Lactobacillus fermentum NS9 restores the antibiotic induced physiological and psychological abnormalities in rats
Abstract
Gut microbiota play a vital role in maintaining the health of the host. Many factors affect gut microbiota; application of broad range antibiotics disturb microbiota, while probiotic application protects the microbiota. To investigate how probiotics alter the physiological and psychological changes induced by antibiotics, we tested the performance of ampicillin-treated rats in the presence or absence of Lactobacillus fermentum strain NS9, in elevated plus maze and Morris water maze. The results showed that NS9 normalised the composition of gut microbiota and alleviated the ampicillin-induced inflammation in the colon. The levels of the mineralocorticoid and N-methyl-D-aspartate receptors were also elevated in the hippocampus of the ampillicin+NS9 treated group. NS9 administration also reduced the anxiety-like behaviour and alleviated the ampicillin-induced impairment in memory retention. These findings suggest that NS9 is beneficial to the host, because it restores the physiological and psychological abnormalities induced by ampicillin. Our results highlight how gut contents regulate the brain, and shed light on the clinical applications of probiotics to treat the side effect of antibiotics and mental disorders.
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Expression of NMDAR and BDNF is significantly reduced in GF mice.
“In addition, expression of NMDAR and BDNF is significantly reduced in GF mice [572, 581, 582]”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [582]
Dysbiosis in weaned rats leads to impaired spatial memory and reduced NMDAR and BDNF levels in the brain.
“Dysbiosis in weaned rats leads to impaired spatial memory and reduced NMDAR and BDNF levels in the brain [582, 583].”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [582]
Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
Cryan, J. F., & Dinan, T. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3346 · Cited by 4,572 · see citing works
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888 · see citing works
Gut Microbiota from Twins Discordant for Obesity Modulate Metabolism in Mice
Ridaura, V. K., Faith, J. J., Rey, F. E., Cheng, J., Duncan, A. E., Kau, A. L., Griffin, N. W., Lombard, V., Henrissat, B., Bain, J. R., et al. (2013) · Science · doi:10.1126/science.1241214 · Cited by 3,788 · see citing works
Normal gut microbiota modulates brain development and behavior
Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010529108 · Cited by 3,228 · see citing works
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., & Koga, Y. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063388 · Cited by 2,735 · see citing works
Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation
REUL, J. M. H. M., & KLOET, E. R. D. (1985) · Endocrinology · doi:10.1210/endo-117-6-2505 · Cited by 2,580 · see citing works
The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory.
Tsien, J. Z., Huerta, P. T., & Tonegawa, S. (1996) · Cell · doi:10.1016/s0092-8674(00)81827-9 · Cited by 1,782 · cited 1× · see citing works
“These findings are consistent with data generated by genetically blocking the NMDA receptor in the hippocampus dentate gyrus CA1 measured by radial maze (Niewoehner et al., 2007; Tsien et al., 1986).”
ResultBercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748 · see citing works
Antibiotics in early life alter the murine colonic microbiome and adiposity
Cho, I., Yamanishi, S., Cox, L., Methé, B. A., Zavadil, J., Li, K., Gao, Z., Mahana, D., Raju, K., Teitler, I., et al. (2012) · Nature · doi:10.1038/nature11400 · Cited by 1,613 · see citing works
The interplay between the intestinal microbiota and the brain
Collins, S. M., Surette, M., & Bercik, P. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2876 · Cited by 1,611 · cited 2× · see citing works
“Recent studies have suggested that the gut microbiota could affect the behaviour of hosts and implicated their involvement in depression, anxiety-like behaviours, and in modulating the hypothalamic-pituitaryadrenal axis (HPA-axis) (Barouei et al., 2012; Collins et al., 2012; Cryan and Dinan, 2012; Tillisch et al., 201…”
Messaoudi, M., Lalonde, R., Violle, N., Javelot, H., Desor, D., Nejdi, A., Bisson, J.-F., Rougeot, C., Pichelin, M., Cazaubiel, M., et al. (2011) · British Journal of Nutrition · doi:10.1017/s0007114510004319 · Cited by 1,324 · see citing works
Consumption of fermented milk product with probiotic modulates brain activity
Tillisch, K., Labus, J., Kilpatrick, L., Jiang, Z., Stains, J., Ebrat, B., Guyonnet, D., Legrain–Raspaud, S., Trotin, B., Naliboff, B., et al. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.02.043 · Cited by 1,192 · see citing works
Long-term impacts of antibiotic exposure on the human intestinal microbiota
Jernberg, C., Löfmark, S., Edlund, C., & Jansson, J. K. (2010) · Microbiology · doi:10.1099/mic.0.040618-0 · Cited by 1,067 · see citing works
Bercik, P., Park, A. J., Sinclair, D., Khoshdel, A., Lu, J., Huang, X., Deng, Y., Blennerhassett, P. A., Fahnestock, M., Moine, D., et al. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2011.01796.x · Cited by 1,018 · see citing works
Desbonnet, L., Garrett, L., Clarke, G., Bienenstock, J., & Dinan, T. G. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2008.03.009 · Cited by 952 · see citing works
Bacterial infection causes stress-induced memory dysfunction in mice
Gareau, M. G., Wine, E., Rodrigues, D. M., Cho, J. H., Whary, M. T., Philpott, D. J., MacQueen, G., & Sherman, P. M. (2011) · Gut · doi:10.1136/gut.2009.202515 · Cited by 909 · cited 6× · see citing works
“However, in the present study, NS9 administration elevated the NMDA receptor expression, but not the BDNF level, which is not consistent with previous reports (Gareau et al., 2011).”
