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Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice
Open accessAbstract
The gut microbiome is emerging as a key regulator of several metabolic, immune and neuroendocrine pathways 1,2. Gut microbiome deregulation has been implicated in major conditions such as obesity, type 2 diabetes, cardiovascular disease, non-alcoholic fatty acid liver disease and cancer 3-6, but its precise role in aging remains to be elucidated. Here, we find that two different mouse models of progeria are characterized by intestinal dysbiosis with alterations that include an increase in the abundance of Proteobacteria and Cyanobacteria, and a decrease in the abundance of Verrucomicrobia. Consistent with these findings, we found that human progeria patients also display intestinal dysbiosis and that long-lived humans (that is, centenarians) exhibit a substantial increase in Verrucomicrobia and a reduction in Proteobacteria. Fecal microbiota transplantation from wild-type mice enhanced healthspan and lifespan in both progeroid mouse models, and transplantation with the verrucomicrobia Akkermansia muciniphila was sufficient to exert beneficial effects. Moreover, metabolomic analysis of ileal content points to the restoration of secondary bile acids as a possible mechanism for the beneficial effects of reestablishing a healthy microbiome. Our results demonstrate that correction of the accelerated aging-associated intestinal dysbiosis is beneficial, suggesting the existence of a link between aging and the gut microbiota that provides a rationale for microbiome-based interventions against age-related diseases.
Overview
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TL;DR
Fecal microbiota transplantation from wild-type donors into progeroid mice extends healthspan and lifespan, while progeroid microbiota can induce metabolic alterations in wild-type recipients. The study links progeria-associated gut dysbiosis to loss of Akkermansia and altered bile acid metabolism, with A. muciniphila supplementation modestly extending lifespan in progeroid mice.
Key findings
- Progeroid mouse models and human progeria patients show intestinal dysbiosis; Lmna G609G/G609G mice at 4 months lose Akkermansia and show increased Enterobacteriaceae, while centenarians have higher Akkermansia, Ruminococcaceae, Christensenellaceae, and Enterobacteriaceae.
- FMT from WT donors into Lmna G609G/G609G mice improved survival (P = 0.0029), with a 13.5% increase in median lifespan (160 vs 141 days) and 9% extended maximal survival (P = 0.04); FMT from old progeroid donors reduced survival (P = 0.045; median 129 days).
- FMT from WT donors into Zmpste24−/− mice enhanced survival (P = 0.0092), with a 13.4% median lifespan increase (279 vs 246 days) and almost 8% maximal survival increase (P = 0.09).
- Oral A. muciniphila supplementation in Lmna G609G/G609G mice modestly extended lifespan (P = 0.016), induced ileal Reg3g and Tff3, thickened intestinal mucosa, and FMT restored depleted secondary bile acids and metabolites including arabinose, ribose, inosine, and PCae(18:0).
Methods
- Gut metagenomic profiling by 16S rRNA V3–V4 sequencing in Lmna G609G/G609G and Zmpste24−/− mice, human HGPS/NGPS families, centenarians (n = 17) and healthy controls (n = 14), using QIIME 2/DADA2, LEfSe, PICRUSt, and HUMAnN2.
- FMT experiments: antibiotic cocktail followed by oral gavage of microbiome suspensions from WT or old progeroid donors into progeroid or WT mice, with assessment of survival, body weight/temperature, glucose, histology, and calorimetry.
- A. muciniphila culture and oral gavage; metabolomic profiling of ileal content by GC-MS and UHPLC-MS; survival analyzed by Kaplan-Meier log-rank tests and maximal survival by Fisher’s exact test at the 80th percentile.
Limitations
- The paper states that human progeria samples were low in number and that environment may have more influence on the gut microbiome than the pathological condition.
- The paper states that future work is needed to identify the functional mechanisms by which specific bacterial species and metabolites mediate the healthspan and lifespan extension conferred by FMT, and to explore applicability in normal or accelerated aging.
- Evident from the text: human progeria analyses included only four HGPS children and one NGPS patient with siblings, and the centenarian cohort was small (17 centenarians vs 14 controls), limiting generalizability; the study also notes a possible beneficial effect of the FMT protocol per se in old-donor transplanted progeroid mice.
