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Cited by 107Gut microbiota and healthT-cell and B-cell ImmunologyGenetics, Aging, and Longevity in Model Organisms

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Heterochronic faecal transplantation boosts gut germinal centres in aged mice

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Stebegg, Marisa, Silva-Cayetano, Alyssa, Innocentin, Silvia, Jenkins, Timothy P., Cantacessi, Cinzia, Gilbert, Colin, Linterman, Michelle A.·2019·Nature Communications
DOI 10.1038/s41467-019-10430-7PMC PMC6547660
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Abstract

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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Fig. 1 Germinal centre B cells are reduced in the Peyer’s patches of aged BALB/c and C57BL/6 mice. Flow cytometric analysis of germinal centre (GC) cell populations in the Peyer’s patches (PPs) of adult (3-month-old) and aged (22-month-old) BALB/c and C57BL/6 mice. a–c Representative flow cytometric plots (a) and quantitation of B220+Ki67+Bcl6+ GC B cells (b, c) in the PPs of 3-month-old and 22-month-old BALB/c mice. d, e Quantitation of B220+Ki67+Bcl6+ GC B cell percentage (d) and number (e) in C57BL/6 mice. f–h Representative flow plots (f) and quantitation of CD4+Foxp3−CXCR5+PD-1+ Tfh cells (g, h) in the PPs of BALB/c mice. i, j Quantitation of Tfh cell percentages (i) and numbers (j) in C57BL/6 mice. k–m Representative flow plots (k) and quantitation of CD4+Foxp3+CXCR5+PD-1+ Tfr cells (l, m) in BALB/c mice. n, o Quantitation of Tfr cell percentages (n) and numbers (o) in C57BL/6 mice. Bar graphs show the combined results of 3–6 independent experiments which were performed with female BALB/c mice and both male and female C57BL/6 mice with a total of n = 11–49 mice per group. Bar height corresponds to the mean, and each circle represents one biological replicate. P-values were determined using the Mann-Whitney test in GraphPad Prism6. Source data are provided as a Source Data file
Fig. 1 Germinal centre B cells are reduced in the Peyer’s patches of aged BALB/c and C57BL/6 mice. Flow cytometric analysis of germinal centre (GC) cell populations in the Peyer’s patches (PPs) of adult (3-month-old) and aged (22-month-old) BALB/c and C57BL/6 mice. a–c Representative flow cytometric plots (a) and quantitation of B220+Ki67+Bcl6+ GC B cells (b, c) in the PPs of 3-month-old and 22-month-old BALB/c mice. d, e Quantitation of B220+Ki67+Bcl6+ GC B cell percentage (d) and number (e) in C57BL/6 mice. f–h Representative flow plots (f) and quantitation of CD4+Foxp3−CXCR5+PD-1+ Tfh cells (g, h) in the PPs of BALB/c mice. i, j Quantitation of Tfh cell percentages (i) and numbers (j) in C57BL/6 mice. k–m Representative flow plots (k) and quantitation of CD4+Foxp3+CXCR5+PD-1+ Tfr cells (l, m) in BALB/c mice. n, o Quantitation of Tfr cell percentages (n) and numbers (o) in C57BL/6 mice. Bar graphs show the combined results of 3–6 independent experiments which were performed with female BALB/c mice and both male and female C57BL/6 mice with a total of n = 11–49 mice per group. Bar height corresponds to the mean, and each circle represents one biological replicate. P-values were determined using the Mann-Whitney test in GraphPad Prism6. Source data are provided as a Source Data fileCC BY · PubMed Central
Fig. 2 The gut microbiome changes during ageing. 16S rRNA sequencing data were generated from faecal pellets collected from adult (3-month-old) and aged (21-month-old) BALB/c females and C57BL/6 males. a, b Bray-Curtis PCoA and d, e bacterial diversities (measured by Shannon index) of samples collected from 3-month-old and 21-month-old BALB/c mice (a, d) and C57BL/6 mice (b, e). The overall p-value was based on ANOVA tests. c, f Depiction of bacterial families whose abundance was significantly different between 3-month-old and 21-month-old BALB/c (c) and C57BL/6 (f) mice as determined by ANOVA analysis after cumulative-sum scaling (CSS). g, h Krona plots depicting the phylogenetic composition of the gut microbiome in 3-month-old (top) and 21-month-old (bottom) BALB/c (g) and C57BL/6 (h) mice. The percentages shown are averages of the samples in each age group. Samples were collected in 2 independent experiments for BALB/c mice and 3 independent experiments for C57BL/6 mice with a total of n = 5–14 mice per group. P-values are based on ANOVA tests *FDR ≤ 0.05, **FDR ≤ 0.01, ***FDR ≤ 0.001. Source data are provided as a Source Data file
Fig. 2 The gut microbiome changes during ageing. 16S rRNA sequencing data were generated from faecal pellets collected from adult (3-month-old) and aged (21-month-old) BALB/c females and C57BL/6 males. a, b Bray-Curtis PCoA and d, e bacterial diversities (measured by Shannon index) of samples collected from 3-month-old and 21-month-old BALB/c mice (a, d) and C57BL/6 mice (b, e). The overall p-value was based on ANOVA tests. c, f Depiction of bacterial families whose abundance was significantly different between 3-month-old and 21-month-old BALB/c (c) and C57BL/6 (f) mice as determined by ANOVA analysis after cumulative-sum scaling (CSS). g, h Krona plots depicting the phylogenetic composition of the gut microbiome in 3-month-old (top) and 21-month-old (bottom) BALB/c (g) and C57BL/6 (h) mice. The percentages shown are averages of the samples in each age group. Samples were collected in 2 independent experiments for BALB/c mice and 3 independent experiments for C57BL/6 mice with a total of n = 5–14 mice per group. P-values are based on ANOVA tests *FDR ≤ 0.05, **FDR ≤ 0.01, ***FDR ≤ 0.001. Source data are provided as a Source Data fileCC BY · PubMed Central
Fig. 3 Co-housing boosts the gut germinal centre response of aged BALB/c mice. Adult and aged female BALB/c mice were co-housed for 30–40 days, then Peyer’s patch (PP) germinal centre (GC) cell populations were analysed by flow cytometry. The percentage and number of B220+Ki67+Bcl6+ GC B cells (a, b), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (c, d) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (e, f) in Peyer’s patches. g–j 16S rRNA sequencing data were generated from faecal pellets collected from 5 adult and 5 aged BALB/c mice at the start and end of co-housing (n = 5 mice per group). Samples were clustered by Bray-Curtis PCoA (g) and bacterial diversities were measured by the Shannon index (h). The overall p-value was based on ANOVA tests. i Venn diagrams showing the numbers of shared and unique bacterial species detected in both age groups of mice before co-housing and after co-housing. j Depiction of bacterial families whose abundance was significantly different between co-housed BALB/c mice as determined by ANOVA analysis after cumulative-sum scaling (CSS). *FDR ≤ 0.05, **FDR ≤ 0.01, ***FDR ≤ 0.001. Families previously found to be significantly decreased in aged versus adult BALB/c mice before co-housing are marked in grey. In a–f bar plots show the combined results of 2 independent experiments with a total of n = 17–18 mice per group. Bar height corresponds to the mean, and each circle represents one biological replicate. P-values were determined using the Mann–Whitney test in GraphPad Prism6. Source data are provided as a Source Data file
Fig. 3 Co-housing boosts the gut germinal centre response of aged BALB/c mice. Adult and aged female BALB/c mice were co-housed for 30–40 days, then Peyer’s patch (PP) germinal centre (GC) cell populations were analysed by flow cytometry. The percentage and number of B220+Ki67+Bcl6+ GC B cells (a, b), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (c, d) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (e, f) in Peyer’s patches. g–j 16S rRNA sequencing data were generated from faecal pellets collected from 5 adult and 5 aged BALB/c mice at the start and end of co-housing (n = 5 mice per group). Samples were clustered by Bray-Curtis PCoA (g) and bacterial diversities were measured by the Shannon index (h). The overall p-value was based on ANOVA tests. i Venn diagrams showing the numbers of shared and unique bacterial species detected in both age groups of mice before co-housing and after co-housing. j Depiction of bacterial families whose abundance was significantly different between co-housed BALB/c mice as determined by ANOVA analysis after cumulative-sum scaling (CSS). *FDR ≤ 0.05, **FDR ≤ 0.01, ***FDR ≤ 0.001. Families previously found to be significantly decreased in aged versus adult BALB/c mice before co-housing are marked in grey. In a–f bar plots show the combined results of 2 independent experiments with a total of n = 17–18 mice per group. Bar height corresponds to the mean, and each circle represents one biological replicate. P-values were determined using the Mann–Whitney test in GraphPad Prism6. Source data are provided as a Source Data fileCC BY · PubMed Central
Fig. 4 Co-housing boosts the gut germinal centre response of aged C57BL/6 mice. a–f Adult and aged female C57BL/6 mice were co-housed for 30–40 days, then Peyer’s patch (PP) germinal centre (GC) cell populations were analysed. The percentage and number of B220+Ki67+Bcl6+ GC B cells (a, b), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (c, d) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (e, f) in Peyer’s patches as quantified by flow cytometry. 16S rRNA sequencing data were generated from faecal pellets collected from 5 adult 3-month-old and 5 aged C57BL/6 mice before (start) and after (end) co-housing. Bray-Curtis PCoA (g) and Shannon diversities (h) of samples collected from adult and aged C57BL/6 mice. The overall p-value was based on ANOVA testing. i Depiction of bacterial families whose abundance was significantly different between co-housed C57BL/6 mice as determined by ANOVA analysis after cumulative-sum scaling (CSS). *FDR ≤ 0.05, **FDR ≤ 0.01, ***FDR ≤ 0.001. In a–f bar plots show the combined results of 2 independent experiments with a total of n = 25–30 mice per group. Bar height corresponds to the mean, each circle represents one biological replicate. P-values were determined using the Mann–Whitney test in GraphPad Prism6. Source data are provided as a Source Data file
Fig. 4 Co-housing boosts the gut germinal centre response of aged C57BL/6 mice. a–f Adult and aged female C57BL/6 mice were co-housed for 30–40 days, then Peyer’s patch (PP) germinal centre (GC) cell populations were analysed. The percentage and number of B220+Ki67+Bcl6+ GC B cells (a, b), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (c, d) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (e, f) in Peyer’s patches as quantified by flow cytometry. 16S rRNA sequencing data were generated from faecal pellets collected from 5 adult 3-month-old and 5 aged C57BL/6 mice before (start) and after (end) co-housing. Bray-Curtis PCoA (g) and Shannon diversities (h) of samples collected from adult and aged C57BL/6 mice. The overall p-value was based on ANOVA testing. i Depiction of bacterial families whose abundance was significantly different between co-housed C57BL/6 mice as determined by ANOVA analysis after cumulative-sum scaling (CSS). *FDR ≤ 0.05, **FDR ≤ 0.01, ***FDR ≤ 0.001. In a–f bar plots show the combined results of 2 independent experiments with a total of n = 25–30 mice per group. Bar height corresponds to the mean, each circle represents one biological replicate. P-values were determined using the Mann–Whitney test in GraphPad Prism6. Source data are provided as a Source Data fileCC BY · PubMed Central
Fig. 5 Faecal microbiota transplantation boosts gut germinal centres irrespective of age directionality. a–g 21-month-old C57BL/6 males were gavaged with faecal pellets from adult, 3-month-old mice. a Experimental outline (created by M. Stebegg) of faecal microbiota transplantation (FMT) where aged C57BL/6 males were given a suspension of faecal pellets from adult C57BL/6 donor mice by oral gavage. The cages of recipient mice were supplemented with fresh faecal pellets and dirty bedding from these donor mice once a week. The percentage and number of B220+Ki67+Bcl6+ germinal centre (GC) B cells (b, c), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (d, e) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (f, g) in Peyer’s patches (PPs) as quantified by flow cytometry. h–n 3-month-old C57BL/6 males were gavaged with faecal pellets from aged 21-month-old mice. (h) Experimental outline of FMT where adult C57BL/6 males were gavaged with faecal pellets from aged mice. The percentage and number of GC B (i, j), Tfh (k, l) and Tfr (m, n) cells in PPs were quantified by flow cytometry. Bar height corresponds to the mean, each circle represents one biological replicate. Bar plots show the combined results of 2 independent experiments with a total of n = 10–15 mice per group. P-values were determined using the Mann-Whitney test in GraphPad Prism6. Source data are provided as a Source Data file
Fig. 5 Faecal microbiota transplantation boosts gut germinal centres irrespective of age directionality. a–g 21-month-old C57BL/6 males were gavaged with faecal pellets from adult, 3-month-old mice. a Experimental outline (created by M. Stebegg) of faecal microbiota transplantation (FMT) where aged C57BL/6 males were given a suspension of faecal pellets from adult C57BL/6 donor mice by oral gavage. The cages of recipient mice were supplemented with fresh faecal pellets and dirty bedding from these donor mice once a week. The percentage and number of B220+Ki67+Bcl6+ germinal centre (GC) B cells (b, c), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (d, e) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (f, g) in Peyer’s patches (PPs) as quantified by flow cytometry. h–n 3-month-old C57BL/6 males were gavaged with faecal pellets from aged 21-month-old mice. (h) Experimental outline of FMT where adult C57BL/6 males were gavaged with faecal pellets from aged mice. The percentage and number of GC B (i, j), Tfh (k, l) and Tfr (m, n) cells in PPs were quantified by flow cytometry. Bar height corresponds to the mean, each circle represents one biological replicate. Bar plots show the combined results of 2 independent experiments with a total of n = 10–15 mice per group. P-values were determined using the Mann-Whitney test in GraphPad Prism6. Source data are provided as a Source Data fileCC BY · PubMed Central
Fig. 6 Faecal microbiota transplantation boosts the gut germinal centre response of aged BALB/c mice. 21-month-old BALB/c mice were given a suspension of faecal pellets taken from 3-month-old mice by oral gavage. The cages of aged recipients were supplemented with fresh faecal pellets and dirty bedding from these donors once a week. a–f Bar plots show the combined results of 2 independent experiments. The percentage and number of B220+Ki67+Bcl6+ germinal centre (GC) B cells (a, b), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (c, d) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (e, f) in Peyer’s patches as quantified by flow cytometry. Bar height corresponds to the mean, each circle represents one biological replicate. Bar plots show the combined results of 2 independent experiments with a total of n = 9–10 mice per group. P-values were determined using the Mann–Whitney test in GraphPad Prism6. g–i 16S rRNA sequencing data were generated from faecal pellets collected from 5 adult donor mice and 5 aged BALB/c mice before and after faecal microbiota transplantation (FMT). g Bray–Curtis PCoA of FMT samples. h Shannon diversities with an overall p-value generated from ANOVA tests. i Venn diagrams showing the numbers of shared and unique bacterial species detected in adult donor mice and aged mice before FMT (start; left) or after FMT (end; right). Source data are provided as a Source Data file
Fig. 6 Faecal microbiota transplantation boosts the gut germinal centre response of aged BALB/c mice. 21-month-old BALB/c mice were given a suspension of faecal pellets taken from 3-month-old mice by oral gavage. The cages of aged recipients were supplemented with fresh faecal pellets and dirty bedding from these donors once a week. a–f Bar plots show the combined results of 2 independent experiments. The percentage and number of B220+Ki67+Bcl6+ germinal centre (GC) B cells (a, b), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (c, d) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (e, f) in Peyer’s patches as quantified by flow cytometry. Bar height corresponds to the mean, each circle represents one biological replicate. Bar plots show the combined results of 2 independent experiments with a total of n = 9–10 mice per group. P-values were determined using the Mann–Whitney test in GraphPad Prism6. g–i 16S rRNA sequencing data were generated from faecal pellets collected from 5 adult donor mice and 5 aged BALB/c mice before and after faecal microbiota transplantation (FMT). g Bray–Curtis PCoA of FMT samples. h Shannon diversities with an overall p-value generated from ANOVA tests. i Venn diagrams showing the numbers of shared and unique bacterial species detected in adult donor mice and aged mice before FMT (start; left) or after FMT (end; right). Source data are provided as a Source Data fileCC BY · PubMed Central
Fig. 7 Faecal microbiota transplantation between adult mice of different strains does not affect gut germinal centres. a, b 16S rRNA sequencing data generated from faecal pellets collected from adult 3-month-old C57BL/6 and BALB/c mice. (a) Bray-Curtis PCoA comparing samples from 3-month-old BALB/c and C57BL/6 mice. b Shannon diversities, with a p-value based on ANOVA tests. c–h Three-month-old C57BL/6 mice were given a suspension of faecal pellets taken from 3-month-old BALB/c mice by oral gavage to achieve faecal microbiota transplantation (FMT). In addition, the cages of C57BL/6 recipients were supplemented with fresh faecal pellets and dirty bedding from BALB/c mice once a week. Control mice were gavaged with PBS. The percentage and number of B220+Ki67+Bcl6+ GC B cells (c, d), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (e, f) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (g, h) in Peyer’s patches as quantified by flow cytometry. Bar plots show the combined results of two experiments with a total of n = 14–15 mice per group. Bar height corresponds to the mean, each circle represents one biological replicate. P-values were determined using the Mann-Whitney test in GraphPad Prism6. Source data are provided as a Source Data file