BackgroundMethodResultInfluentialBercik, P., Verdu, E. F., Foster, J. A., Macri, J., Potter, M., Huang, X., Malinowski, P., Jackson, W., Blennerhassett, P., Neufeld, K. A., et al. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.06.063 · Cited by 674 · see citing works
Gut microbiota disturbance during antibiotic therapy: a multi-omic approach
Pérez‐Cobas, A. E., Gosalbes, M. J., Friedrichs, A. K., Knecht, H., Artacho, A., Eismann, K., Otto, W., Rojo, D., Bargiela, R., von Bergen�, M., et al. (2012) · Gut · doi:10.1136/gutjnl-2012-303184 · Cited by 603 · see citing works
Guo, X., Xia, X., Tang, R., Zhou, J., Zhao, H., & Wang, K. (2008) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2008.02408.x · Cited by 502 · see citing works
Antibiotic use and inflammatory bowel diseases in childhood
Hviid, A. P., Svanström, H., & Frisch, M. (2010) · Gut · doi:10.1136/gut.2010.219683 · Cited by 492 · see citing works
Kalinichev, M., Easterling, K. W., Plotsky, P. M., & Holtzman, S. G. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00781-5 · Cited by 484 · see citing works
Sekirov, I., Tam, N. M., Jogova, M., Robertson, M. L., Li, Y., Lupp, C., & Finlay, B. B. (2008) · Infection and Immunity · doi:10.1128/iai.00319-08 · Cited by 483 · see citing works
Gareau, M. G., Jury, J., MacQueen, G., Sherman, P. M., & Perdue, M. H. (2007) · Gut · doi:10.1136/gut.2006.117176 · Cited by 472 · see citing works
Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy
Mitra, R., & Sapolsky, R. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705615105 · Cited by 409 · see citing works
Microbiota, Disease, and Back to Health: A Metastable Journey
Blumberg, R. S., & Powrie, F. M. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3004184 · Cited by 279 · see citing works
Loss of the limbic mineralocorticoid receptor impairs behavioral plasticity
Berger, S., Wolfer, D. P., Selbach, O., Alter, H., Erdmann, G., Reichardt, H. M., Chepkova, A. N., Welzl, H., Haas, H. L., Lipp, H.-P., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503878102 · Cited by 272 · see citing works
Li, W., Dowd, S. E., Scurlock, B., Acosta-Martinez, V., & Lyte, M. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.12.004 · Cited by 246 · see citing works
Self-citationGABA Potency at GABAA Receptors Found in Synaptic and Extrasynaptic Zones
Mortensen, M., Patel, B., & Smart, T. G. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00001 · Cited by 244 · see citing works
Axling, U., Olsson, C., Xu, J., Fernandez, C., Larsson, S. M., Ström, K., Ahrné, S., Holm, C., Molin, G., & Berger, K. (2012) · Nutrition & Metabolism · doi:10.1186/1743-7075-9-105 · Cited by 228 · see citing works
Visceral hyperalgesia and intestinal dysmotility in a mouse model of postinfective gut dysfunction
Berčík, P., Wang, L., Verdu, E. F., Mao, Y., Blennerhassett, P. A., Khan, W. I., Kean, I. R. L., Tougas, G. H., & Collins, S. M. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.04.006 · Cited by 218 · see citing works
Self-citationNiewoehner, B., Single, F. N., Hvalby, Ø., Jensen, V., Borgloh, S. M. Z. A., SEEBURG, P. H., Rawlins, J. N. P., Sprengel, R., & Bannerman, D. M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05312.x · Cited by 209 · see citing works
Recommendations for Probiotic Use—2011 Update
Floch, M. H., Walker, W. A., Madsen, K. L., Sanders, M. E., Macfarlane, G. T., Flint, H. J., Dieleman, L. A., Ringel, Y., Guandalini, S., Kelly, C. P., et al. (2011) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e318230928b · Cited by 207 · see citing works
NMDA receptor antagonists sustain LTP and spatial memory: active processes mediate LTP decay
Villarreal, D. M., Do, V., Haddad, E., & Derrick, B. E. (2001) · Nature Neuroscience · doi:10.1038/nn776 · Cited by 190 · see citing works
Yau, J. L. W., Olsson, T., Morris, R., Meaney, M. J., & Seckl, J. R. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00612-9 · Cited by 176 · see citing works
Gass, P., Kretz, O., Wolfer, D. P., Berger, S., Tronche, F., Reichardt, H. M., Kellendonk, C., Lipp, H., Schmid, W., & Schütz, G. (2000) · EMBO Reports · doi:10.1093/embo-reports/kvd088 · Cited by 159 · see citing works
Dai, C., Zheng, C., Meng, F., Zhou, Z., Sang, L.-X., & Jiang, M. (2012) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-012-1488-3 · Cited by 156 · see citing works
