neurosci 2013;24:191–204.
    1. Colucci R, Gambaccini D, Ghisu N, Rossi G, Costa F, Tuccori M, et al. Influence of the serotonin transporter 5HTTLPR polymorphism on symptom severity in irritable bowel syndrome. PLoS One 2013;8(2):e54831.
    1. Morse JK, Wiegand SJ, Anderson K, You Y, Cai N, Carnahan J, et al. Brain-derived neurotrophic factor (BDNF) prevents the degeneration of medial septal cholinergic neurons following fimbria transection. J Neurosci 1993;13:4146–4156.
    1. Montiel-Castro AJ, González-Cervantes RM, Bravo-Ruiseco G, Pacheco-López G. The microbiota-gut-brain axis: neurobehavioral correlates, health and sociality. Front Integr Neurosci 2013;7:70.
    1. Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y, et al. Brain, behavior, and immunity altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun 2015;48:186–194.
    1. Sarkar A, Lehto SM, Harty S, Dinan TG, Cryan JF, Burnet PWJ. Psychobiotics and the manipulation of bacteria–gut–brain signals. Trends Neurosci 2016;39:763–781.
    1. Hata T, Asano Y, Yoshihara K, Kimura-Todani T, Miyata N, Zhang XT, et al. Regulation of gut luminal serotonin by commensal microbiota in mice. PLoS One 2017;12(7):e0180745.
    1. Malinova TS, Dijkstra CD, de Vries HE. Serotonin: A mediator of the gut-brain axis in multiple sclerosis. Mult Scler 2018;24:1144–1150.
    1. Martinowich K, Lu B. Interaction between BDNF and serotonin: role in mood disorders. Neuropsychopharmacology 2008;33:73–83.
    1. Pittalà V, Salerno L, Modica M, Siracusa MA, Romeo G. 5-HT 7 receptor ligands: recent developments and potential therapeutic applications. Mini Rev Med Chem 2007;7:945–960.
    1. Articles I, Academy N. Neurotrophin release by neurotrophins: Implications for activity-dependent neuronal plasticity. Proc Natl Acad Sci U S A 1997;94:13279–13286.
    1. Erny D, Hrabě de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 2015;18:965–977.
    1. Evrensel A, Ceylan ME. Gut-microbiota-brain axis: the missing link in depression. Clin Psychopharmacol Neurosci 2015;13:239–244.
    1. George R, Kumar J, Gouda S, Park Y, Shin H, Das G. Science direct benefaction of probiotics for human health: A review. J Food Drug Anal 2018;26:927–939.
    1. Mayer EA. Gut feelings: the emerging biology of gut–brain communication. Nat Rev Neurosci 2011;12:453–466.
    1. Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F. Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 2006;24: 1850–1856.
    1. Aidy Sahar El, Ramsteijn Anouschka S., Dini-Andreote Francisco, van Eijk Roel, Houwing Danielle J., Salles Joana F., et al. Serotonin transporter genotype modulates the gut microbiota composition in young rats, an effect augmented by early life stress. Front Cell Neurosci 2017; 11: 222.
    1. Wang YM, Ge XZ, Wang WQ, Wang T, Cao HL, Wang BL, et al. Lactobacillus rhamnosus GG supernatant up-regulates serotonin trasporter expression in intestinal epithelial cells and mice intestinal tissues. Neurogastroenterol Motil 2015; 27: 1239–1248.
    1. Canossa M, Giordano E, Cappello S, Guarnieri C, Frri S. Nitric oxide down-regulates brain-derived neurotrophoc factor secretion in culture hippocampal neurons. Proc Natl Acad Sci U S A 2002;99:3282–3287.

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