Cited by 203Gut microbiota and healthGastrointestinal motility and disordersGenetics, Aging, and Longevity in Model Organisms

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Revisiting Metchnikoff: Age-related alterations in microbiota-gut-brain axis in the mouse

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Scott, Karen A., Ida, Masayuki, Peterson, Veronica L., Prenderville, Jack A., Moloney, Gerard M., Izumo, Takayuki, Murphy, Kiera, Murphy, Amy, Ross, R. Paul, Stanton, Catherine, Dinan, Timothy G., Cryan, John F.·2017·Brain, Behavior, and Immunity

DOI 10.1016/j.bbi.2017.02.004

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Abstract

Over the last decade, there has been increased interest in the role of the gut microbiome in health including brain health. This is by no means a new theory; Elie Metchnikoff proposed over a century ago that targeting the gut by consuming lactic acid bacteria such as those in yogurt, could improve or delay the onset of cognitive decline associated with ageing. However, there is limited information characterising the relationship between the behavioural and physiological sequelae of ageing and alterations in the gut microbiome. To this end, we assessed the behavioural, physiological and caecal microbiota profile of aged male mice. Older mice (20-21months old) exhibited deficits in spatial memory and increases in anxiety-like behaviours compared to younger mice (2-3months old). They also exhibited increased gut permeability, which was directly correlated with elevations in peripheral pro-inflammatory cytokines. Furthermore, stress exacerbated the gut permeability of aged mice. Examination of the caecal microbiota revealed significant increases in phylum TM7, family Porphyromonadaceae and genus Odoribacter of aged mice. This represents a shift of aged microbiota towards a profile previously associated with inflammatory disease, particularly gastrointestinal and liver disorders. Furthermore, Porphyromonadaceae, which has also been associated with cognitive decline and affective disorders, was directly correlated with anxiety-like behaviour in aged mice. These changes suggest that changes in the gut microbiota and associated increases in gut permeability and peripheral inflammation may be important mediators of the impairments in behavioural, affective and cognitive functions seen in ageing.

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Additional file 7 of Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain
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Additional file 5 of Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain
Parker, A., Romano, S., Ansorge, R., Aboelnour, A., Le Gall, G., Savva, G. M., Pontifex, M. G., Telatin, A., Baker, D., Jones, E. J., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19695980
Additional file 1 of Discrete patterns of microbiome variability across timescales in a wild rodent population
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Additional file 3 of Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain
Parker, A., Romano, S., Ansorge, R., Aboelnour, A., Le Gall, G., Savva, G. M., Pontifex, M. G., Telatin, A., Baker, D., Jones, E. J., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19695974
Additional file 6 of Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain
Parker, A., Romano, S., Ansorge, R., Aboelnour, A., Le Gall, G., Savva, G. M., Pontifex, M. G., Telatin, A., Baker, D., Jones, E. J., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19695983
Additional file 2 of Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain
Parker, A., Romano, S., Ansorge, R., Aboelnour, A., Le Gall, G., Savva, G. M., Pontifex, M. G., Telatin, A., Baker, D., Jones, E. J., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19695971
Additional file 4 of Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain
Parker, A., Romano, S., Ansorge, R., Aboelnour, A., Le Gall, G., Savva, G. M., Pontifex, M. G., Telatin, A., Baker, D., Jones, E. J., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19695977
Additional file 1 of Akkermansia muciniphila, which is enriched in the gut microbiota by metformin, improves cognitive function in aged mice by reducing the proinflammatory cytokine interleukin-6
Zhu, X., Shen, J., Feng, S., Huang, C., Wang, H., Huo, F., & Liu, H. (2023) · Figshare · doi:10.6084/m9.figshare.23265023
Additional file 1 of Huanglian Jiedu decoction remodels the periphery microenvironment to inhibit Alzheimer’s disease progression based on the “brain-gut” axis through multiple integrated omics
Gu, X., Zhou, J., Zhou, Y., Wang, H., Si, N., Ren, W., Zhao, W., Fan, X., Gao, W., Wei, X., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13979062

Authors: Scott, K. A., Ida, M., Peterson, V. L., Prenderville, J. A., Moloney, G. M., Izumo, T., Murphy, K., Murphy, A., Ross, R. P., Stanton, C., Dinan, T. G., & Cryan, J. F.
Affiliations: University College Cork (IE)
Suntory (Japan) (JP)
Teagasc - The Irish Agriculture and Food Development Authority (IE)
Corresponding author: Cryan, John F.
ORCID: Scott, Karen A.
Peterson, Veronica L.
Moloney, Gerard M.
Izumo, Takayuki
Murphy, Kiera
Ross, R. Paul
Stanton, Catherine
Dinan, Timothy G.
Cryan, John F.
Venue: Brain, Behavior, and Immunity
Publisher: Elsevier BV
Published: 2017-10
Volume: 65
Pages: 20-32
ISSN: 0889-1591 (ISSN-L)
DOI: 10.1016/j.bbi.2017.02.004
OpenAlex: W2585159410
Cited by: 202
References: 87
Citations by year: 2026: 5 · 2025: 13 · 2024: 21 · 2023: 15 · 2022: 32 · 2021: 27 · 2020: 24 · 2019: 34 · 2018: 20 · 2017: 11
FWCI: 9.95
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (am, 300 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Brain Behavior and Immunity (acceptedVersion)
PubMed (publishedVersion)
Arrow@dit (Dublin Institute of Technology) (acceptedVersion)
Cork Open Research Archive (University College Cork, Ireland) (submittedVersion, cc-by-nc-nd)
Funders: Science Foundation Ireland
SFI
Health Research Board (12)
Department of Agriculture, Food & the Marine
Enterprise Ireland
APC Microbiome Institute
University College Cork
AstraZeneca
Mead Johnson
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords: gut microbiota, microbiota-gut-brain axis, aging, cognitive decline, spatial memory, anxiety-like behavior, intestinal permeability, peripheral inflammation, inflammatory cytokines, Porphyromonadaceae, Odoribacter, cecal microbiota, stress, lactic acid bacteria, mouse model
MeSH terms: Gastrointestinal Microbiome, Age Factors, Animals, Anxiety, Behavior, Animal, Brain, Cognition, Inflammation, Male, Mice, Inbred C57BL, Cytokines, Porphyromonas, Gastrointestinal Tract, Mice, Microbiota

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