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Outer Membrane Vesicles of a Human Commensal Mediate Immune Regulation and Disease Protection
Open accessAbstract
Commensal bacteria impact host health and immunity through various mechanisms, including the production of immunomodulatory molecules. Bacteroides fragilis produces a capsular polysaccharide (PSA), which induces regulatory T cells and mucosal tolerance. However, unlike pathogens, which employ secretion systems, the mechanisms by which commensal bacteria deliver molecules to the host remain unknown. We reveal that Bacteroides fragilis releases PSA in outer membrane vesicles (OMVs) that induce immunomodulatory effects and prevent experimental colitis. Dendritic cells (DCs) sense OMV-associated PSA through TLR2, resulting in enhanced regulatory T cells and anti-inflammatory cytokine production. OMV-induced signaling in DCs requires growth arrest and DNA-damage-inducible protein (Gadd45α). DCs treated with PSA-containing OMVs prevent experimental colitis, whereas Gadd45α(-/-) DCs are unable to promote regulatory T cell responses or suppress proinflammatory cytokine production and host pathology. These findings demonstrate that OMV-mediated delivery of a commensal molecule prevents disease, uncovering a mechanism of interkingdom communication between the microbiota and mammals.
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“Furthermore, PSA produced by Leuconostoc mesenteroides strain NTM048 or Bacteroides fragilis acts as an immunostimulant to enhance the mucosal barrier and influence systemic immune responses [111, 112] (Fig. 5G).”
From Gut microbiota influence immunotherapy responses: mechanisms and therapeutic strategies (2022) · cites this paper as [112]
In the citing paper
“some bacterial species have been shown to drive Treg development via alternative pathways dependent on polysaccharide A and TLR signaling to dendritic cells”
From The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy (2018) · cites this paper as Shen et al., 2012
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Bacterial extracellular vesicles in the brain: Pathological effects and therapeutic possibilities
Arenas, Y. M., Izquierdo‐Altarejos, P., Pérez‐Martínez, G., Felipo, V., & Llansola, M. (2025) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-25-00236 · Cited by 3
“There are yet few studies reporting beneficial effects of BEVs on the brain and neurological and neurodegenerative diseases.”
InfluentialA Paradigm Shift in SSTI Management: The Multifunctional Role of Extracellular Vesicles
Barathan, M., & Hanafiah, A. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26136481 · Cited by 3
“OMVs from commensal gut bacteria such as Bacteroides fragilis have been shown to promote the maturation of the immune system and enhance regulatory T cell activation, leading to increased anti-inflammatory cytokine production and prevention of inflammatory disease [190].”
CREB-mediated sensing of bacterial membrane vesicles unveils a conserved host defense pathway
Wang, S., Qi, B., Du, C., Ma, P., Zhang, Y., Chen, S., Tian, E., & Deng, H. (2025) · Mucosal Immunology · doi:10.1016/j.mucimm.2025.08.007 · Cited by 3
Sheikh, A., Scano, C., Xu, J., Ojo, T., Conforti, J. M., Haberman, K. L., King, B., Martinez, A. S., Pujol, M., Watkins, J., et al. (2025) · Journal of Extracellular Biology · doi:10.1002/jex2.70086 · Cited by 3
“…sought to better understand the mechanistic basis for the differential phenotypic effects of OMVs from two strains of the same species of B. fragilis , apart from the genotoxin BFT, observed in previous studies (Zakharzhevskaya, Vanyushkina, et al. 2017; Shen et al. 2012; Shagaleeva et al. 2024).”
Oral–Gut Microbial Crosstalk and Therapeutic Applications of Bacterial Extracellular Vesicles
Fu, W., Yang, N., Yan, J., Han, B., Niu, Q., Li, Z., Bai, R., & Yu, T. (2025) · Biomolecules · doi:10.3390/biom16010026 · Cited by 3
“…dendritic cells (DCs), activating intracellular signaling to promote an anti-inflammatory response, which is implicated in the prevention of colitis [149]; Bacteroides thetaiotaomicron BEVs are able to induce IL-10 expression in colonic DCs and IL-6 and CD80 expression in blood-derived DCs [150].”
