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Longevity in Mice Is Promoted by Probiotic-Induced Suppression of Colonic Senescence Dependent on Upregulation of Gut Bacterial Polyamine Production
Open accessAbstract
BACKGROUND: Chronic low-grade inflammation is recognized as an important factor contributing to senescence and age-related diseases. In mammals, levels of polyamines (PAs) decrease during the ageing process; PAs are known to decrease systemic inflammation by inhibiting inflammatory cytokine synthesis in macrophages. Reductions in intestinal luminal PAs levels have been associated with intestinal barrier dysfunction. The probiotic strain Bifidobacterium animalis subsp. lactis LKM512 is known to increase intestinal luminal PA concentrations. METHODOLOGY/PRINCIPAL FINDINGS: We supplemented the diet of 10-month-old Crj:CD-1 female mice with LKM512 for 11 months, while the controls received no supplementation. Survival rates were compared using Kaplan-Meier survival curves. LKM512-treated mice survived significantly longer than controls (P<0.001); moreover, skin ulcers and tumors were more common in the control mice. We then analyzed inflammatory and intestinal conditions by measuring several markers using HPLC, ELISA, reverse transcription-quantitative PCR, and histological slices. LKM512 mice showed altered 16S rRNA gene expression of several predominant intestinal bacterial groups. The fecal concentrations of PAs, but not of short-chain fatty acids, were significantly higher in LKM512-treated mice (P<0.05). Colonic mucosal function was also better in LKM512 mice, with increased mucus secretion and better maintenance of tight junctions. Changes in gene expression levels were evaluated using the NimbleGen mouse DNA microarray. LKM512 administration also downregulated the expression of ageing-associated and inflammation-associated genes and gene expression levels in 21-month-old LKM512-treated mice resembled those in 10-month-old untreated (younger) mice. CONCLUSION/SIGNIFICANCE: Our study demonstrated increased longevity in mice following probiotic treatment with LKM512, possibly due to the suppression of chronic low-grade inflammation in the colon induced by higher PA levels. This indicates that ingestion of specific probiotics may be an easy approach for improving intestinal health and increasing lifespan. Further studies are required to clarify its effectiveness in humans.
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“Similarly, nutrient supplementation with polyamine preparations containing spermidine or provision of a polyamine-producing gut flora increases longevity in mice (Matsumoto et al., 2011; Soda et al., 2009).”
From The Hallmarks of Aging (2013) · cites this paper as Matsumoto et al., 2011
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“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 [78]
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“B. animalis, a probiotic species positively associated with longevity in mice [78] and negatively correlated with inflammation and human obesity [81]”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [78]
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“Polyamines exhibit numerous beneficial effects including increased longevity, recovery of injured mucosa, as well as favorable effects on cognitive function.122, 123, 124”
From Regulation of Intestinal Barrier Function by Microbial Metabolites (2021) · cites this paper as [124]
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The role of commensal microbes in the lifespan of Drosophila melanogaster
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“For example, Bifidobacterium animalis lactis has promoted longevity and reduced tumor incidence in mice [33], and Lactobacillus salivarius isolated from a centenarian's fecal samples extended the lifespan of C.”
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Zhu, G., Zhao, J., Zhang, H., Wang, G., & Chen, W. (2023) · Advances in Nutrition · doi:10.1016/j.advnut.2023.04.005 · Cited by 78
“lactis LKM512 supplementation effectively ameliorated age-related colonic inflammation by upregulating polyamine production in the intestinal lumen [108].”
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“Frontiers in Immunology 02 regulation of inflammation-related genes and the improvement of intestinal barrier function (22, 23).”
BackgroundMolecular interactions between the intestinal microbiota and the host
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“Spermidine, synthesized by B. lactis, has been shown to have antimutagenic effects and is promising in decreasing colon mutagenesis or tumorigenesis in humans (Table S1) (Matsumoto & Benno, 2004; Matsumoto et al., 2011).”
BackgroundIdentifying Molecular Targets of Lifestyle Modifications in Colon Cancer Prevention
Derry, M. M., Raina, K., Agarwal, C., & Agarwal, R. (2013) · Frontiers in Oncology · doi:10.3389/fonc.2013.00119 · Cited by 71
“Bifidobacterium animalis also increases polyamine concentrations and has been shown to alter IGF-1 expression (Matsumoto et al., 2011).”
BackgroundHost and microbiota metabolic signals in aging and longevity
Zhou, Y., Hu, G., & Wang, M. C. (2021) · Nature Chemical Biology · doi:10.1038/s41589-021-00837-z · Cited by 70
Calorie Restriction Mimetics: Upstream-Type Compounds for Modulating Glucose Metabolism
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“Longevity in mice has been shown to be promoted by gut bacterial polyamine production [58].”
BackgroundSelf-citationPharmacological potential of biogenic amine–polyamine interactions beyond neurotransmission
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“On one hand, anti-ageing and anti-inflammatory effects of microbiotaproduced polyamines have been reported (Li et al., 2001; Matsumoto et al., 2011).”
BackgroundBioengineered Systems and Designer Matrices That Recapitulate the Intestinal Stem Cell Niche
Wang, Y., Kim, R., Hinman, S. S., Zwarycz, B., Magness, S. T., & Allbritton, N. L. (2018) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2018.01.008 · Cited by 73
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“Polyamine possesses not only antioxidant activity [22, 23] but also anti-inflammatory activity [24, 25] and the ability to enhance cell proliferation [26], provide protection against damaging radiation [27], and promote longevity [28, 29].”
A Novel Putrescine Exporter SapBCDF of Escherichia coli
Sugiyama, Y., Nakamura, A., Matsumoto, M., Kanbe, A., Sakanaka, M., Higashi, K., Igarashi, K., Katayama, T., Suzuki, H., & Kurihara, S. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.762450 · Cited by 64
“However, up-regulation of colonic luminal polyamines produced by the intestinal microbiota delays senescence in mice (11, 12).”
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“lactis LKM12 compared to control mice, possibly due to the anti-inflammatory effects of polyamines produced by the bacteria (8).”
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Celiberto, L. S., Bedani, R., Rossi, E. A., & Cavallini, D. (2015) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2014.941457 · Cited by 67
“Matsumoto et al. (2011) used the same organism, B. lactis LKM512, to study longevity in mice.”
MethodGut microbiota and anti-aging: Focusing on spermidine
Yu, L., Pan, J., Guo, M., Duan, H., Zhang, H., Narbad, A., Zhai, Q., Tian, F., & Chen, W. (2023) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2023.2224867 · Cited by 63
“This was further confirmed by animal experiments in which mice supplemented with LKM512 showed a significant increase in fecal polyamine concentrations, enhanced gut mucosal function, and down-regulated expression of genes associated to aging and inflammation (Matsumoto et al. 2011).”
Gut microbial metabolites and its impact on human health
Rahman, S. (2023) · Annals of Gastroenterology · doi:10.20524/aog.2023.0809 · Cited by 70
“Recent epidemiological studies have demonstrated a decrease in cardiovascular events and mortality with an increased PA intake, specifically spermidine [76-78].”
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“Middle-aged mice that were supplemented with Bifidobacterium animalis showed decreased colon permeability, extended lifespan, and improved quality of life (21).”
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The aging mouse microbiome has obesogenic characteristics
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“Another study also reported that the administration of LKM512 in Crj:CD-1 mice increased longevity by augmenting intestinal polyamine levels (44).”
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“Supplementation with spermidine increased lifespan in yeast, worms, flies, and human cells, and a polyamine-rich diet (as well as probiotics that induce polyamine production) decreased mortality in mice [73,74].”
BackgroundProbiotic bacteria as modulators of cellular senescence: emerging concepts and opportunities
Sharma, R., & Padwad, Y. S. (2019) · Gut Microbes · doi:10.1080/19490976.2019.1697148 · Cited by 56
“lactis LKM512, Matsumoto et al.(74) observed a higher survival rate and reduced incidence of skin ulcers and tumors in probiotic fed mice as compared to control.”
BackgroundHealth-Promoting Effects of Dietary Polyamines
Hirano, R., Shirasawa, H., & Kurihara, S. (2021) · Medical Sciences · doi:10.3390/medsci9010008 · Cited by 60
“lactis LKM512 in mice increased polyamines levels in the intestine and significantly extended the lifespan, which was associated with the downregulation of inflammation-associated genes and improvement of the intestinal barrier function [17].”
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BackgroundProbiotics: Comprehensive Exploration of the Growth Promotion Mechanisms in Shrimps
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“Mice fed diets supplemented with Lactobacillus as a probiotic not only showed no pathogenic response, but also lived longer than littermates on a standard diet [9].”
Long-term treatment with spermidine increases health span of middle-aged Sprague-Dawley male rats
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“It is likely that at a younger age, the requirements for biogenic amines are higher due to growth and the decrease of their content thereafter seems positive for longevity, as their excess is detrimental and relates to tumors and deleterious effects of aging (Matsumoto et al. 2011).”
BackgroundAnnotation-free discovery of functional groups in microbial communities
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“The ability of probiotics to extend the life span in mice depends on bacterial-derived putrescine to inhibit colonic cell senescence (17).”
BackgroundInfluential
Metadata
- Authors
- Matsumoto, M., Kurihara, S., Kibe, R., Ashida, H., & Benno, Y.
- Affiliations
- RIKEN (JP)
- Kyoto University (JP)
- Corresponding author
- Matsumoto, Mitsuharu
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-08-16
- Volume
- 6
- Issue
- 8
- Pages
- e23652
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3156754
- OpenAlex
- W2164188362
- Cited by
- 290
- References
- 60
- Citations by year
- 2026: 10 · 2025: 30 · 2024: 19 · 2023: 27 · 2022: 29 · 2021: 38 · 2020: 15 · 2019: 25 · 2018: 23 · 2017: 16 · 2016: 10 · 2015: 8 · 2014: 18 · 2013: 14 · 2012: 8
- FWCI
- 18.71
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- probiotics, polyamines, longevity, lifespan extension, low-grade inflammation, gut microbiota, intestinal barrier function, mucus secretion, tight junctions, skin ulcers
- MeSH terms
- Animals, Bacteria, Bifidobacterium, Colon, Feces, Female, Longevity, Mice, Inbred ICR, Mucus, Neoplasms, Polyamines, RNA, Ribosomal, 16S, Skin Ulcer, Spermine, Gene Expression Regulation, Bacterial, Cellular Senescence, Tight Junctions, Probiotics, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Mice, Kaplan-Meier Estimate
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