Heterochronic faecal transplantation boosts gut germinal centres in aged mice
Open accessAbstract
Ageing is a complex multifactorial process associated with a plethora of disorders, which contribute significantly to morbidity worldwide. One of the organs significantly affected by age is the gut. Age-dependent changes of the gut-associated microbiome have been linked to increased frailty and systemic inflammation. This change in microbial composition with age occurs in parallel with a decline in function of the gut immune system; however, it is not clear whether there is a causal link between the two. Here we report that the defective germinal centre reaction in Peyer’s patches of aged mice can be rescued by faecal transfers from younger adults into aged mice and by immunisations with cholera toxin, without affecting germinal centre reactions in peripheral lymph nodes. This demonstrates that the poor germinal centre reaction in aged animals is not irreversible, and that it is possible to improve this response in older individuals by providing appropriate stimuli.
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Changes in the aging intestinal microbiota can adversely affect host metabolism and immunity and are associated with development of cardiovascular, autoimmune, metabolic, and neurodegenerative disorders.
“These changes can adversely affect the host metabolism and immunity [25–27, 40, 64, 86, 110, 112, 118] and are associated with the development of cardiovascular, autoimmune, metabolic, and neurodegenerative disorders [17, 90, 122, 132].”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [112]
In aged mice, receiving microbiota from young mice has been reported to extend life span or halt functional decline in the mucosal immune system.
“Similar beneficial effects have been reported in aged mice receiving microbiota from young mice to extend life span [8, 61] or halt the functional decline in the mucosal immune system [112].”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [112]
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“showed that heterochronic FMT from young into old mice and vice versa, boosts germinal center (GC) reaction in Peyer’s patches irrespective of age directionality (19).”
BackgroundSelf-citationThe metabolomic signature of extreme longevity: naked mole rats versus mice
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The gut microbiota is an emerging target for improving brain health during ageing
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“Furthermore, when microbes were transferred from young to aged mice via heterochronic FMT, the ageing-induced deficiency in the Peyer’s patch germinal cell reaction, a key compartment of intestinal immunity, was rescued (Stebegg et al., 2019).”
InfluentialMicrobiota–host interactions shape ageing dynamics
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“Analogously, transplanting microbiota from young mice to middle-aged mice boosted immune function, reactivating defective germinal centres in the gut [103]; and transplanting microbiota from healthy donors to progeroid (i.”
BackgroundEffects of gut microbiota on neurodegenerative diseases
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“In line with this, transplanting young mice’s fecal microbiota restored deficient B cell proliferation in the Peyer’s patches of old mice (Stebegg et al., 2019), demonstrating defenses against immunological dysregulation brought on by aging in young mice’s microbiome.”
BackgroundLiu, Q., Li, J., Sun, X., Lin, J., Yu, Z., Xiao, Y., Li, D., Sun, B., Bao, H., & Liu, Y. (2025) · Journal of Hematology & Oncology · doi:10.1186/s13045-025-01735-w · Cited by 54 · see citing works
“Fecal microbiota transplantation (FMT) between young and aged mice in the same strain restores the frequency and quantity of B cells in germinal center (GC) via adjuvant-like manner, highlighting strain-specific efficacy [192].”
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Crosstalk between gut microbiota and cellular senescence: a vicious cycle leading to aging gut
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“Additionally, the transplantation of fecal microbiota from young mice to aged mice has been performed, demonstrating protective effects of young mouse microbiota [60].”
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Resilience integrates concepts in aging research
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“, 2016) or the consequences of transplanting a diverse microbial community from young donors to naturally aged or progeroid hosts (Bárcena et al., 2019; Smith et al., 2017; Stebegg et al., 2019).”
BackgroundMicrobial Stimulation Reverses the Age-Related Decline in M Cells in Aged Mice
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Gut microbiota shape B cell in health and disease settings
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The Aged Intestine: Performance and Rejuvenation
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“Moreover, gut microbiota could play a role in regulating blood pressure (Hendrik et al., 2019; Tang et al., 2019).”
BackgroundThe gut-cardiovascular connection: new era for cardiovascular therapy
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“In murine studies, FMT can be simply achieved by oral gavage of the microbial content into the recipient mice [207].”
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BackgroundEstablishment and Resilience of Transplanted Gut Microbiota in Aged Mice
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“successfully performedheterologous FMT from youngdonormice into aged recipientmice (Bárcena et al., 2019; Spychala et al., 2018; Stebegg et al., 2019), the long-term colonization of the transplanted microbiota is usually maintainedby regularly repeating the FMTprocedure (Bárcena et al.”
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“Moreover, the defective germinal center response in aged mice can be rescued by replenishing the gut microbiome of aged mice with that of a younger animal [77].”
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“, 2017) and was also decreased in abundance in patients with colorectal cancer (Stebegg et al., 2019).”
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“FMT has been shown to rejuvenate aged HSCs [194], rescue ageing-associated germinal center deficiency [373], and enhance healthspan and lifespan in progeroid mouse models [191], thereby providing a potential therapy to rejuvenate aged immune system.”
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“Given the accumulating evidence of the role of the gut microbiota on overall health, life quality and/or expectancy could potentially be improved by remodeling the gut microbiome through interventions for probiotic/prebiotic regulation or fecal microbiota transplantation (FMT) (Smith et al., 2017; Vaiserman et al., 20…”
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“The cages of Young (FMT) mice and Young (Control) mice were respectively replenished with dirty bedding and fresh stools from aged or aged-matched young donor mice semiweekly [12].”
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The cellular factors that impair the germinal center in advanced age
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Self-citationFecal microbiota transplantation holds the secret to youth
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“…F-CON, F-SD, F − SD + MT (F-SM), and F-R group, FMT was performed via oral gavage of a feces into wild mice as described Stebegg et al.; [20] Aeromonas veronii colonization experiment: C-CON, C-Aeromonas (C-A), and C − Aeromonas + MT (C-AM) groups; and LPS experiment: LPS, LPS +…”
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Immune aging in annual killifish
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“87 However, our study was conducted in female BALB/cBy mice, and we and others 53 have not reported increased aggressive behavior or other behavioral changes in these cohoused mice.”
Gut microbiota is associated with persistence of longer-term BNT162b2 vaccine immunogenicity
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“Similar to humans, mice also experience age-related changes to the microbiome.(35) Interestingly, cohousing younger mice with older mice has been shown to reverse such aging-related changes in a previous study.”
BackgroundImpact of gut microbiota on cardiac aging
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“We used antibiotics before FMT based on the previous data [21,26,27].”
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The influence of aging and the microbiome in multiple sclerosis and other neurologic diseases
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“Using FMT, a causal role for the microbiota in several aspects of aging, including frailty and loss of physical fitness, 204 altered cognition, 116,137,205–208 impaired immunity, 209,210 and reduced neurogenesis, 211 has been described.”
The effect of T cell aging on the change of human tissue structure
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Additional file 1 of Gut microbiota of the young ameliorates physical fitness of the aged in mice
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“…t h e i r i n t e r a c t i o n w i t h t h e i n t e s t i n a l e p i t h e l i u m , t h e r e b y n e u t r a l i z i n g p o t e n t i a l t h r e a t s [ 55 – 59 ] T h e p r e s e n c e o f c e r t a i n c o mm e n s a l b a c t e r i a h a s b ee n l i n k e d t o i n c r e a s e d T G F - β”
- Authors
- Stebegg, M., Silva-Cayetano, A., Innocentin, S., Jenkins, T. P., Cantacessi, C., Gilbert, C., & Linterman, M. A.
- Affiliations
- Babraham Institute (GB)
- University of Cambridge (GB)
- Corresponding author
- Linterman, Michelle A.
- ORCID
- Venue
- Nature Communications
- Published
- 2019-06-04
- Volume
- 10
- Issue
- 1
- Pages
- 2443-2443
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC6547660
- OpenAlex
- W2948768639
- Cited by
- 107
- References
- 53
- Citations by year
- 2026: 12 · 2025: 9 · 2024: 16 · 2023: 17 · 2022: 17 · 2021: 18 · 2020: 14 · 2019: 3 · 2018: 1
- FWCI
- 4.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Apollo (cc-by)
- Funders
- Wellcome Trust
- European Commission (675395)
- Directorate for Biological Sciences
- Biotechnology and Biological Sciences Research Council (BBS/E/B/000C0407, BBS/E/B/000C0427)
- H2020 European Research Council (637801)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- Peyer's patches, gut-associated lymphoid tissue, gut microbiota, immunosenescence, frailty, systemic inflammation, aged mice
- MeSH terms
- Gastrointestinal Microbiome, Fecal Microbiota Transplantation, Aging, Animals, Cholera Toxin, Female, Immunoglobulin A, Immunization, Nitrophenols, Peyer's Patches, Phenylacetates, Germinal Center, Mice, Dysbiosis
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