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Claims the paper makes
56 Own result · 19 Not checked yet · 8 Own method · 3 Own interpretation · 1 No basis given
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Analysis of centenarians and progeria mouse models point to a beneficial role for the genus Akkermansia, as oral gavage of Akkermansia muciniphila extends the lifespan of progeroid mice.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
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In the paper
“In turn, the microbiota of centenarians is characterized by the presence of both pathological-and healthassociated bacterial genera.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“We show that fecal microbiota transplantation (FMT) from wild-type (WT) donors to progeroid recipients attenuates the accelerated-aging phenotype and increases survival, whereas FMT from progeroid donors to WT recipients induces metabolic alterations.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“At a lower taxonomical level, Lmna G609G/G609G 4mo mice showed a loss in Clostridiaceae, Allobaculum, Sutterella, Dehalobacterium, Rikenella and Akkermansia (Fig. 1d).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
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In the paper
“However, when samples were compared by geographical location (i.e., comparing families), a differential clustering was observed at the quantitative (Fig. 2b) and qualitative levels (Extended Data Fig. 4e).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“We show that fecal microbiota transplantation (FMT) from wild-type (WT) donors to progeroid recipients attenuates the accelerated-aging phenotype and increases survival, whereas FMT from progeroid donors to WT recipients induces metabolic alterations.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
boosteddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“By contrast, Lmna G609G/G609G 4mo exhibited an increment in Mucispirillum, Enterococcus, Acinetobacter, Staphylococcus, Parabacteroides, Bacteroides, Prevotella and Enterobacteriaceae, which contains the genus Escherichia and has been associated with dysbiosis and intestinal inflammation 20 (Fig. 1d).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
What the sources say
- Not checked yetcites [20] Maharshak, N. et al. Altered enteric microbiota ecology in interleukin 10-deficient mice during development and progression of intestinal inflammation. Gut Microbes 4, 316–324 (2013). source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Zmpste24 -/-mice also showed a tendency to a lower amount of Verrucomicrobia (Extended Data Fig. 3e), although this trend was less marked than in Lmna G609G/G609G animals, perhaps due to the later onset of the progeroid phenotype in Zmpste24 -/-mice.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“We show that fecal microbiota transplantation (FMT) from wild-type (WT) donors to progeroid recipients attenuates the accelerated-aging phenotype and increases survival, whereas FMT from progeroid donors to WT recipients induces metabolic alterations.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“We found intestinal dysbiosis in both mouse models and progeria patients.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
plaincorrelational- Asserted: passes — The authors put it forward as true.
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- It may state two separate claims as one. 34
- Probably not a substantial claim. 18
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In the paper
“We noted a similar profile for WT and Lmna G609G/G609G mice at 1 month of age (Fig. 1b and Extended Data Fig. 2a), observing solely an increment in the genera Allobaculum from the family Erysipelotrichaceae, Desulfovibrio (class deltaproteobacteria) and Clostridiales of the families Ruminococcaceae and Lachnospiraceae, in Lmna G609G/G609G 1mo (Extended Data Fig. 2b).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
plain- Asserted: passes — The authors put it forward as true.
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“When comparing progeria patients with their healthy controls, we found no differences in alpha-diversity (Extended Data Fig. 4b,c) or beta-diversity indices (Fig. 2a and Extended Data Fig. 4d).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plainn = 4- Asserted: passes — The authors put it forward as true.