Role of exosomes in gastrointestinal physiology and pathophysiology
Wellington, V. N. A., & Singh, S. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1717977 · Cited by 5
From food to vesicle: nutritional influences on gut microbial inflammatory signaling
Verbunt, J., Mennens, L., Jocken, J. W. E., Blaak, E. E., Savelkoul, P. H. M., & Stassen, F. R. M. (2026) · Frontiers in Nutrition · doi:10.3389/fnut.2026.1756462 · Cited by 3
Emerging Therapeutic Approaches for Modulating the Intestinal Microbiota
Cosimato, I., Brescia, A., Franci, G., Casolaro, V., & Folliero, V. (2026) · Pharmaceutics · doi:10.3390/pharmaceutics18020197 · Cited by 4
“Conversely, DCs lacking Gadd45 α are unable to promote the activation of Treg cells or to suppress the production of pro-inflammatory cytokines, rendering them incapable of limiting the progression of the disease [157].”
From Microbial Ecology to Functional Components in Microbe–Host Interactions
Wang, T., Wang, Z., Yang, X., & Zhang, L. (2026) · Biology · doi:10.3390/biology15080635 · Cited by 3
“By carrying LPS, proteins, and nucleic acids, OMVs can engage host immune pathways at low intensity without bacterial invasion, functioning as “remote immunomodulatory” signaling units [162,163].”
Probiotic-derived extracellular vesicles: a novel approach for managing metabolic disorders
Wang, Y., Li, Q., Chen, X., Nie, X., Li, Z., & Xie, J. (2026) · Journal of Future Foods · doi:10.1016/j.jfutfo.2026.04.013 · Cited by 3
Zhou, Z., Shi, Y., Fu, Y., Huang, Y., Song, Y., & Li, C. (2026) · Virulence · doi:10.1080/21505594.2026.2654259 · Cited by 4
“This pattern favors protective immunity without triggering excessive inflammation [107,108](Figure 4).”
Ramadan, Y. N., Bukhari, S. Q., Alatawi, Z., Oriquat, G., Ellah, N. H. A., Mohamedosman, E. H. A., Ahmed, R., & Hetta, . F. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27115009 · Cited by 5
Yang, X., Zhao, Q., Wang, X., Zhang, Y., Ma, J., Liu, Y., & Wang, H. (2025) · Technology and Health Care · doi:10.1177/09287329241301680 · Cited by 3
“Metabolites secreted by different members of the Bacteroides genus can help maintain the stability of the immune system and are key participants in immune regulation.”
Mechanistic insights into postbiotics as therapeutic agents in type 2 diabetes management
Ebadpour, N., Faraji, N., Abavisani, M., Karav, S., & Sahebkar, A. (2025) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-025-04456-6 · Cited by 3
“EVs are spherical bilayers secreted from bacteria that enter the circulation system of the host, performing metabolic and immunological influence (Unal et al. 2011; Shen et al. 2012).”
