Role of Probiotic Strain Lactobacillus acidophilus in the Reversal of Gut Dysbiosis Induced Brain Cognitive Decline

Authors

DOI:

https://doi.org/10.18006/2024.12(1).36.48

Keywords:

Learning, Memory, Pseudomonas aeruginosa, Bacillus subtilis, Escherichia coli, Lactobacillus acidophilus, Enterotoxin, Cognitive impairment

Abstract

In the central nervous system, bidirectional communication between the brain and gut results in memory formation due to synaptic plasticity changes. During a healthy state, oral balanced microflora plays a pivotal role in memory formation by inhibiting the enterotoxin level produced by infectious pathogens. In disease conditions, beneficial microbial dysbiosis may result in excess enterotoxin production. Further, excess enterotoxin secretion prevents beneficial bacteria's proliferation and impairs neurotransmitter precursor compounds' transport to the brain. Blockade of neurotransmitter precursor compounds may result in the development of memory loss. The present study stated the role of Lactobacillus acidophilus in recovering memory loss. Reversal of cognitive impairment is shown with the help of a three-step behavioural analysis, which consists of one pre-infusive behavioural analysis and two post-infusive behavioural analyses (phase 1 and 2). The pre-infusive analysis showed no cognitive impairment in an assimilated environment without any infusions. After oral microbial infusions, phase 1 of post-infusive behavioural analysis showed the presence of cognitive impairment in the experimental groups who received oral infusions. Formed cognitive impairment is reverted with the help of L. acidophilus oral infusion in phase 2 of post-infusive analysis. Comparative three-step behavioural analysis proved that Pseudomonas aeuroginosa induced cognitive impairment may revert to normal conditions with the help of L. acidophilus. The outcome of the present study proves that cognitive impairment developed due to poor oral hygiene can be treated with the help of probiotic microorganisms.

Author Biography

Murugan Mukilan, Department of Biotechnology, Sri Ramakrishna College of Arts & Science, Coimbatore 641 006, Tamil Nadu, India

Advanced Technology Development Centre, Indian Institute of Technology, Kharagpur 721 302, West Bengal, India

References

Abraham, W.C., Jones, O.D., & Glanzman, D.L. (2019). Is plasticity of synapses the mechanism of long-term memory storage? Npj Science of learning, 4, 9. DOI: https://doi.org/10.1038/s41539-019-0048-y

Angelucci, F., Cechova, K., Amlerova, J., & Hort, J. (2019). Antibiotics, gut microbiota, and Alzheimer's disease. Journal of Neuroinflammation, 16, 108. DOI: https://doi.org/10.1186/s12974-019-1494-4

Aponte, M., Murru, N., & Shoukat, M. (2020). Therapeutic, Prophylatic, and Functional Use of Probiotics: A Current Perspective. Frontiers in Microbiology, 11, 562048. DOI: https://doi.org/10.3389/fmicb.2020.562048

Asadpoor, M., Ithakisiou, G., Henricks, P.A., Pieters, R., et al. (2021). Non-Digestible Oligosaccharides and Short Chain Fatty Acids as Therapeutic Targets against Enterotoxin-Producing Bacteria and Their Toxins. Toxins, 13, 175. DOI: https://doi.org/10.3390/toxins13030175

Asl, Z.R., Sepehri, G., & Salami, M. (2019). Probiotic treatment improves the impaired spatial cognitive performance and restores synaptic plasticity in an animal model of alzheimer's disease. Behavioural Brain Research, 376, 112183. DOI: https://doi.org/10.1016/j.bbr.2019.112183

Bai, Y., & Suzuki, T. (2020). Activity-Dependent Synaptic Plasticity in Drosophila melanogaster. Frontiers in physiology, 11, 161. DOI: https://doi.org/10.3389/fphys.2020.00161

Bermúdez-Humarán, L.G., Salinas, E., Ortiz, G.G., Ramirez-Jirano, L.J., et al. (2019). From Probiotics to Psychobiotics: Live Beneficial Bacteria Which Act on the Brain-Gut Axis. Nutrients, 11, 890. DOI: https://doi.org/10.3390/nu11040890