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In the paper
“The gut microbiome of a fraction of WT 22mo exhibited a tendency towards intestinal dysbiosis (Extended Data Fig. 2a); however, the only significant shift consisted in the loss in Rikenella (Extended Data Fig. 2e), a change also found when comparing Lmna G609G/G609G 4mo to WT 4mo mice (Fig. 1d).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Similar differences were revealed by hierarchical clustering, where Lmna G609G/G609G 4mo mice were grouped together and separated from all other groups (Extended Data Fig. 1e,f).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Although Zmpste24 -/-mice showed no differences in bacterial diversity (Extended Data Fig. 3b), they exhibited higher bacterial richness (Extended Data Fig. 3c).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“LEfSe analysis detected an increase in KEGG pathways related to pathological bacteria such as 'Bacterial invasion of epithelial cells' (ko05100) and 'Flagellar assembly' (ko02040), and a differential enrichment in multiple metabolic pathways (Extended Data Fig. 2f and Supplemental Table S3).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Like Lmna G609G/G609G mice, Zmpste24 -/-animals showed differences in beta diversity at the quantitative (Fig. 1f) and qualitative level (Extended Data Fig. 3d), clustering differently from WT mice, and exhibited signs of dysbiosis (Fig. 1g, Extended Data Fig. 3e) with a high abundance of Proteobacteria (class Alphaproteobacteria) and Cyanobacteria (Fig. 1g, Extended Data Fig. 3e and Supplementary”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
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In the paper
“Alterations in the gut microbiome in progeria patients and long-lived humans.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Metabolomic analysis
plaincorrelationaln = 5- Asserted: passes — The authors put it forward as true.
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In the paper
“(b) family (P = 0.001, PERMANOVA) (Family A, n = 3; Family B, n = 3; Family C, n = 3; Family D, n = 2; Family E, n = 3).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Metabolomic analysis
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Body weight loss (Fig. 3m and Extended Data Fig. 8a) and hypoglycemia (Fig. 3n) were avoided in Zmpste24 -/--WTmic mice.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Most importantly, Lmna G609G/G609G -WTmic showed improved survival compared to control Lmna G609G/G609G mice (P = 0.0029), with a 13.5% increase in median lifespan (160 vs 141 days, respectively) (Fig. 3f).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“G609G 4mo mice show statistical differences with each of the other groups (see Supplementary Table 1).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Metabolomic analysis
plaincorrelationaln = 9 ·- Asserted: passes — The authors put it forward as true.
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In the paper
“We also noted an increase in intestinal inflammation markers in Lmna G609G/G609G mice that was recovered in Lmna G609G/G609G -WTmic (Extended Data Fig. 6d).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“In contrast, Lmna G609G/G609G -oG609Gmic showed reduced survival compared to control Lmna G609G/G609G mice (P = 0.045), with a reduction in median lifespan (129 days) (Fig. 3f).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“As recently described 28 , different bile acids were decreased in Lmna G609G/G609G compared to WT mice, and recovered in Lmna G609G/G609G -WTmic (Fig. 4e).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
What the sources say
- Not checked yetcites [28] Barcena, C. et al. Methionine restriction extends lifespan in progeroid mice and alters lipid and bile acid metabolism. Cell Rep. 24, 2392–2403 (2018). source
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Centenarians showed lower alpha-diversity compared to their controls (Extended Data Fig. 5b), and a considerably lower bacterial richness (Extended Data Fig. 5c).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“However, this maneuver caused metabolic alterations, including a higher body weight, higher glucose levels, lower O2 consumption, lower CO2 production and reduced energy expenditure (Fig. 3g-k and Extended Data Fig. 7a-d).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“(e) Validation using qPCR of the differences in abundance of E. coli (W = 6, P = 0.0046) and A. muciniphila (W = 52, P = 0.03) between WT (n = 8) and G609G mice (n = 8) at 10 weeks of age.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Metabolomic analysis
plaincorrelationaln = 8 ·- Asserted: passes — The authors put it forward as true.
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In the paper
“At a lower taxonomic level, centenarians were characterized by a lower abundance of Desulfovibrionaceae, Lachnospiraceae and Erysipelotrichaceaethe last two enriched in progeria patientsand Prevotella, Sutterella, Roseburia, or Butyricicoccus, among other differences (Fig. 2f).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“however, the changes from 1 to 4 months were more profound in progeroid mice, displaying a loss in Akkermansia and Dehalobacterium and an enrichment in Parabacteroides, Prevotella and the Enterobacteriaceae, among other differences (Extended Data Fig. 2d).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Metabolomic analysis
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“This manipulation caused Zmpste24 -/- mice to manifest a less pronounced cervicothoracic lordokyphosis, larger body size and maintained grooming (Fig. 3l).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Spleen weight, typically reduced in progeroid mice, was similar in Lmna G609G/G609G -WTmic and Lmna G609G/G609G controls, but lower in Lmna G609G/G609G -oG609Gmic (Extended Data Fig. 6c).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“LEfSe analysis pointed to a loss in Gemmiger -family Ruminococcaceae-and an enrichment in Clostridium from families Erysipelotrichaceae and Lachnospiraceae in progeria patients (Fig. 2c).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaincorrelationaln = 4- Asserted: passes — The authors put it forward as true.