Jefferis, T., Scano, C., Ashraf, A., Stevens, D., Sevcik, A., Bruce, E. D., Greathouse, K. L., & Sayes, C. M. (2025) · The Journal of Immunology · doi:10.1093/jimmun/vkaf257 · Cited by 3
Immunomodulatory and antiinflammatory mechanisms of probiotics
Freitas, A. D. S., Fernandes, L. J. D. S., Coelho-Rocha, N. D., de Jesus, L. C. L., Rodovalho, V. D. R., da Silva, T. F., Carvalho, R. D. D. O., & Azevedo, V. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85170-1.00019-1 · Cited by 4
Biochemical Features of Beneficial Microbes: Foundations for Therapeutic Microbiology
Engevik, M. A., & Versalovic, J. A. (2018) · ASM Press eBooks · doi:10.1128/9781555819705.ch1 · Cited by 2
Jayathilaka, E. H. T. T., Dias, M. K. H. M., Tennakoon, M. S. B. W. T. M. N. S., Chulhong, O., Nikapitiya, C., Shin, H., & Zoysa, M. D. (2024) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2024.109945 · Cited by 3
The Microbiome–Gut–Brain Axis and the Consequences of Infection and Dysbiosis
Bienenstock, J., Kunze, W., & Forsythe, P. (2016) · The American Journal of Gastroenterology Supplements · doi:10.1038/ajgsup.2016.12 · Cited by 4
Isolation and characterization of Faecalibacterium prausnitzii extracellular vesicles
Jafari, B., Nejad, R. K., Vaziri, F., & Siadat, S. D. (2017) · Vaccine Research · doi:10.29252/vacres.4.3.4.51 · Cited by 3
“This is due to their ability in carrying an extensive range of enzymes used in digestion of polysaccharides, as well as their roles in immunomodulatory functions and signaling pathways [21].”
Cross-Talk between Next-Generation Probiotics and the Immune System
Syromyatnikov, M., Гладких, М. И., Nesterova, E. Y., Kazemzadeh, S., Dmitrievna, M. P., & Korneeva, O. S. (2025) · Biocell · doi:10.32604/biocell.2025.065311 · Cited by 3
Dietz‐Ziegler, S., Kewitz, S., Kaiser, G., Rühle, J., Marmé, A., Dalpke, A. H., Cheaib, B. A., Pauluschke‐Fröhlich, J., Henes, M., Velić, A., et al. (2025) · European Journal of Immunology · doi:10.1002/eji.70056 · Cited by 2
Han, J. M., Lim, J., Kim, W. S., Yoo, B.-G., Jung, J., Lim, S., & Byun, E. (2025) · Antioxidants · doi:10.3390/antiox14091108 · Cited by 3
Sosa, C. D. L., Díaz, F. R. G., Álvarez, H. R., Ruíz, A. V., Higuera-Piedrahita, R. I., de la Crúz-Crúz, H. A., Cuéllar-Ordaz, J. A., Rico, G. R., Negrete‐Abascal, E., Reyes‐López, M., et al. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27062764 · Cited by 2
Kim, Y., Park, N., Cheng, X., & Lee, Y. (2026) · Journal of Controlled Release · doi:10.1016/j.jconrel.2026.114872 · Cited by 3
Gao, X., Wang, W., Sun, M., Zhao, H., Shang, Z., Wong, A. S. T., Wang, Y., Zhao, M., & Liu, D. (2026) · Biomedical Technology · doi:10.1016/j.bmt.2026.100138 · Cited by 2
Zhang, M., Zhao, X., Tang, M., & Zou, W. (2026) · Membranes · doi:10.3390/membranes16060208 · Cited by 2
“PSA-OMV-treated DCs can regulate T cells and suppress inflammation in experimental models, whereas Gadd45 α ( − / − ) DCs fail to modulate T cells or suppress inflammation [105].”
Bacterial Extracellular Vesicles in the Strategic Interplay Between Pathogens and Hosts
Liang, J., Li, M., Xu, J., & Chen, S. (2026) · Microorganisms · doi:10.3390/microorganisms14061362 · Cited by 2
“This is particularly relevant in mucosal niches, where host cells, commensals, probiotics, and invading pathogens coexist in the same ecological space [67,68].”
Analysis of Bacterial Extracellular Vesicles by Immunogold Transmission Electron Microscopy
Pirolli, N. H., & Jay, S. M. (2024) · Methods in molecular biology · doi:10.1007/978-1-0716-4055-5_2 · Cited by 2
Kameli, N., Becker, H. E. F., Jonkers, D. M. A. E., Penders, J., Savelkoul, P. H. M., & Stassen, F. R. M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252313194 · Cited by 2
Proteogenomic annotation of T6SS components identified in Bacteroides fragilis secretome
Zakharzhevskaya, N. B., Shagaleeva, O. Y., Kashatnikova, D. A., Goncharov, A. O., