Anti-inflammatory and Neuroprotective Effects of Lactobacillus Strains Contribute to its Antidepressant-Like Property Against Chronic Unpredictable Stress-Induced Behavioural Abnormalities in Mice http://www.doi.org/10.26538/tjnpr/v7i8.36

Main Article Content

Olusegun A. Adeoluwa
Gladys O. Adeoluwa
Abiola O. Obisesan
Lily O. Otomewo
Funmilayo R. Adeniyi
Godsgift O. Asigo
Tunde Salawu-Erih
Rebecca K. Efretuei
Patricia E. Chinwuba
Ganiyu A. Bakre

Abstract

Depression is one of the most worrisome disorders of the central nervous system (CNS). Recently, more researchers have delved into studying the links between the gut microbiota and psychiatric disorders such as depression, anxiety, and cognitive impairments such as amnesia. With this novel angle came the research into probiotics, the gut microbiota-modifying bacteria. This study was therefore designed to evaluate the neuroprotective effect of specific probiotic strains on chronic unpredictable stress induced depressive symptoms in mice. Thirty-five mice (20-30 g) were shared into five groups randomly. Groups 1 and 2 received vehicle (10 mL/kg), groups 3 and 4 received probiotics (10 mL/kg), and group 5 received fluoxetine (10 mg/kg). Only groups 2, 3 and 5 were exposed to an unpredictable order of chronic mild stress daily for twenty-one (21) days. Afterward, behavioural, and biochemical assays were carried out. The results revealed that chronic unpredictable stress caused significant (p<0.05) elevation in depressive-like behaviours, increased
the production of proinflammatory cytokines and even signalled hippocampal neurodegeneration. However, a significant (p<0.05) reversal of these effects was observed in the probiotics-treated groups as effectively as the fluoxetine group. It can be concluded that anti-inflammatory and neuroprotective effects of lactobacillus strains may contribute to its antidepressive-like action against CUS-induced depression in mice. 

Downloads

Download data is not yet available.

Article Details

How to Cite
Adeoluwa, O. A., Adeoluwa, G. O., Obisesan, A. O., Otomewo, L. O., Adeniyi, F. R., Asigo, G. O., Salawu-Erih, T., Efretuei, R. K., Chinwuba, P. E., & Bakre, G. A. (2023). Anti-inflammatory and Neuroprotective Effects of Lactobacillus Strains Contribute to its Antidepressant-Like Property Against Chronic Unpredictable Stress-Induced Behavioural Abnormalities in Mice: http://www.doi.org/10.26538/tjnpr/v7i8.36. Tropical Journal of Natural Product Research (TJNPR), 7(8), 3813-3818. https://tjnpr.org/index.php/home/article/view/2464
Section
Articles

How to Cite

Adeoluwa, O. A., Adeoluwa, G. O., Obisesan, A. O., Otomewo, L. O., Adeniyi, F. R., Asigo, G. O., Salawu-Erih, T., Efretuei, R. K., Chinwuba, P. E., & Bakre, G. A. (2023). Anti-inflammatory and Neuroprotective Effects of Lactobacillus Strains Contribute to its Antidepressant-Like Property Against Chronic Unpredictable Stress-Induced Behavioural Abnormalities in Mice: http://www.doi.org/10.26538/tjnpr/v7i8.36. Tropical Journal of Natural Product Research (TJNPR), 7(8), 3813-3818. https://tjnpr.org/index.php/home/article/view/2464

References

Chao L, Liu C, Sutthawongwadee S, Li Y, Lv W, Chen W, Yu L, Zhou J, Guo A, Li Z, Guo S. Effects of probiotics on depressive or anxiety variables in healthy participants under stress conditions or with a depressive or anxiety diagnosis: a meta-analysis of randomized controlled trials. Front Neurol.2020; 11(421):1-10.

Institute of Health Metrics and Evaluation. Global Health Data Exchange (GHDx). http://ghdx.healhdata.org/gbdresults-tool?params=gbd-api-2019-permalink/d780dffbe8a381b25e1416884959e

Zheng P, Wu J, Zhang H, Perry SW, Yin B, Tan X, Chai T, Liang W, Huang Y, Li Y, Duan J, Wong ML, Licinio J, Xie P. The gut microbiome modulates gut-brain axis glycerophospholipid metabolism in a region-specific manner in a nonhuman primate model of depression. Mol Psychiatry. 2021; 26:2380–2392.

L-In V, Saengha W, Karirat T, Konsue A, Wangkahart E, Katisart T. Probiotics from Thai fermented foods reduced anxiety and enhanced neuroplasticity in a Wistar rat model. Trop J Nat Prod Res. 2022; 6(6):910-914. Doi: 10.26538/tjnpr/v6i6.15.

Ajayi AS, Ogunleye BO, Oluwasola MA, Okediya CK, Akpata OB, Akinnola OO. Screening of probiotic characteristics of lactic acid bacteria isolated from some fermented Nigerian food products. Trop J Nat Prod Res. 2020;4(12):1166-1169

Applegate JA, Walker CLF, Ambikapathi R, Black RE. Systematic review of probiotics for the treatment of community-acquired acute diarrhea in children. BMC Public Health 2013; 13(Suppl 3):S16.

Food and Agriculture Organization (FAO) of the United Nations and World Health Organization (WHO). Evaluation of health and nutritional properties of powder milk and live lactic acid bacteria. FAO and WHO Expert Consultation Report 2021.

Li W, Dowd SE, Scurlock B, Acosta-Martinez V, Lyte M. Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria. Physiol Behav.2009; 96:557–567.

Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Nat Acad Sci USA. 2011; 108:16050–16055.

Bravo JA, Julio-Pieper M, Forsythe P, Kunze W, Dinan TG, Bienenstock J, Cryan JF. Communication between gastrointestinal bacteria and the nervous system. Curr Opin Pharmacol. 2012; 12:667–672.

Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 2016; 165:1332-1345.

Distrutti E, Cipriani S, Mencarelli A, Renga B, Fiorucci S. Probiotics VSL#3 Protect against development of visceral pain in murine model of irritable bowel syndrome. PLoS One 2013; 8:e63893.

Leta V, Ray Chaudhuri K, Milner O, Chung-Faye G, Metta V, Pariante CM, Borsini A. Neurogenic and antiinflammatory effects of probiotics in Parkinson's disease: A systematic review of preclinical and clinical evidence. Brain, Behavior, and Immunity 2021;98: 59-73. Accessed using

https://doi.org/10.1016/j.bbi.2021.07.026

Ng QX, Peters C, Ho CYX, Lim DY, Yeo WS. A metaanalysis of the use of probiotics to alleviate depressive symptoms. J Affect Disord2018; 228:13–19.

Marotta A, Sarno E, Del Casale A, Pane M, Mogna L, Amoruso A, Felis GE and Fiorio M. Effects of Probiotics on Cognitive Reactivity, Mood, and Sleep Quality. Front Psychiatry. 2019; 10(164):1-11. Accessed using Doi: 10.3389/fpsyt.2019.00164

Noonan S, Zaveri M, Macaninch E, Martyn K. Food & mood: a review of supplementary prebiotic and probiotic interventions in the treatment of anxiety and depression in adults. BMJ Nutrition, Prevention & Health 2020; 3(2):351-362.

Rajoka MSR, Jin M, Haobin Z, Li Q, Shao D, Jiang C, Huang Q, Yang H, Shi J, Hussain N. Functional characterization and biotechnological potential of exopolysaccharide produced by Lactobacillus rhamnosus strains isolated from human breast milk. LWT 2018;89:638-647

National Research Council. Guide for the care and use of laboratory animals. National Academies Press 2010

Antoniuk S, Bijata M, Ponimaskin E, Wlodarczyk J. Chronic unpredictable mild stress for modeling depression in rodents: meta-analysis of model reliability. Neurosci Biobehav Rev. 2019; 99:101–116. Accessed using doi: 10.1016/j.neubiorev.2018.12.002

Akinluyi ET, Edem EE, Dakoru KM, Nnodim CJ, Oladipupo MA, Adeoluwa OA, Obisesan AO, Ben-Azu B, Adebayo OG. Psychobiotic interventions attenuate chronic alcohol use-mediated exacerbation of posttraumatic stress disorder in rats: the role of gut-liver axis response. J Complement Integr Med. 2022;20(1):92-105

Yang CR, Bai YY, Ruan CS, Zhou FH, Li F, Li CQ, Zhou XF. (2017). Injection of anti-proBDNF in Anterior Cingulate Cortex (ACC) reverses chronic stress-induced adverse mood behaviors in mice. Neurotox Res. 31: 298–308.

Nikolova YS, Misquitta KA, Rocco BR, Prevot TD, Knodt AR, Ellegood J, Voineskos AN, Lerch JP, Hariri AR, Sibille E, Banasr M. Shifting priorities: highly conserved behavioral and brain network adaptations to chronic stress across species. Transl. Psychiatry 2018; 8(1):1-13.

Kraeuter AK, Guest PC, Sarnyai Z. The open field test for measuring locomotor activity and anxiety-like behaviour. In: Guest PC (Eds) Pre-Clinical Models. Methods in Molecular Biology, vol 1916. Humana Press, New York, 2018.

Porsolt RD, Anton G, Blavet N, Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Euro J of Pharmacol. 1978;47(4):379-391

Steru L, Chermat, R., Thierry, B., Simon, P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl.) 1985;85:367–370.

Zhang X, Bearer EL, Perles-Barbacaru AT, Jacobs RE. Increased anatomical detail by in vitro MR microscopy with a modified Golgi impregnation method. Magnetic Resonance in Medicine 2010; 63(5):1391-1397

Weber K, Giannakopoulos P, Herrmann FR, Bartolomei J, Digiorgio S, Ortiz Chicherio N, Delaloye C, Ghisletta P, Lecerf T, De Ribaupierre A, Canuto A. Stressful life events and neuroticism as predictors of late-life versus early-life depression. Psychogeriatrics. 2013; 13(4):221–228.

MacQueen G, Frodl T. The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research? Mol Psychiatry. 2011; 16:252–264.

Qiao H, Li MX, Xu C, Chen HB, An SC, Ma XM. Dendritic spines in depression: what we learned from animal models. Neural Plast. 2016; 2016:8056370.

Chevalier G, Siopi E, Guenin-Mace L, Pascal M, Laval T, Rifflet A, Boneca IG, Demangel C, Colsch B, Pruvost A, Chu-Van E, Messager A, Leulier F, Lepousez G, Eberl G, Lledo PM. Effect of gut microbiota on depressive-like behaviors in mice is mediated by the endocannabinoid system. Nature Communications 2020; 11(1):1-15

Shehu A, Magaji MG, Yau J, Mahmud B, Ahmed A. Antidepressant effect of methanol stem bark extract of Adansonia digitata L. (Malvaceae) in mice. Trop J Nat Prod Res.2018;2(2):87-91

Akkasheh G, Kashani-Poor Z, Tajabadi-Ebrahimi M, Jafari P, Akbari H, Taghizadeh M, Memarzadeh MR, Asemi Z, Esmaillzadeh A. Clinical and metabolic response to probiotic administration in patients with major depressive disorder: A randomized, double-blind, placebo-controlled trial. Nutrition. 2016; 32(3):315-320.

Steenbergen L, Sellaro R, van Hemert S, Bosch JA, Colzato LS. A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood.Brain Behav Immun. 2015; 48:258-264.

Gacias M, Gaspari S, Santos PM, Tamburini S, Andrade M, Zhang F, Shen N, Tolstikov V, Kiebish MA, Dupree JL, Zachariou V, Clemente JC, Casaccia P. Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior. eLife 2016; 5:e13442.

Wang H, Lee IS, Braun C, Enck P. Effect of probiotics on central nervous system functions in animals and humans: a systematic review. J Neurogastroenterol. Motil. 2016; 22:589–605.

Kazemi A, Noorbala AA, Azam K, Eskandari MH, Djafarian K. Effect of probiotic and prebiotic vs placebo on psychological outcomes in patients with major depressive disorder: a randomized clinical trial. Clin. Nutr. 2018. Doi: 10.1016/j.clnu.2018.04.010 [Epub ahead of print].

Vermeulen E, Brouwer IA, Stronks K, Bandinelli S, Ferrucci L, Visser M, Nicolaou M. Inflammatory dietary patterns and depressive symptoms in Italian older adults. Brain Behav. Immunity 2018; 67:290–298.

Pfau ML, Menard C, Russo SJ. Inflammatory mediators in mood disorders: therapeutic opportunities. Annual Review of Pharmacology Toxicology. 2018; 58:411–428

Huang L, Lv X, Ze X, Ma Z, Zhang X, He R, Fan J, Zhang M, Sun B, Wang F, Liu H. Combined probiotics attenuate chronic unpredictable mild stress-induced depressive-like and anxiety-like behaviors in rats. Front. Psychiatry. 2022;13:990465. Downloaded using Doi:10.3389/fpsyt.2022.990465

Li N, Wang Q, Wang Y, Sun A, Lin Y, Jin Y and Li X. Oral Probiotics Ameliorate the Behavioral Deficits Induced by Chronic Mild Stress in Mice via the Gut MicrobiotaInflammation Axis. Front Behav Neurosci. 2018; 12:266.

Consonni A, Cordiglieri C, Rinaldi E, Marolda R, Ravanelli I, Guidesi E, Elli M, Mantegazza R, Baggi F. Administration of bifidobacterium and lactobacillus strains modulates experimental myasthenia gravis and experimental encephalomyelitis in Lewis rats. Oncotarget 2018; 9:22269–

Chong HX, Yusoff NAA, Hor YY, Lew LC, Jaafar MH, Choi SB, Yusoff MSB, Wahid N, Abdullah MFIL, Zakaria N, Ong KL, Park YH, Liong MT. Lactobacillus plantarum DR7 alleviates stress and anxiety in adults: a randomised, doubleblind, placebo-controlled study. Benef Microbes.2019; 10(4):355-373.

Gao L, CaiY, Wang H, Wang G, Zhang Q, Yan X. Probing prefrontal cortex hemodynamic alterations during facial emotion recognition for major depression disorder through functional near-infrared spectroscopy. J Neural Eng. 2019;16(2):026026

Campbell S, Marriott M, Nahmias C, MacQueen GM. Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am J Psychiatry 2004; 161(4):598-607.

Michael DR, Davies TS, Loxley KE, Allen MD, Good MA, Hughes TR, Plummer SF. In vitro neuroprotective activities of two distinct probiotic consortia. Benef. Microbes 2019; 10(4):437–447

Bonfili L, Cecarini V, Berardi S, Scarpona S, Suchodolski JS, Nasuti C, Fiorini D, Boarelli MC, Rossi G, Eleuteri AM. Microbiota modulation counteracts Alzheimer’s disease progression influencing neuronal proteolysis and gut hormones plasma levels. Sc. Rep. 2017; 7(1):2426.