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In the paper
“LEfSe analysis showed that centenarians presented less Betaproteobacteria and more Synergistia and Verrucomicrobiae, among others (Fig. 2e and Supplementary Table 2).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaincorrelational- Asserted: passes — The authors put it forward as true.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Like Lmna G609G/G609G mice transplanted with WT microbiota, Zmpste24 -/--WTmic mice also exhibited enhanced survival (P = 0.0092), with a median lifespan increase of 13.4% (279 vs 246 days) (Fig. 3o).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“(b) Relative expression levels of Reg3g and Tff3 in G609G (n = 8) and AKK (n = 7) mice.Differences were analyzed with an unpaired two-tailed Student's t-test.For Reg3g, t = 2.33, df = 13, P = 0.0365; for Tff3, t = 2.42, df = 13, P = 0.0306.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Metabolomic analysis
plainn = 8 ·- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“In mammals, the gut microbiota is involved in food processing, activation of satiety pathways, protection against pathogens, and production of metabolites including vitamins, short chain fatty acids and secondary bile acids [8][9][10] .”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
What the sources say
- Not checked yetcites [8] Rios-Covian, D. et al. Intestinal short chain fatty acids and their link with diet and human health. Front. Microbiol. 7, 185 (2016). source
- Not checked yetcites [9] Breton, J. et al. Gut commensal E. coli proteins activate host satiety pathways following nutrient-induced bacterial growth. Cell Metab. 23, 324–334 (2016). source
- Not checked yetcites [10] Wahlstrom, A., Sayin, S. I., Marschall, H. U. & Backhed, F. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab. 24, 41–50 (2016). source
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“It is now known that the microbiota has essential metabolic and immunological functions conserved from worms 7 to humans 1,2 .”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
What the sources say
- Not checked yetcites [1] Thaiss, C. A., Zmora, N., Levy, M. & Elinav, E. The microbiome and innate immunity. Nature 535, 65–74 (2016). source
- Not checked yetcites [2] Leulier, F. et al. Integrative physiology: at the crossroads of nutrition, microbiota, animal physiology and human health. Cell Metab. 25, 522–534 (2017). source
boosteddirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“The gut microbiota also signals to distant organs, contributing to the maintenance of host physiology 11 .”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
What the sources say
- Not checked yetcites [11] Schroeder, B. O. & Backhed, F. Signals from the gut microbiota to distant organs in physiology and disease. Nat. Med. 22, 1079–1089 (2016). source
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
None of the sources cited for this claim have been checked yet.
In the paper
“Intestinal microbiota alterations are associated with major conditions like obesity, type-2 diabetes, cardiovascular disease, non-alcoholic fatty acid liver disease, cancer, and the response to antineoplastic therapy [3][4][5][6] .”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
What the sources say
- Not checked yetcites [3] Koeth, R. A. et al. Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 19, 576–585 (2013). source
- Not checked yetcites [4] Loomba, R. et al. Gut microbiome-based metagenomic signature for non-invasive detection of advanced fibrosis in human nonalcoholic fatty liver disease. Cell Metab. 25, 1054–1062 (2017). source
- Not checked yetcites [5] Qin, J. et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490, 55–60 (2012). source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The promising in vivo results obtained in this study suggest that therapeutic interventions on the intestinal microbiome may lead to healthspan end even lifespan improvements.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
hedgedconditional- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“These results are in line with previous studies reporting high levels of Akkermansia and Christensenellaceae and low levels of Roseburia in centenarians 12,24 .”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
What the sources say
plaincorrelational- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Of note, secondary bile acids are produced by the gut microbiota 38 and positively correlate with Akkermansia levels in mice 39 .”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
What the sources say
- Not checked yetcites [38] de Aguiar Vallim, T. Q., Tarling, E. J. & Edwards, P. A. Pleiotropic roles of bile acids in metabolism. Cell Metab. 17, 657–669 (2013). source
- Not checked yetcites [39] Pierre, J. F. et al. Activation of bile acid signaling improves metabolic phenotypes in high-fat diet-induced obese mice. Am. J. Physiol. Gastrointest. Liver Physiol. 311, G286–G304 (2016). source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“Considering that bile acids regulate metabolism and anti-inflammatory signals 40 and that they are depleted in Lmna G609G/G609G mice 28 , the restoration of secondary bile acidsand other metabolites (arabinose, ribose, inosine)by FMT might contribute to extend healthspan and lifespan in progeroid mice (Fig. 4g).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
What the sources say
- Not checked yetcites [40] Postler, T. S. & Ghosh, S. Understanding the holobiont: how microbial metabolites affect human health and shape the immune system. Cell Metab. 26, 110–130 (2017). source
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Of note, high abundance of Akkermansia has been associated with improved immunomodulation and metabolic homeostasis, reduced inflammation, and protection against atherosclerosis [17][18][19] .”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
What the sources say
- Not checked yetcites [17] Plovier, H. et al. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat. Med. 23, 107–113 (2017). source
- Not checked yetcites [18] Schneeberger, M. et al. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci. Rep. 5, 16643 (2015). source
- Not checked yetcites [19] Everard, A. et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl Acad. Sci. USA 110, 9066–9071 (2013). source
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Previous studies have described that successful FMT treatment of recurrent infection by C. difficile relies on restoration of correct bile acid metabolism 35,36 , and that antibioticinduced microbiome depletion reduces the secondary bile acid pool 37 .”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
What the sources say
- Not checked yetcites [35] Weingarden, A. R. et al. Microbiota transplantation restores normal fecal bile acid composition in recurrent Clostridium difficile infection. Am. J. Physiol. Gastrointest. Liver Physiol. 306, G310–G319 (2014). source
- Not checked yetcites [36] Buffie, C. G. et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 517, 205–208 (2015). source
- Not checked yetcites [37] Zarrinpar, A. et al. Antibiotic-induced microbiome depletion alters metabolic homeostasis by affecting gut signaling and colonic metabolism. Nat. Commun. 9, 2872 (2018). source
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
In the paper
“By contrast, Lmna G609G/G609G 4mo exhibited an increment in Mucispirillum, Enterococcus, Acinetobacter, Staphylococcus, Parabacteroides, Bacteroides, Prevotella and Enterobacteriaceae, which contains the genus Escherichia and has been associated with dysbiosis and intestinal inflammation 20 (Fig. 1d).”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Abstract
What the sources say
- Not checked yetcites [20] Maharshak, N. et al. Altered enteric microbiota ecology in interleukin 10-deficient mice during development and progression of intestinal inflammation. Gut Microbes 4, 316–324 (2013). source
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“FMT might modulate obesity and metabolism in humans and mice 29,30 , ameliorate metabolic syndrome in patients 31 , and contribute to the treatment of refractory immune checkpoint inhibitor (ICI)-associated colitis 32 and recurrent infections by Clostridium difficile 33 .”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Lmna G609G/G609G 4mo mice.
What the sources say
- Not checked yetcites [29] Ridaura, V. K. et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341, 1241214 (2013). source
- Not checked yetcites [30] Cox, L. M. et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158, 705–721 (2014). source
- Not checked yetcites [31] Vrieze, A. et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143, 913–916 (2012). source
- Not checked yetcites [32] Wang, Y. et al. Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis. Nat. Med. 24, 1804–1808 (2018). source
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“This QC sample was re-injected in each batch to monitor and correct analytical bias.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Additional information
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“Differentially expressed metabolites in each condition were identified using moderate t-statistic implemented in the R/Bioconductor package limma 46 , using sex as a covariate.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Additional information
What the sources say
- Not checked yetcites [46] Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015). source
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Normalization was performed by correcting the area of the MS picks across the batches using the QC pooled samples and by centering their values around the mean of the QC areas.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Additional information
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Research involving humans was approved by the Ethical Committee of Regional Clinical Research of the Principality of Asturias, project no.105/16.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Additional information
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Number of mice allocated per group was based on previous experiments and their distribution was randomized, being indicated in each Figure legend.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Additional information
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“All participants read and signed an informed consent.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Additional information
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
The paper relies on this without support.
No alterations in the gut microbiome have been described in accelerated aging syndromes.
“Although some works have explored the microbiome profile of long-lived humans 12,13 , no alterations have been described in accelerated aging syndromes.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Studies in the past decade have demonstrated that gut microbiome composition changes with age, that exceptionally long-lived individuals have a different microbiome composition from average older adults131–133, and that certain microorganisms131,134,135 and the metabolites they produce132,134,136 are beneficial to human health.”
From Measuring biological age using omics data (2022) · cites this paper as [134]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“two different mouse models of progeria exhibit intestinal dysbiosis mainly characterized by an increase in the abundance of Proteobacteria and Cyanobacteria, and a decrease in levels of Verrucomicrobia.”
From Hallmarks of aging: An expanding universe (2023) · cites this paper as [285]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Restoration of secondary bile acids and other metabolites depleted in progeroid mice phenocopied the beneficial effects of reestablishing a healthy microbiome 285”
From Hallmarks of aging: An expanding universe (2023) · cites this paper as [285]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“administration of the verrucomicrobium Akkermansia muciniphila was also sufficient to obtain such effects.”
From Hallmarks of aging: An expanding universe (2023) · cites this paper as [285]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“| | HGPS mouse | Fecal microbiota transplantation from wt mice; Akkermansia muciniphila administration | Enhanced healthspan and lifespan | 285 |”
From Hallmarks of aging: An expanding universe (2023) · cites this paper as [285]
Experimental — accuracy not yet measured
The cited source says what the claim attributes to it.
In the citing paper
“FMT from wild-type to progeroid mice recipients enhanced healthspan and lifespan in both accelerated-aging models”
From Hallmarks of aging: An expanding universe (2023) · cites this paper as [285]
The cited source says what the claim attributes to it.
In the citing paper
“FMT from progeroid donors to wild-type recipients induced detrimental metabolic alterations.”
From Hallmarks of aging: An expanding universe (2023) · cites this paper as [285]
In the citing paper
“Many studies have shown that Akkermansia can effectively improve symptoms in mouse models of diseases such as ALS [34], progeria [35], and chronic colitis [36] by promoting healing and recovery of intestinal mucosal layer and reducing the expression of proinflammatory cytokines such as TNF-α and interferon gamma (IFN-γ) in the colon.”
From Neuroprotective Effect of Ceftriaxone on MPTP‐Induced Parkinson’s Disease Mouse Model by Regulating Inflammation and Intestinal Microbiota (2021) · cites this paper as [35]
In the citing paper
“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 [8]
In the citing paper
“Members of the Bifidobacteriaceae, Akkermansiaceae, and Eubacteriaceae families that are associated with beneficial effects on intestinal and extra-intestinal health in both mice and humans”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [8]
In the citing paper
“and are associated with promoting intestinal and extra-intestinal health and healthy aging.”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [8]
In the citing paper
“In mouse models of accelerated aging, supplementation with A. muciniphila can also attenuate age-related decline in colon thickness and immune activation [73], and exert beneficial effects on lifespan and healthspan [8].”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [8]
In the citing paper
“oral administration of Akkermansia species not only improves cancer immunosurveillance in tumor-bearing mice but also prolongs lifespan in progeroid mice 57”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [57]
In the citing paper
“oral administration of Akkermansia species not only improves cancer immunosurveillance in tumor-bearing mice but also prolongs lifespan in progeroid mice 57”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [57]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Rated major: it would touch a result — a value a result rests on, reported and recomputed p-values on opposite sides of the significance level, two passages that conflict with no sign which is right, or a cited work retracted before this paper was published.
In the paper
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Akkermansia muciniphila culture and oral supplementation
“Lmna G609G/G609G mice were treated by oral gavage with 100 L of either Akkermansia suspension (AKK group, n = 9) or anaerobic PBS (control group, n=12) three days a week beginning at 12 weeks of age and until decease.”
§ Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice > Metabolomic analysis
“A. muciniphila transplantation was performed starting at 7-8 weeks of age.”
Citations
Cites
limma powers differential expression analyses for RNA-sequencing and microarray studies
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Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis
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Gut Microbiota from Twins Discordant for Obesity Modulate Metabolism in Mice
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Duodenal Infusion of Donor Feces for Recurrent Clostridium difficile
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Cited by
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Liu, Y., He, Y., Fan, S., Gong, X., Zhou, Y., Jian, Y., Ouyang, J., Jiang, Q., & Zhang, P. (2023) · Animals · doi:10.3390/ani13233731 · Cited by 9
Structural characteristics of gut microbiota in longevity from Changshou town, Hubei, China
Ai, X., Liu, Y., Shi, J., Xie, X., Li, L., Duan, R., Lv, Y., Xiong, K., Miao, Y., & Zhang, Y. (2024) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-024-13140-3 · Cited by 9
Guo, J., Cao, Y., Zhang, T., Xu, C., Liu, Z., Li, W., & Wang, Q. (2024) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s459891 · Cited by 8
Ma, X., Fan, M., Hannachi, K., Qian, H., Li, Y., & Li, Y. (2024) · Food Research International · doi:10.1016/j.foodres.2024.115381 · Cited by 9
Zhang, S., Mao, X., Chang, L., Li, M., Wei, C., Li, H., Shen, X., Niu, K., Zhang, R., Jiang, Y., et al. (2025) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2025.119944 · Cited by 8
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Metadata
- Authors
- Bárcena, C., Valdés-Mas, R., Mayoral, P., Garabaya, C., Durand, S., Rodríguez, F., Fernández-García, M. T., Salazar, N., Nogacka, A. M., Garatachea, N., Bossut, N., Aprahamian, F., Lucia, A., Kroemer, G., Freije, J. M. P., Quirós, P. M., & López-Otín, C.
- Affiliations
- Universidad de Oviedo (ES)
- Inserm (FR)
- Consejo Superior de Investigaciones Científicas (ES)
- Universidad de Zaragoza (ES)
- Karolinska University Hospital (SE)
- Corresponding author
- Quirós, Pedro M.
- ORCID
- Venue
- Nature Medicine
- Published
- 2019-07-22
- Volume
- 25
- Issue
- 8
- Pages
- 1234-1242
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- OpenAlex
- W2963531283
- Cited by
- 661
- References
- 49
- Citations by year
- 2026: 78 · 2025: 110 · 2024: 124 · 2023: 90 · 2022: 95 · 2021: 86 · 2020: 65 · 2019: 12
- FWCI
- 22.10
- Type
- journal article
- Language
- en
- Open access
- green
- hal.science
- Licence
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by-nc-nd)
- ABACUS. Repositorio de Producción Científica (Universidad Europea) (submittedVersion)
- Consultation of the Doctoral Thesis Database (TESEO) (Ministerio de Educación, Cultura y Deporte) (submittedVersion, cc-by-nc-nd)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- Funders
- Agence Nationale de la Recherche (ANR-16-ECVD-0008)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- fecal microbiota transplantation, gut microbiota, aging, healthspan, lifespan extension, Hutchinson-Gilford progeria syndrome, gut dysbiosis, Akkermansia muciniphila, Verrucomicrobia, Proteobacteria, centenarians, secondary bile acids, microbiota-targeted interventions
- MeSH terms
- Gastrointestinal Microbiome, Fecal Microbiota Transplantation, Animals, Disease Models, Animal, Female, Humans, Longevity, Male, Mice, Inbred C57BL, Progeria, Mice, Metabolomics, Dysbiosis
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