Fig. 7 Faecal microbiota transplantation between adult mice of different strains does not affect gut germinal centres. a, b 16S rRNA sequencing data generated from faecal pellets collected from adult 3-month-old C57BL/6 and BALB/c mice. (a) Bray-Curtis PCoA comparing samples from 3-month-old BALB/c and C57BL/6 mice. b Shannon diversities, with a p-value based on ANOVA tests. c–h Three-month-old C57BL/6 mice were given a suspension of faecal pellets taken from 3-month-old BALB/c mice by oral gavage to achieve faecal microbiota transplantation (FMT). In addition, the cages of C57BL/6 recipients were supplemented with fresh faecal pellets and dirty bedding from BALB/c mice once a week. Control mice were gavaged with PBS. The percentage and number of B220+Ki67+Bcl6+ GC B cells (c, d), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (e, f) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (g, h) in Peyer’s patches as quantified by flow cytometry. Bar plots show the combined results of two experiments with a total of n = 14–15 mice per group. Bar height corresponds to the mean, each circle represents one biological replicate. P-values were determined using the Mann-Whitney test in GraphPad Prism6. Source data are provided as a Source Data fileCC BY · PubMed Central
Fig. 8 Faecal microbiota transplantation does not enhance NP-CTx-specific immune responses in the gut. 21-month-old C57BL/6 mice received faecal microbiota transplantation (FMT) or PBS by oral gavage as described above, followed by three oral immunisations with NP-CTx once a week. After three weeks, NP-CTx-specific antibody levels were analysed in PBS-gavaged, NP-CTx-immunised 23-months-old C57BL/6 mice (CTx) compared with aged mice receiving FMT plus NP-CTx (FMT + CTx). Peyer’s patch (PP) germinal centre (GC) responses in these mice were compared with naïve, 23-month-old C57BL/6 mice (Ctrl). a–d Antigen-specific IgA levels against CTx (a) and NP (b–d) in faecal contents from the ileum were assessed by ELISA. NP20-specific IgA (b), high-affinity NP2-specific IgA (c) and the ratio of NP2-to-NP20-specific IgA antibodies (d) were used as a measure for affinity maturation. e–h Antigen-specific IgG1 levels against CTx (e) and NP (f–h) in the serum were assessed by ELISAs for CTx-specific IgG1 (e), NP20-specific IgG1 (f), high-affinity NP2-specific IgG1 (g) and the ratio of NP2-to-NP20-specific IgG1 antibodies (h). i–n The percentage and number of B220+Ki67+Bcl6+ GC B cells (i, j), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (k, l) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (m, n) in PPs were quantified by flow cytometry. Bar plots show the combined results of 2 independent experiments with a total of n = 10–13 mice per group. Bar height corresponds to the mean, and each circle represents one biological replicate. P-values were determined using Mann–Whitney tests (a–h) or the Kruskal–Wallis test with Dunn’s multiple testing correction (i–n) in GraphPad Prism6. Source data are provided as a Source Data file
Fig. 8 Faecal microbiota transplantation does not enhance NP-CTx-specific immune responses in the gut. 21-month-old C57BL/6 mice received faecal microbiota transplantation (FMT) or PBS by oral gavage as described above, followed by three oral immunisations with NP-CTx once a week. After three weeks, NP-CTx-specific antibody levels were analysed in PBS-gavaged, NP-CTx-immunised 23-months-old C57BL/6 mice (CTx) compared with aged mice receiving FMT plus NP-CTx (FMT + CTx). Peyer’s patch (PP) germinal centre (GC) responses in these mice were compared with naïve, 23-month-old C57BL/6 mice (Ctrl). a–d Antigen-specific IgA levels against CTx (a) and NP (b–d) in faecal contents from the ileum were assessed by ELISA. NP20-specific IgA (b), high-affinity NP2-specific IgA (c) and the ratio of NP2-to-NP20-specific IgA antibodies (d) were used as a measure for affinity maturation. e–h Antigen-specific IgG1 levels against CTx (e) and NP (f–h) in the serum were assessed by ELISAs for CTx-specific IgG1 (e), NP20-specific IgG1 (f), high-affinity NP2-specific IgG1 (g) and the ratio of NP2-to-NP20-specific IgG1 antibodies (h). i–n The percentage and number of B220+Ki67+Bcl6+ GC B cells (i, j), CD4+Foxp3-CXCR5+PD-1+ Tfh cells (k, l) and CD4+Foxp3+CXCR5+PD-1+ Tfr cells (m, n) in PPs were quantified by flow cytometry. Bar plots show the combined results of 2 independent experiments with a total of n = 10–13 mice per group. Bar height corresponds to the mean, and each circle represents one biological replicate. P-values were determined using Mann–Whitney tests (a–h) or the Kruskal–Wallis test with Dunn’s multiple testing correction (i–n) in GraphPad Prism6. Source data are provided as a Source Data fileCC BY · PubMed Central

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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
Publisher
Springer Science and Business Media LLC
Published
2019-06-04
Volume
10
Issue
1
Pages
2443-2443
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-019-10430-7
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
FWCI
4.30
Type
journal article
Language
en
Open access
Licence
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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