Cited by 382Gut microbiota and healthTryptophan and brain disordersGastrointestinal motility and disorders

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Antibiotic-induced microbiota perturbation causes gut endocannabinoidome changes, hippocampal neuroglial reorganization and depression in mice

Guida, F., Turco, F., Iannotta, M., De Gregorio, D., Palumbo, I., Sarnelli, G., Furiano, A., Napolitano, F., Boccella, S., Luongo, L., Mazzitelli, M., Usiello, A., De Filippis, F., Iannotti, F.A., Piscitelli, F., Ercolini, D., de Novellis, V., Di Marzo, V., Cuomo, R., Maione, S.·2018·Brain Behavior and Immunity

DOI 10.1016/j.bbi.2017.09.001

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Abstract

The microbiota-gut-brain axis (MGBA) regulates the reciprocal interaction between chronic inflammatory bowel and psychiatric disorders. This interaction involves multiple pathways that are highly debated. We examined the behavioural, biochemical and electrophysiological alterations, as well as gut microbiota composition in a model of antibiotic-induced experimental dysbiosis. Inflammation of the small intestine was also assessed. Mice were exposed to a mixture of antimicrobials for 2weeks. Afterwards, they received Lactobacillus casei DG (LCDG) or a vehicle for up to 7days via oral gavage. Perturbation of microbiota was accompanied by a general inflammatory state and alteration of some endocannabinoidome members in the gut. Behavioural changes, including increased immobility in the tail suspension test and reduced social recognition were observed, and were associated with altered BDNF/TrkB signalling, TRPV1 phosphorylation and neuronal firing in the hippocampus. Moreover, morphological rearrangements of non-neuronal cells in brain areas controlling emotional behaviour were detected. Subsequent probiotic administration, compared with vehicle, counteracted most of these gut inflammatory, behavioural, biochemical and functional alterations. Interestingly, levels of Lachnospiraceae were found to significantly correlate with the behavioural changes observed in dysbiotic mice. Our findings clarify some of the biomolecular and functional modifications leading to the development of affective disorders associated with gut microbiota alterations.

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Additional file 14 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688688
Additional file 4 of The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
Xu, L., Surathu, A., Raplee, I., Chockalingam, A., Stewart, S. R., Walker, L., Sacks, L. V., Patel, V. P., Li, Z., & Rouse, R. L. (2020) · Figshare · doi:10.6084/m9.figshare.12050103
Additional file 18 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688700
Additional file 2 of The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
Xu, L., Surathu, A., Raplee, I., Chockalingam, A., Stewart, S. R., Walker, L., Sacks, L. V., Patel, V. P., Li, Z., & Rouse, R. L. (2020) · Figshare · doi:10.6084/m9.figshare.12050091
Additional file 5 of The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
Xu, L., Surathu, A., Raplee, I., Chockalingam, A., Stewart, S. R., Walker, L., Sacks, L. V., Patel, V. P., Li, Z., & Rouse, R. L. (2020) · Figshare · doi:10.6084/m9.figshare.12263762
Additional file 4 of The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
Xu, L., Surathu, A., Raplee, I., Chockalingam, A., Stewart, S. R., Walker, L., Sacks, L. V., Patel, V. P., Li, Z., & Rouse, R. L. (2020) · Figshare · doi:10.6084/m9.figshare.12263759
Additional file 17 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688697
Additional file 6 of The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
Xu, L., Surathu, A., Raplee, I., Chockalingam, A., Stewart, S. R., Walker, L., Sacks, L. V., Patel, V. P., Li, Z., & Rouse, R. L. (2020) · Figshare · doi:10.6084/m9.figshare.12263765
Additional file 20 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688706
Additional file 3 of The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
Xu, L., Surathu, A., Raplee, I., Chockalingam, A., Stewart, S. R., Walker, L., Sacks, L. V., Patel, V. P., Li, Z., & Rouse, R. L. (2020) · Figshare · doi:10.6084/m9.figshare.12263756
Additional file 15 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688691
Additional file 3 of The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
Xu, L., Surathu, A., Raplee, I., Chockalingam, A., Stewart, S. R., Walker, L., Sacks, L. V., Patel, V. P., Li, Z., & Rouse, R. L. (2020) · Figshare · doi:10.6084/m9.figshare.12050094
Additional file 13 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688685
Additional file 19 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688703
Additional file 2 of The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
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Additional file 16 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
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Additional file 7 of Beyond the lesion site: minocycline augments inflammation and anxiety-like behavior following SCI in rats through action on the gut microbiota
Schmidt, E. K. A., Raposo, P. J. F., Espin, A. T., Fenrich, K. K., & Fouad, K. (2021) · Figshare · doi:10.6084/m9.figshare.14853219
Additional file 5 of Beyond the lesion site: minocycline augments inflammation and anxiety-like behavior following SCI in rats through action on the gut microbiota
Schmidt, E. K. A., Raposo, P. J. F., Espin, A. T., Fenrich, K. K., & Fouad, K. (2021) · Figshare · doi:10.6084/m9.figshare.14853213
Additional file 9 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688664
Additional file 11 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688673
Additional file 3 of Gut dysbiosis induces the development of depression-like behavior through abnormal synapse pruning in microglia-mediated by complement C3
Hao, W., Ma, Q., Wang, L., Yuan, N., Gan, H. T., He, L., Li, X., Huang, J., & Chen, J. (2024) · Figshare · doi:10.6084/m9.figshare.26682949
Additional file 2 of Gut dysbiosis induces the development of depression-like behavior through abnormal synapse pruning in microglia-mediated by complement C3
Hao, W., Ma, Q., Wang, L., Yuan, N., Gan, H. T., He, L., Li, X., Huang, J., & Chen, J. (2024) · Figshare · doi:10.6084/m9.figshare.26682946
Additional file 9 of Beyond the lesion site: minocycline augments inflammation and anxiety-like behavior following SCI in rats through action on the gut microbiota
Schmidt, E. K. A., Raposo, P. J. F., Espin, A. T., Fenrich, K. K., & Fouad, K. (2021) · Figshare · doi:10.6084/m9.figshare.14853225
Additional file 2 of Beyond the lesion site: minocycline augments inflammation and anxiety-like behavior following SCI in rats through action on the gut microbiota
Schmidt, E. K. A., Raposo, P. J. F., Espin, A. T., Fenrich, K. K., & Fouad, K. (2021) · Figshare · doi:10.6084/m9.figshare.14853204
Additional file 4 of Beyond the lesion site: minocycline augments inflammation and anxiety-like behavior following SCI in rats through action on the gut microbiota
Schmidt, E. K. A., Raposo, P. J. F., Espin, A. T., Fenrich, K. K., & Fouad, K. (2021) · Figshare · doi:10.6084/m9.figshare.14853210
Additional file 8 of Beyond the lesion site: minocycline augments inflammation and anxiety-like behavior following SCI in rats through action on the gut microbiota
Schmidt, E. K. A., Raposo, P. J. F., Espin, A. T., Fenrich, K. K., & Fouad, K. (2021) · Figshare · doi:10.6084/m9.figshare.14853222
Additional file 1 of Gut dysbiosis induces the development of depression-like behavior through abnormal synapse pruning in microglia-mediated by complement C3
Hao, W., Ma, Q., Wang, L., Yuan, N., Gan, H. T., He, L., Li, X., Huang, J., & Chen, J. (2024) · Figshare · doi:10.6084/m9.figshare.26682943
Additional file 4 of Gut dysbiosis induces the development of depression-like behavior through abnormal synapse pruning in microglia-mediated by complement C3
Hao, W., Ma, Q., Wang, L., Yuan, N., Gan, H. T., He, L., Li, X., Huang, J., & Chen, J. (2024) · Figshare · doi:10.6084/m9.figshare.26682952
Additional file 6 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688646
Additional file 8 of Gut dysbiosis induces the development of depression-like behavior through abnormal synapse pruning in microglia-mediated by complement C3
Hao, W., Ma, Q., Wang, L., Yuan, N., Gan, H. T., He, L., Li, X., Huang, J., & Chen, J. (2024) · Figshare · doi:10.6084/m9.figshare.26682964
Additional file 7 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688649
Additional file 2 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688631
Additional file 3 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688634
Additional file 1 of Gut microbiota intervention attenuates thermogenesis in broilers exposed to high temperature through modulation of the hypothalamic 5-HT pathway
Li, S., Li, X., Wang, K., Li, Y., Nagaoka, K., & Li, C. (2023) · Figshare · doi:10.6084/m9.figshare.24892819
Additional file 1 of The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
Xu, L., Surathu, A., Raplee, I., Chockalingam, A., Stewart, S. R., Walker, L., Sacks, L., Patel, V., Li, Z., & Rouse, R. L. (2020) · Figshare · doi:10.6084/m9.figshare.12263750
Additional file 12 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688679
Additional file 1 of The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
Xu, L., Surathu, A., Raplee, I., Chockalingam, A., Stewart, S. R., Walker, L., Sacks, L., Patel, V., Li, Z., & Rouse, R. L. (2020) · Figshare · doi:10.6084/m9.figshare.12050085
Additional file 3 of Beyond the lesion site: minocycline augments inflammation and anxiety-like behavior following SCI in rats through action on the gut microbiota
Schmidt, E. K. A., Raposo, P. J. F., Espin, A. T., Fenrich, K. K., & Fouad, K. (2021) · Figshare · doi:10.6084/m9.figshare.14853207
Additional file 1 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688628
Additional file 3 of Gut microbiota intervention attenuates thermogenesis in broilers exposed to high temperature through modulation of the hypothalamic 5-HT pathway
Li, S., Li, X., Wang, K., Li, Y., Nagaoka, K., & Li, C. (2024) · Figshare · doi:10.6084/m9.figshare.26657248
Additional file 7 of Gut dysbiosis induces the development of depression-like behavior through abnormal synapse pruning in microglia-mediated by complement C3
Hao, W., Ma, Q., Wang, L., Yuan, N., Gan, H. T., He, L., Li, X., Huang, J., & Chen, J. (2024) · Figshare · doi:10.6084/m9.figshare.26682961
Additional file 1 of Beyond the lesion site: minocycline augments inflammation and anxiety-like behavior following SCI in rats through action on the gut microbiota
Schmidt, E. K. A., Raposo, P. J. F., Espin, A. T., Fenrich, K. K., & Fouad, K. (2021) · Figshare · doi:10.6084/m9.figshare.14853201
Additional file 5 of Gut dysbiosis induces the development of depression-like behavior through abnormal synapse pruning in microglia-mediated by complement C3
Hao, W., Ma, Q., Wang, L., Yuan, N., Gan, H. T., He, L., Li, X., Huang, J., & Chen, J. (2024) · Figshare · doi:10.6084/m9.figshare.26682955
Additional file 4 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688640
Additional file 5 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688643
Additional file 8 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Hao, Z., Meng, C., Li, L., Feng, S., Zhu, Y., Yang, J., Han, L., Sun, L., Lv, W., Figeys, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22688655
Additional file 6 of Beyond the lesion site: minocycline augments inflammation and anxiety-like behavior following SCI in rats through action on the gut microbiota
Schmidt, E. K. A., Raposo, P. J. F., Espin, A. T., Fenrich, K. K., & Fouad, K. (2021) · Figshare · doi:10.6084/m9.figshare.14853216
Additional file 2 of Gut microbiota intervention attenuates thermogenesis in broilers exposed to high temperature through modulation of the hypothalamic 5-HT pathway
Li, S., Li, X., Wang, K., Li, Y., Nagaoka, K., & Li, C. (2024) · Figshare · doi:10.6084/m9.figshare.24892936
Additional file 10 of Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
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Additional file 6 of Gut dysbiosis induces the development of depression-like behavior through abnormal synapse pruning in microglia-mediated by complement C3
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Inserra, A., VanderZwaag, J., Campanale, A., Murray, C. J., & Szabo, A. J. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-27340-7.00008-5
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Authors: Guida, F., Turco, F., Iannotta, M., De Gregorio, D., Palumbo, I., Sarnelli, G., Furiano, A., Napolitano, F., Boccella, S., Luongo, L., Mazzitelli, M., Usiello, A., De Filippis, F., Iannotti, F. A., Piscitelli, F., Ercolini, D., de Novellis, V., Di Marzo, V., Cuomo, R., & Maione, S.
Affiliations: University of Campania "Luigi Vanvitelli" (IT)
Federico II University Hospital (IT)
CEINGE Biotecnologie Avanzate Franco Salvatore (Italy) (IT)
Istituto di Chimica Biomolecolare (IT)
University of Naples Federico II (IT)
Corresponding author: Guida, F.
Maione, S.
ORCID: Guida, F.
Turco, F.
Iannotta, M.
Palumbo, I.
Sarnelli, G.
Napolitano, F.
Boccella, S.
Luongo, L.
Mazzitelli, M.
Usiello, A.
Iannotti, F.A.
Piscitelli, F.
Ercolini, D.
Cuomo, R.
Maione, S.
Venue: Brain Behavior and Immunity
Publisher: Elsevier BV
Published: 2018-01
Volume: 67
Pages: 230-245
ISSN: 0889-1591 (ISSN-L)
DOI: 10.1016/j.bbi.2017.09.001
OpenAlex: W2753690838
Cited by: 367
References: 87
Citations by year: 2026: 20 · 2025: 45 · 2024: 52 · 2023: 58 · 2022: 49 · 2021: 48 · 2020: 38 · 2019: 37 · 2018: 18
FWCI: 11.50
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Behavior and Immunity (publishedVersion)
PubMed (publishedVersion)
Archivio Istituzionale della Ricerca - Università degli Studi della Campania "Luigi Vanvitelli" (submittedVersion)
Archivio Istituzionale della Ricerca - Università Vita-Salute San Raffaele (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords: microbiota-gut-brain axis, antibiotic-induced dysbiosis, depression, probiotics, Lactobacillus casei, BDNF/TrkB signaling, TRPV1, Lachnospiraceae, intestinal inflammation, social recognition, anxiety-like behavior, mood disorders
MeSH terms: Gastrointestinal Microbiome, Animals, Anti-Bacterial Agents, Behavior, Animal, Depression, Hippocampus, Inflammation, Intestinal Mucosa, Intestines, Male, Mice, Inbred C57BL, Neuroglia, Neurons, Brain-Derived Neurotrophic Factor, Probiotics, Endocannabinoids, Dysbiosis

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Antibiotic-induced microbiota perturbation causes gut endocannabinoidome changes, hippocampal neuroglial reorganization and depression in mice

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