Bisaz, R., Travaglia, A., & Alberini, C.M. (2014). The neurobiological bases of memory formation: from physiological conditions to psychopathology. Psychopathology, 47, 347-356. DOI: https://doi.org/10.1159/000363702

Chen, D., Yang, X., Yang, J., Lai, G., et al. (2017). Prebiotic effect of fructooligosaccharides from Morinda officinalis on alzheimer's disease in rodent models by targeting the microbiota-gut-brain axis. Frontiers in Aging Neuroscience, 9, 403. DOI: https://doi.org/10.3389/fnagi.2017.00403

Da, D., Zhao, Q., Zhang, H., Wu, W., et al. (2023). Oral microbiome in older adults with mild cognitive impairment. Journal of Oral Microbiology, 15, 2173544. DOI: https://doi.org/10.1080/20002297.2023.2173544

Dai, W., Liu, J., Qiu, Y., Teng, Z., et al. (2022). Gut Microbial Dysbiosis and Cognitive impairment in Bipolar Disorder: Current Evidence. Frontiers in Pharmacology, 13, 893567. DOI: https://doi.org/10.3389/fphar.2022.893567

Daliri, E.B., Tango, C.N., Lee, B.H., & Oh, D. (2018). Human microbiome restoration and safety. International Journal of Medical Microbiology, 30, 487-497. DOI: https://doi.org/10.1016/j.ijmm.2018.05.002

Evans, H.T., Blackmore, D., Götz, J., & Bodea, L. (2021). De novo proteomic methods for examining the molecular mechanisms underpinning long-term memory. Brain Research Bulletin, 169, 94-103. DOI: https://doi.org/10.1016/j.brainresbull.2020.12.015

Fung, T.C., Olson, C.A., & Hsiao, E.Y. (2017). Interactions between the microbiota, immune and nervous systems in health and disease. Nature Neuroscience, 20, 145-155. DOI: https://doi.org/10.1038/nn.4476

Ganesh, A., Bogdanowicz, W., Balamurugan, K., Marimuthu, G., & Rajan, K.E. (2012). Egr-1 antisense oligodeoxynucleotide administration into the olfactory bulb impairs olfactory learning in the greater short-nosed fruit bat Cynopterus sphinx. Brain Research, 1471, 33-45. DOI: https://doi.org/10.1016/j.brainres.2012.06.038

Ganesh, A., Bogdanowicz, W., Haupt, M., Marimuthu, G., & Rajan, K.E. (2010). Role of olfactory bulb serotonin in olfactory learning in the greater short-nosed fruit bat, Cynopterus sphinx (Chiroptera: Pteropodidae). Brain Research, 1352, 108-117. DOI: https://doi.org/10.1016/j.brainres.2010.06.058

García-Cabrerizo, R., Carbia, C., Ơriordan, K.J., Schellekens, H., & Cryan, J.F. (2021). Microbiota-gut-brain axis as a regulator of reward processes. Journal of Neurochemistry, 157, 1495-1524. DOI: https://doi.org/10.1111/jnc.15284

Gentile, C.L., & Weir, T.L. (2018). The gut microbiota at the intersection of diet and human health. Science, 362, 776-780. DOI: https://doi.org/10.1126/science.aau5812

Herman, J., McKlveen, J.M., Ghosal, S., Kopp, B., et al. (2016). Regulation of the Hypothalamic-Pituitary-Adrenocortical Stress Response. Comprehensive Physiology, 6, 603-621. DOI: https://doi.org/10.1002/cphy.c150015

Hillemacher, T., Bachmann, O., Kahl, K.G., & Frieling, H. (2018). Alcohol, microbiome, and their effect on psychiatric disorders. Progress in Neuropsychopharmacology and Biological Psychiatry, 85, 105-115. DOI: https://doi.org/10.1016/j.pnpbp.2018.04.015

Hinds, J.A., & Sanchez, E.R. (2022). The Role of the Hypothalamus-Pituitary-Adrenal (HPA) Axis in Test-Induced Anxiety: Assessments, Physiological Responses, and Molecular Details. Stresses, 2, 146-155. DOI: https://doi.org/10.3390/stresses2010011

Jemimah, S., Chabib, C.M.M., Hadjileontiadis, L., & Alshehhi, A. (2023). Gut microbiome dysbiosis in Alzheimer's disease and mild cognitive impairment: A systematic review and meta-analysis. PLOS ONE, 18, e0285346. DOI: https://doi.org/10.1371/journal.pone.0285346

Jiang, C., Li, G., Huang, P., Liu, Z., & Zhao, B. (2017). The gut microbiota and alzheimer's disease. Journal of Alzheimer's Disease, 58, 1-15. DOI: https://doi.org/10.3233/JAD-161141

Kaczmarek, J.L., Thompso, S.V., & Holscher, H.D. (2017). Complex interactions of circadian rhythms, eating behaviours, and the gastrointestinal microbiota and their potential impact on health. Nutrition Reviews, 75, 673-682. DOI: https://doi.org/10.1093/nutrit/nux036

Lin, H., Chen, C., deBelle, J.S., Tully, T., & Chiang, A. (2021). CREB A and CREB B in two identified neurons gate long-term memory formation in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 118, e2100624118. DOI: https://doi.org/10.1073/pnas.2100624118

Lotz, S.K., Blackhurst, B.M., Reagin, K.L., & Funk, K.E. (2021). Microbial Infections Are a Risk Factor for Neurodegenerative Diseases. Frontiers in Cellular Neuroscience, 15, 691136. DOI: https://doi.org/10.3389/fncel.2021.691136

Luca, C.D., Colangelo, A.M., Alberghina, L., & Papa, M. (2018). Neuro-Immune Hemostasis: Homeostasis and Diseases in the Central Nervous System. Frontiers in Cellular Neuroscience, 12, 459. DOI: https://doi.org/10.3389/fncel.2018.00459

Ma, J., Piao, X., Mahfuz, S., Long, S., & Wang, J. (2022). The interaction among gut microbes, the intestinal barrier and short chain fatty acids. Animal Nutrition, 9, 159-174. DOI: https://doi.org/10.1016/j.aninu.2021.09.012

Ma, Q., Xing, C., Long, W., Wang, H.Y., Liu, Q., & Wang, R. (2019). Impact of microbiota on central nervous system and neurological diseases: the gut-brain axis. Journal of Neuroinflammation, 16, 53. DOI: https://doi.org/10.1186/s12974-019-1434-3

Mazziotta, C., Tognon, M., Martini, F., Torreggiani, E. & Rotondo, J.C. (2023). Probiotics Mechanism of Action on Immune Cells and Beneficial Effects on Human Health. Cells, 12, 184. DOI: https://doi.org/10.3390/cells12010184

Mendez, M., Arias, N., Uceda, S., & Arias, J.L. (2015). c-Fos expression correlates with performance on novel object and novel place recognition tests. Brain Research Bulletin, 117, 16-23. DOI: https://doi.org/10.1016/j.brainresbull.2015.07.004

Miri, S., Yeo, J., Abubaker, S., Hammami, R. (2023). Neuromicrobiology, an emerging neurometabolic facet of the gut microbiome? Frontiers in Microbiology, 14, 1098412. DOI: https://doi.org/10.3389/fmicb.2023.1098412

Misiak, B., Łoniewski, I., Marlicz, W., Freydeca, W., et al. (2020). The HPA axis dysregulation in severe mental illness: can we shift the blame to gut microbiota. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 102, 109951. DOI: https://doi.org/10.1016/j.pnpbp.2020.109951

Morshedi, M., Saghafi-Asl, M., & Hosseinifard, E.S. (2020). The potential therapeutic effects of the gut microbiome manipulation by symbiotic containing-Lactobacillus plantarum on neuropsychological performance of diabetic rats. Journal of Translational Medicine, 18, 18. DOI: https://doi.org/10.1186/s12967-019-02169-y

Mukilan, M. (2022). Effect of Probiotics, Prebiotics and Synbiotic Supplementation on Cognitive Impairment: A Review. Journal of Experimental Biology and Agricultural Sciences, 10, 1-11. DOI: https://doi.org/10.18006/2022.10(1).1.11

Mukilan, M. (2023). Impact of Pseudomonas aeruginosa, Bacillus subtilis, Staphylococcus aureus, and Escherichia coli Oral Infusions on Cognitive Memory Decline in Mild Cognitive Impairment. Journal of Experimental Biology and Agricultural Sciences, 11, 581-592. DOI: https://doi.org/10.18006/2023.11(3).581.592

Mukilan, M., Bogdanowicz, W., Marimuthu, G., & Rajan, K.E. (2018a). Odour discrimination learning in the Indian greater short-nosed fruit bat (Cynopterus sphix): differential expression of Egr-1, C-fos and PP-1 in the olfactory bulb, amygdala and hippocampus. Journal of Experimental Biology, 221, jeb175364. DOI: https://doi.org/10.1242/jeb.175364

Mukilan, M., Rajathei, D.M., Jeyaraj, E., Kayalvizhi, N., & Rajan, K.E. (2018b). MiR-132 regulated olfactory bulb proteins linked to olfactory learning in greater short-nosed fruit bat Cynopterus sphinx. Gene, 671, 10-20. DOI: https://doi.org/10.1016/j.gene.2018.05.107

Mukilan, M., Varman, D.R., Sudhakar, S., & Rajan, K.E. (2015). Activity-dependent expression of miR-132 regulates immediate early gene induction during olfactory learning in the greater short-nosed fruit bat, Cynopterus sphinx. Neurobiology of Learning and Memory, 120, 41-51. DOI: https://doi.org/10.1016/j.nlm.2015.02.010

Myers Jr, M.G., Affinati, A.H., Richardson, N., & Schwartz, M.W. (2021). Central nervous system regulation of organismal energy and glucose homeostasis. Nature Metabolism, 3, 737-750. DOI: https://doi.org/10.1038/s42255-021-00408-5

Naomi, R., Embong, H., Othman, F., Ghazi, H.F., et al. (2022). Probiotics for Alzheimer's Disease: A Systematic Review. Nutrients, 14, 20. DOI: https://doi.org/10.3390/nu14010020

Ney, L., Wipplinger, M., Grossmann, M., Engert, N., et al. (2023). Short chain fatty acids: Key regulators of the local and systemic immune response in inflammatory diseases and infections. Open Biology, 13, 230014. DOI: https://doi.org/10.1098/rsob.230014

Ng, K.M., Pannu, S., Liu, S., Burckhardt, J.C., et al. (2023). Single-strain behavior predicts responses to environmental pH and osmolality in the gut microbiota. mBio, 14, e0075323. DOI: https://doi.org/10.1128/mbio.00753-23

O'Donnell, M.P., Fox, B.W., Chao, P., Schroeder, F.C., & Sengupta, P. (2020). A neurotransmitter produced by gut bacteria modulates host sensory behaviour. Nature, 583, 415-420. DOI: https://doi.org/10.1038/s41586-020-2395-5

Orr, M.E., Reveles, K.R., Yeh, C., Young, E.H., et al. (2020). Can oral health and oral-derived biospecimens predict progression of dementia? Oral Diseases, 26, 249-258. DOI: https://doi.org/10.1111/odi.13201

Ortega-Martínez S. (2015). A new perspective on the role of the CREB family of transcription factors in memory consolidation via adult hippocampal neurogenesis. Frontiers in Molecular Neuroscience, 8, 46. DOI: https://doi.org/10.3389/fnmol.2015.00046

Park, S., & Wu, X. (2022). Modulation of the Gut Microbiota in Memory Impairment and Alzhiemer's Disease via the Inhibition of the Parasympathetic Nervous System. International Journal of Molecular Sciences, 23, 13574. DOI: https://doi.org/10.3390/ijms232113574

Piatek, J., Krauss, H., Ciechelska-Rybarczyk, A., Bernatek, M., et al. (2020). In-Vitro Growth Inhibiion of Bacterial Pathogens by Probiotics and a Synbiotic: Product Composition Matters. International Journal of Environmental Research and Public Health, 17, 3332. DOI: https://doi.org/10.3390/ijerph17093332

Preethi, J., Singh, H.K., Charles, P.D., Charles, P.D., & Rajan, K.E. (2012). Participation of microRNA 124-CREB pathway: a parallel memory enhancing mechanism of standardized extract of Bacopa monniera (BESEB CDRI-08). Neurochemical Research, 37, 2167-2177. DOI: https://doi.org/10.1007/s11064-012-0840-z

Qian, X., Xie, R., Liu, X., Chen, S., & Tang, H. (2022). Mechanisms of Short-Chain Fatty Acids Derived from Gut Microbiota in Alzheimer's Disease. Aging and Disease, 13, 1252-1266. DOI: https://doi.org/10.14336/AD.2021.1215

Raheem, A., Liang, L., Zhang, G., & Cui, S. (2021). Modulatory Effects of Probiotics uring Pathogenic Infections With Emphasis on Immune Regulation. Frontiers in Immunology, 12, 616713. DOI: https://doi.org/10.3389/fimmu.2021.616713

Rajan, K.E., Ganesh, A., Dharaneedharan, S., & Radhakrishnan, K. (2011). Spatial learning-induced egr-1 expression in telencephalon of gold fish Carassius auratus. Fish Physiology and Biochemistry, 37, 153-159. DOI: https://doi.org/10.1007/s10695-010-9425-4

Salami, M. (2021). Interplay of Good Bacteria and Central Nervous System: Cognitive Aspects and Mechanistic Considerations. Frontiers in Neuroscience, 15, 613120. DOI: https://doi.org/10.3389/fnins.2021.613120

Sarkar, S.P., Mazumder, P.M., & Banerjee, S. (2020). Probiotics protect against gut dysbiosis associated decline in learning and memory. Journal of Neuroimmunology, 348, 577390. DOI: https://doi.org/10.1016/j.jneuroim.2020.577390

Savin, Z., Kivity, S., Yonath, H., & Yehuda, S. (2018). Smoking and the intestinal microbiome. Archives of Microbiology, 200, 677-684. DOI: https://doi.org/10.1007/s00203-018-1506-2

Sen, T., Gupta, R., Kaiser, H., & Sen, N. (2017). Activation of PERK Elicits Memory Impairment through Inactiation of CREB and Downregulation of PSD95 After Traumatic Brain Injury. The Journal of Neuroscience, 37, 5900-5911. DOI: https://doi.org/10.1523/JNEUROSCI.2343-16.2017

Shandilya, S., Kumar, S., Jha, N.J., Kesari, K.K., & Ruokolainen, J. (2022). Interplay of gut microbiota and oxidative stress: Prespective on neurodegeneration and neuroprotection. Journal of Advanced Research, 38, 223-244. DOI: https://doi.org/10.1016/j.jare.2021.09.005

Sheng, J.A., Bales, N.J., Myers, S.A., Bautista, A.I., et al. (2021). The Hypothalamic-Pituitary-Adrenal Axis: Development, Programming Actions of Hormones, and Maternal-Fetal Interactions. Frontiers in Behavioral Neuroscience, 14, 601939. DOI: https://doi.org/10.3389/fnbeh.2020.601939

Strandwitz, P. (2018). Neurotransmitter modulation by the gut microbiota. Brain Research, 1693, 128-133. DOI: https://doi.org/10.1016/j.brainres.2018.03.015

Thangaleela, S., Shanmugapriya, S., Mukilan, M., Radhakrishnan, K., & Rajan, K.E. (2018). Alterations in MicroRNA-132/212 Expression Impairs Fear Memory in Goldfish Carassius auratus. Annals of Neurosciences, 25, 90-97. DOI: https://doi.org/10.1159/000486842

Wong, C.B., Kobayashi, Y., & Xiao, J. (2018). Probiotics for preventing cognitive impairment in alzheimer's disease. In A. Evrensel, & B.O. Ünsalver, (eds), Gut Microbiota, IntechOpen.

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2024-03-15

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Mukilan, M., Antony Mathew, M. T., Yaswanth, S., & Mallikarjun, V. (2024). Role of Probiotic Strain Lactobacillus acidophilus in the Reversal of Gut Dysbiosis Induced Brain Cognitive Decline. Journal of Experimental Biology and Agricultural Sciences, 12(1), 36–48. https://doi.org/10.18006/2024.12(1).36.48

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