Lai, M., Horsburgh, K. J., Bae, S., Carter, R. N., Stenvers, D. J., Fowler, J. H., Yau, J. L. W., Gómez-Sánchez, C. E., Holmes, M. C., Kenyon, C. J., et al. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05427.x · Cited by 147 · see citing works
Boughton-Smith, N. K., Wallace, J. L., & Whitle, B. J. R. (1988) · Inflammation Research · doi:10.1007/bf01969102 · Cited by 112 · see citing works
Lönnermark, E., Friman, V., Lappas, G., Sandberg, T., Berggren, A., & Adlerberth, I. (2010) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e3181b2683f · Cited by 110 · see citing works
Kallen, V., Tulen, J. H. M., Utens, E. M. W. J., Treffers, P. D. A., de Jong, F. H., & Ferdinand, R. F. (2007) · Depression and Anxiety · doi:10.1002/da.20287 · Cited by 101 · see citing works
Barouei, J., Moussavi, M., & Hodgson, D. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046051 · Cited by 99 · see citing works
Recommendations for Probiotic Use
Floch, M. H., Madsen, K., Jenkins, D. J. A., Guandalini, S., Katz, J. A., Onderdonk, A. B., Walker, W. A., Fedorak, R. N., & Camilleri, M. (2006) · Journal of Clinical Gastroenterology · doi:10.1097/00004836-200603000-00022 · Cited by 88 · see citing works
Lyra, A., Krogius-Kurikka, L., Nikkilä, J., Malinen, E., Kajander, K., Kurikka, K., Korpela, R., & Palva, A. (2010) · BMC Gastroenterology · doi:10.1186/1471-230x-10-110 · Cited by 86 · see citing works
Continuous blockade of brain mineralocorticoid receptors impairs spatial learning in rats
Yau, J. L. W., Noble, J., & Seckl, J. R. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00858-7 · Cited by 71 · see citing works
Brinks, V., van der Mark, M. H., de Kloet, E. R., & Oitzl, M. S. (2007) · Neural Plasticity · doi:10.1155/2007/90163 · Cited by 70 · see citing works
Antibiotic associated diarrhea in children.
Alam, S., & Mushtaq, M. (2009) · PubMed · Cited by 67 · see citing works
Fu, C. J., Carter, J. N., Li, Y., Porter, J. H., & Kerley, M. S. (2006) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2006.01893.x · Cited by 67 · see citing works
Effects of NS lactobacillus strains on lipid metabolism of rats fed a high-cholesterol diet
Hu, X., Wang, T., Li, W., Jin, F., & Wang, L. (2013) · Lipids in Health and Disease · doi:10.1186/1476-511x-12-67 · Cited by 66 · see citing works
Self-citationSteroid modulation of hippocampal plasticity: switching between cognitive and emotional memories
Maggio, N., & Segal, M. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00012 · Cited by 60 · see citing works
Vasselli, J. R., & Sclafani, A. J. (1979) · Physiology & Behavior · doi:10.1016/0031-9384(79)90056-8 · Cited by 55 · see citing works
Role of the Brain-Gut Axis in the Pathophysiology of Crohn’s Disease
Stasi, C., & Orlandelli, E. (2008) · Digestive Diseases · doi:10.1159/000116774 · Cited by 54 · see citing works
Sharma, A. N., Pise, A., Sharma, J. N., & Shukla, P. (2014) · Metabolic Brain Disease · doi:10.1007/s11011-014-9627-z · Cited by 50 · see citing works
Anseloni, V. C. Z., Coimbra, N. C., Morato, S., & Brandão, M. L. (1999) · Experimental Brain Research · doi:10.1007/s002210050896 · Cited by 50 · see citing works
Influence of a probiotic lactobacillus strain on the intestinal ecosystem in a stress model mouse
Palomar, M. M., Galdeano, C. M., & Perdigón, G. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.08.015 · Cited by 46 · see citing works
Frisch, C., Kudin, A. P., Elger, C. E., Kunz, W. S., & Helmstaedter, C. (2006) · Epilepsy Research · doi:10.1016/j.eplepsyres.2006.10.001 · Cited by 46 · see citing works
Holsboer, F., Steiger, A., & Maier, W. (1983) · PubMed · Cited by 45 · see citing works
Oprica, M., Zhu, S., Goiny, M., Pham, T. M., Mohammed, A. H. S., Winblad, B. G., Bartfai, T., & Schultzberg, M. (2004) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2004.07.006 · Cited by 32 · see citing works
Nutten, S., Schumann, A., Donnicola, D., Mercenier, A., Rami, S., & García‐Ródenas, C. L. (2006) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00055-06 · Cited by 20 · see citing works
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Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
Interactions between the microbiota, immune and nervous systems in health and disease
Fung, T. C., Olson, C. A., & Hsiao, E. Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4476 · Cited by 1,900 · see citing works
Stress & the gut-brain axis: Regulation by the microbiome
Foster, J. A., Rinaman, L., & Cryan, J. F. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.03.001 · Cited by 1,150 · see citing works
Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease
Guo, T., Zhang, D., Zeng, Y., Huang, T. Y., Xu, H., & Zhao, Y. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00391-7 · Cited by 994 · see citing works
The Gut Microbiota and Alzheimer’s Disease
Jiang, C., Li, G., Huang, P., Liu, Z., & Zhao, B. (2017) · Journal of Alzheimer's Disease · doi:10.3233/jad-161141 · Cited by 852 · see citing works
The microbiome and host behavior
Vuong, H. E., Yano, J. M., Fung, T. C., & Hsiao, E. Y. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031347 · Cited by 537 · see citing works
Gut microbiota and the neuroendocrine system
Farzi, A., Fröhlich, E. E., & Holzer, P. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0600-5 · Cited by 478 · see citing works
Inflammation: the link between comorbidities, genetics, and Alzheimer’s disease
Newcombe, E. A., Camats-Perna, J., Silva, M. L., Valmas, N., Huat, T. J., & Medeiros, R. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1313-3 · Cited by 532 · see citing works
Antibiotics, gut microbiota, and Alzheimer’s disease
Angelucci, F., Cechova, K., Amlerova, J., & Hort, J. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1494-4 · Cited by 454 · see citing works
Leclercq, S., Mian, F. M., Stanisz, A. M., Bindels, L. B., Cambier, E., Ben-Amram, H., Koren, O., Forsythe, P., & Bienenstock, J. (2017) · Nature Communications · doi:10.1038/ncomms15062 · Cited by 434 · see citing works
The progress of gut microbiome research related to brain disorders
Zhu, S., Jiang, Y., Xu, K., Cui, M., Ye, W., Zhao, G., Jin, L., & Chen, X. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-1705-z · Cited by 419 · see citing works
Limbu, S. M., Zhou, L., Sun, S.-X., Zhang, M.-L., & Du, Z.-Y. (2018) · Environment International · doi:10.1016/j.envint.2018.03.034 · Cited by 384 · see citing works
Recognizing Depression from the Microbiota–Gut–Brain Axis
Liang, S., Wu, X., Hu, X., Wang, T., & Jin, F. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19061592 · Cited by 387 · see citing works
Self-citationKanmani, S., & Koo, B. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207551 · Cited by 381 · see citing works
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Hu, X., Wang, T., & Jin, F. (2016) · Science China Life Sciences · doi:10.1007/s11427-016-5083-9 · Cited by 371 · see citing works
Self-citationThe impact of the microbiota-gut-brain axis on Alzheimer’s disease pathophysiology
Doifode, T., Giridharan, V. V., Generoso, J. S., Bhatti, G., Collodel, A., Schulz, P. E., Forlenza, O. V., & Barichello, T. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2020.105314 · Cited by 347 · see citing works
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Wang, H., Lee, I.-S., Braun, C., & Enck, P. (2016) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16018 · Cited by 334 · see citing works
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Megur, A., Baltriukienė, D., Bukelskienė, V., & Burokas, A. (2020) · Nutrients · doi:10.3390/nu13010037 · Cited by 323 · see citing works
Gut microbiota in neurodegenerative disorders
Sarkar, S. R., & Banerjee, S. (2019) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2019.01.004 · Cited by 319 · see citing works
Sherwin, E., Sandhu, K. V., Dinan, T. G., & Cryan, J. F. (2016) · CNS Drugs · doi:10.1007/s40263-016-0370-3 · Cited by 297 · see citing works
Gut-Brain Psychology: Rethinking Psychology From the Microbiota–Gut–Brain Axis
Liang, S., Wu, X., & Jin, F. (2018) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2018.00033 · Cited by 269 · see citing works
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Ling, Z., Zhu, M., Yan, X., Cheng, Y., Shao, L., Liu, X., Jiang, R., & Wu, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.634069 · Cited by 245 · see citing works
Liu, Q., Xi, Y., Wang, Q., Liu, J., Li, P., Meng, X., Liu, K., Chen, W., Liu, X., & Liu, Z. (2021) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2021.04.005 · Cited by 241 · see citing works
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Sarkar, A., Harty, S., Lehto, S. M., Moeller, A. H., Dinan, T. G., Dunbar, R., Cryan, J. F., & Burnet, P. W. J. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.04.006 · Cited by 231 · see citing works
Cytotoxicity of Nanoparticles Contained in Food on Intestinal Cells and the Gut Microbiota
Fröhlich, E. E., & Fröhlich, E. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17040509 · Cited by 224 · see citing works
Gut microbiota in patients with Alzheimer’s disease spectrum: a systematic review and meta-analysis
Hung, C.-C., Chang, C., Huang, C.-W., Nouchi, R., & Cheng, C. (2022) · Aging · doi:10.18632/aging.203826 · Cited by 217 · see citing works
The links between the gut microbiome, aging, modern lifestyle and Alzheimer's disease
Askarova, S., Umbayev, B., Masoud, A.-R., Kaiyrlykyzy, A., Safarova, Y., Tsoy, A., Olzhayev, F., & Kushugulova, A. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00104 · Cited by 208 · see citing works
The role of probiotics and prebiotics in modulating of the gut-brain axis
Ansari, F., Neshat, M., Pourjafar, H., Jafari, S. M., Samakkhah, S. A., & Mirzakhani, E. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1173660 · Cited by 219 · see citing works
Liu, C., Tan, L., Zhang, L., Tian, W., & Ma, L. (2021) · Frontiers in Environmental Science · doi:10.3389/fenvs.2021.692298 · Cited by 183 · see citing works
Cowan, C. S. M., Dinan, T. G., & Cryan, J. F. (2020) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13156 · Cited by 176 · see citing works
The microbiota, immunoregulation, and mental health: implications for public health
Lowry, C. A., Smith, D. G., Siebler, P. H., Schmidt, D., Stamper, C. E., Hassell, J. E., Yamashita, P. S., Fox, J. H., Reber, S. O., Brenner, L. A., et al. (2016) · Current Environmental Health Reports · doi:10.1007/s40572-016-0100-5 · Cited by 172 · see citing works
Gut microbiota and pro/prebiotics in Alzheimer’s disease
Pluta, R. M., Ułamek-Kozioł, M., Januszewski, S., & Czuczwar, S. J. (2020) · Aging · doi:10.18632/aging.102930 · Cited by 171 · see citing works
Tochitani, S., Ikeno, T., Ito, T., Sakurai, A., Yamauchi, T., & Matsuzaki, H. (2016) · PLOS ONE · doi:10.1371/journal.pone.0138293 · Cited by 157 · see citing works
Impact of Environmental Pollutants on Gut Microbiome and Mental Health via the Gut–Brain Axis
Singh, S., Sharma, P., Pal, N., Kumawat, M., Shubham, S., Sarma, D. K., Tiwari, R. R., Kumar, M., & Nagpal, R. (2022) · Microorganisms · doi:10.3390/microorganisms10071457 · Cited by 157 · see citing works
Kim, H. S., Kim, S., Shin, S. J., Park, Y. H., Nam, Y., Lee, K. W., Lee, K. W., Kim, S., Yang, H. D., Yang, H. D., et al. (2021) · Translational Neurodegeneration · doi:10.1186/s40035-021-00273-y · Cited by 161 · see citing works
Park, J. Y., Choi, J., Lee, Y., Lee, J.-E., Lee, E. H., Kwon, H.-J., Yang, J., Jeong, B.-R., Kim, Y., & Han, P. (2017) · Experimental Neurobiology · doi:10.5607/en.2017.26.6.369 · Cited by 148 · see citing works
Relevance of gutmicrobiota in cognition, behaviour and Alzheimer’s disease
de J.R. De-Paula, V., Forlenza, A. S., & Forlenza, O. V. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.07.007 · Cited by 145 · see citing works
The Relationship Between the Gut Microbiome and Neurodegenerative Diseases
Zhu, X., Li, B., Lou, P., Dai, T., Chen, Y., Zhuge, A., Yuan, Y., & Li, L. (2021) · Neuroscience Bulletin · doi:10.1007/s12264-021-00730-8 · Cited by 134 · see citing works
Reis, D. J., Ilardi, S. S., & Punt, S. E. W. (2018) · PLOS ONE · doi:10.1371/journal.pone.0199041 · Cited by 123 · see citing works
Zhou, Y., Wang, Y., Quan, M., Zhao, H., & Jia, J. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-201497 · Cited by 123 · see citing works
Microbiota modulation as preventative and therapeutic approach in Alzheimer’s disease
Bonfili, L., Cecarini, V., Gogoi, O., Gong, C., Cuccioloni, M., Angeletti, M., Rossi, G., & Eleuteri, A. M. (2020) · FEBS Journal · doi:10.1111/febs.15571 · Cited by 118 · see citing works
The gut microbiota — brain axis of insects
Liberti, J., & Engel, P. (2020) · Current Opinion in Insect Science · doi:10.1016/j.cois.2020.01.004 · Cited by 104 · see citing works
Tian, P., Zou, R., Song, L., Zhang, X., Jiang, B., Wang, G., Lee, Y. K., Zhao, J., Zhang, H., & Chen, W. (2019) · Food & Function · doi:10.1039/c9fo01630a · Cited by 103 · see citing works
O’Hagan, C., Li, J. V., Marchesi, J. R., Plummer, S. F., Garaiová, I., & Good, M. A. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.05.015 · Cited by 97 · see citing works
Borrego-Ruiz, A., & Borrego, J. J. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110861 · Cited by 106 · see citing works
The microbiome of the built environment and mental health
Hoisington, A. J., Brenner, L. A., Kinney, K. A., Postolache, T. T., & Lowry, C. A. (2015) · Microbiome · doi:10.1186/s40168-015-0127-0 · Cited by 91 · see citing works
Xie, Z., Lu, H., Yang, S., Zeng, Y., Li, W., Wang, L., Luo, G., Fang, F., Zeng, T., & Cheng, W. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.568423 · Cited by 90 · see citing works
Self-citationHuman Gut Microbiota in Health and Alzheimer’s Disease
Szablewski, L. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-170908 · Cited by 92 · see citing works
The gut microbiome and Alzheimer’s disease: Complex and bidirectional interactions
Tarawneh, R. M., & Penhos, E. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104814 · Cited by 89 · see citing works
Accelerated Amyloid Beta Pathogenesis by Bacterial Amyloid FapC
Javed, I., Zhang, Z., Adamčík, J., Andrikopoulos, N., Li, Y., Otzen, D. E., Lin, S., Mezzenga, R., Davis, T. P., Ding, F., et al. (2020) · Advanced Science · doi:10.1002/advs.202001299 · Cited by 82 · see citing works
Su, A., Yang, W., Zhao, L., Pei, F., Yuan, B., Zhong, L., Ma, G., & Hu, Q. (2018) · Food & Function · doi:10.1039/c7fo01991b · Cited by 80 · see citing works
Li, Y., Shao, L., Mou, Y., Zhang, Y., & Ping, Y. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1957407 · Cited by 81 · see citing works
Kuijer, E. J., & Steenbergen, L. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105296 · Cited by 71 · see citing works
Antibiotics and the nervous system: More than just the microbes?
Champagne-Jorgensen, K., Kunze, W. A., Forsythe, P., Bienenstock, J., & McVey Neufeld, K.-A. (2019) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.12.014 · Cited by 92 · see citing works
Yang, S., Qiao, J., Zhang, M., Kwok, L., Matijašić, B. B., Zhang, H., & Zhang, W. (2024) · Journal of Advanced Research · doi:10.1016/j.jare.2024.06.006 · Cited by 72 · see citing works
Salami, M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.613120 · Cited by 67 · see citing works
Liu, J., Yu, C., Li, R., Liu, K., Jin, G., Ge, R., Tang, F., & Cui, S. (2020) · Food & Function · doi:10.1039/c9fo03007g · Cited by 65 · see citing works
Gut Microbiota Regulation and Their Implication in the Development of Neurodegenerative Disease
Sun, P., Su, L., Zhu, H., Li, X., Guo, Y., Du, X., Zhang, L., & Qin, C. (2021) · Microorganisms · doi:10.3390/microorganisms9112281 · Cited by 66 · see citing works
Disrupted Neurogenesis in Germ-Free Mice: Effects of Age and Sex
Scott, G. A., Terstege, D. J., Vu, A. P., Law, S., Evans, A., & Epp, J. R. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00407 · Cited by 64 · see citing works
Lyte, M., Chapel, A., Lyte, J. M., Ai, Y., Proctor, A., Jane, J.-L., & Phillips, G. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0146406 · Cited by 62 · see citing works
Dietary Regulation of Gut-Brain Axis in Alzheimer’s Disease: Importance of Microbiota Metabolites
Frausto, D. M., Forsyth, C. B., Keshavarzian, A., & Voigt, R. M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.736814 · Cited by 61 · see citing works
The microbiome and disorders of the central nervous system
Felice, V. D., & O'Mahony, S. M. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.016 · Cited by 60 · see citing works
Exploring the microbiota-gut-brain axis: impact on brain structure and function
Yassin, L. K., Nakhal, M. M., Alderei, A., Almehairbi, A., Mydeen, A. B., Akour, A. A., & Hamad, M. I. K. (2025) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2025.1504065 · Cited by 60 · see citing works
Immunoregulatory effect of mast cells influenced by microbes in neurodegenerative diseases
Girolamo, F., Coppola, C., & Ribatti, D. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.06.017 · Cited by 60 · see citing works
Zhao, Z., Wang, B., Mu, L., Wang, H., Luo, J., Yang, Y., Yang, H., Li, M., Zhou, L., & Tao, C. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00258 · Cited by 57 · see citing works
Ross, K. (2023) · EXPLORE · doi:10.1016/j.explore.2023.02.007 · Cited by 59 · see citing works
Target Dysbiosis of Gut Microbes as a Future Therapeutic Manipulation in Alzheimer’s Disease
Zhu, F., Li, C., Chu, F., Tian, X., & Zhu, J. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.544235 · Cited by 58 · see citing works
Aguayo, S. D., Schuh, C. M. A. P., Vicente, B., & Aguayo, L. G. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-180319 · Cited by 59 · see citing works
Liu, S., Gao, J., Liu, K., & Zhang, H. (2021) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2021.111560 · Cited by 58 · see citing works
Gut microbiota modulates stress-induced hypertension through the HPA axis
Wu, Q. J., Xu, Z., Song, S., Zhang, H., Zhang, W., Liu, L., Chen, Y., & Sun, J. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.05.014 · Cited by 56 · see citing works
Rahmati, H., Momenabadi, S., Vafaei, A. A., Bandegi, A. R., Mazaheri, Z., & Vakili, A. (2019) · Molecular Biology Reports · doi:10.1007/s11033-019-04949-7 · Cited by 55 · see citing works
Enduring neurobehavioral effects induced by microbiota depletion during the adolescent period
Lach, G., Fülling, C., Bastiaanssen, T. F. S., Fouhy, F., Donovan, A. N. O., Ventura‐Silva, A. P., Stanton, C., Dinan, T. G., & Cryan, J. F. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-01073-0 · Cited by 55 · see citing works
do Nascimento, L. C. P., Lacerda, D. C., Ferreira, D. J. S., de Souza, E. L., & Alves, J. L. D. B. (2022) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-022-09943-3 · Cited by 51 · see citing works
Effects of gut microbiota on neurodegenerative diseases
Khatoon, S., Kalam, N., Rashid, S., & Bano, G. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1145241 · Cited by 51 · see citing works
The Microbiome and Mental Health: Looking Back, Moving Forward with Lessons from Allergic Diseases
Logan, A. C., Jacka, F. N., Craig, J. M., & Prescott, S. L. (2016) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2016.14.2.131 · Cited by 51 · see citing works
Lebovitz, Y., Kowalski, E., Wang, X., Kelly, C., Lee, M., McDonald, V., Ward, R., Creasey, M., Mills, W. A., Basso, E. K. G., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.07.025 · Cited by 53 · see citing works
Rode, J., Edebol Carlman, H. M. T., König, J., Hutchinson, A. N., Thunberg, P., Persson, J., & Brummer, R. J. (2022) · Cells · doi:10.3390/cells11182922 · Cited by 50 · see citing works
The chemistry of gut microbiome in health and diseases
Lau, A., Tan, L. T., Mutalib, N. A., Wong, S. H., Letchumanan, V., & Lee, L. (2021) · Progress In Microbes & Molecular Biology · doi:10.36877/pmmb.a0000175 · Cited by 52 · see citing works
Zhang, Y., Ding, N., Hao, X., Zhao, J., Zhao, Y., Li, Y., & Li, Z. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1018371 · Cited by 52 · see citing works
Improving Alzheimer's disease by altering gut microbiota in tree shrews with ginsenoside Rg1
Wang, L., Lu, J., Zeng, Y.-Q., Guo, Y., Wu, C., Zhao, H., Zheng, H. Y., & Jiao, J. (2020) · FEMS Microbiology Letters · doi:10.1093/femsle/fnaa011 · Cited by 50 · see citing works
Self-citationSaccharomyces boulardii ameliorates gut dysbiosis associated cognitive decline
Sarkar, S. R., Mazumder, P. M., Chatterjee, K., Sarkar, A., Adhikary, M., Mukhopadhyay, K., & Banerjee, S. (2021) · Physiology & Behavior · doi:10.1016/j.physbeh.2021.113411 · Cited by 49 · see citing works
Microglia and gut microbiota: A double-edged sword in Alzheimer's disease
Bano, N., Khan, S., Ahamad, S., Kanshana, J. S., Dar, N. J., Khan, S. J., Nazir, A., & Bhat, S. A. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102515 · Cited by 49 · see citing works
González-Sanmiguel, J., Schuh, C. M. A. P., Muñoz-Montesino, C., Contreras‐Kallens, P., Aguayo, L. G., & Aguayo, S. D. (2020) · Cells · doi:10.3390/cells9112476 · Cited by 48 · see citing works
Wang, H., He, S., Xin, J., Zhang, T., Sun, N., Li, L., Ni, X., Zeng, D., Ma, H., & Bai, Y. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.662148 · Cited by 47 · see citing works
The Microbiota-Gut-Brain Axis as a Key to Neuropsychiatric Disorders: A Mini Review
Stopińska, K., Radziwoń-Zaleska, M., & Domitrz, I. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10204640 · Cited by 47 · see citing works
Yan, S., Zhu, H., Cheng, R., Tang, Z., & Zhang, M. (2022) · Physiology & Behavior · doi:10.1016/j.physbeh.2022.114023 · Cited by 47 · see citing works
Hadizadeh, M., Hamidi, G. A., & Salami, M. (2019) · PubMed Central · doi:10.22038/ijbms.2019.33956.8078 · Cited by 48 · see citing works
Probiotics protect against gut dysbiosis associated decline in learning and memory
Sarkar, S. R., Mazumder, P. M., & Banerjee, S. (2020) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2020.577390 · Cited by 46 · see citing works
Is adolescence the missing developmental link in Microbiome–Gut–Brain axis communication?
Flannery, J., Callaghan, B. L., Sharpton, T. J., Fisher, P. A., & Pfeifer, J. H. (2019) · Developmental Psychobiology · doi:10.1002/dev.21821 · Cited by 46 · see citing works
Hashim, H. M., & Makpol, S. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.1007166 · Cited by 46 · see citing works
Impact of Gut Microbiota in Brain Ageing: Polyphenols as Beneficial Modulators
Sarubbo, F., Moranta, D., Tejada, S., Jiménez-García, M., & Esteban, S. (2023) · Antioxidants · doi:10.3390/antiox12040812 · Cited by 44 · see citing works
Zhou, Z., Hui, E. S. K., Kranz, G. S., Chang, J. R., de Luca, K. E., Pinto, S. M., Chan, W. W. Y., Yau, S., Chau, B. K. H., Samartzis, D., et al. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101767 · Cited by 46 · see citing works
Rehman, M. U. U., Ghazanfar, S., Haq, R. U., Ullah, S., Khan, S., Wu, J.-B., Ahmad, W., & Tipu, M. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.915595 · Cited by 37 · see citing works
Wang, J., Lei, X., Xie, Z., Zhang, X., Cheng, X., Zhou, W., & Zhang, Y. (2019) · Aging · doi:10.18632/aging.101990 · Cited by 39 · see citing works
Jiang, J. H., Liu, H., Wang, Z., Tian, H., Wang, S., Yang, J., & Ren, J. (2021) · PLoS ONE · doi:10.1371/journal.pone.0259530 · Cited by 39 · see citing works
Tillmann, S., & Wegener, G. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.08.025 · Cited by 38 · see citing works
Tian, P., Chen, Y., Qian, X., Zou, R., Zhu, H., Zhao, J., Zhang, H., Wang, G., & Chen, W. (2021) · Food & Function · doi:10.1039/d1fo01608c · Cited by 37 · see citing works
The Role of Genetic, Environmental, and Dietary Factors in Alzheimer’s Disease: A Narrative Review
Mertaş, B., & Boşgelmez, İ. İ. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26031222 · Cited by 35 · see citing works
Some Candidate Drugs for Pharmacotherapy of Alzheimer’s Disease
Miziak, B., Błaszczyk, B., & Czuczwar, S. J. (2021) · Pharmaceuticals · doi:10.3390/ph14050458 · Cited by 35 · see citing works
Harrison, R. A., Sharafeldin, N., Rexer, J. L., Streck, B. P., Petersen, M. E., Henneghan, A. M., & Kesler, S. R. (2021) · The Oncologist · doi:10.1002/onco.13867 · Cited by 35 · see citing works
- Authors
- Wang, T., Hu, X., Liang, S., Li, W., Wu, X., Wang, L., & Jin, F.
- Affiliations
- Chinese Academy of Sciences (CN)
- Hangzhou Normal University (CN)
- Venue
- Beneficial Microbes
- Publisher
- Walter de Gruyter GmbH
- Published
- 2015-10-15
- Volume
- 6
- Issue
- 5
- Pages
- 707-718
- ISSN
- 1876-2883 (ISSN-L)
- 1876-2891
- OpenAlex
- W2099514643
- Cited by
- 233
- References
- 59
- Citations by year
- 2026: 11 · 2025: 12 · 2024: 23 · 2023: 24 · 2022: 34 · 2021: 40 · 2020: 28 · 2019: 16 · 2018: 19 · 2017: 15 · 2016: 9 · 2015: 2
- FWCI
- 20.07
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Beneficial Microbes (publishedVersion)
- PubMed (publishedVersion)
- Institutional Repository of Institute of Psychology, Chinese Academy of Sciences (Institute of Psychology, Chinese Academy of Sciences) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- probiotics, ampicillin, antibiotic-induced gut dysbiosis, gut-brain axis, anxiety-like behavior, memory impairment, hippocampus, mineralocorticoid receptor, NMDA receptor, colonic inflammation, antibiotic adverse effects
- MeSH terms
- Gastrointestinal Microbiome, Ampicillin, Animals, Anti-Bacterial Agents, Anxiety, Gastroenteritis, Hippocampus, Memory Disorders, Receptors, N-Methyl-D-Aspartate, Receptors, Mineralocorticoid, Probiotics, Rats, Limosilactobacillus fermentum
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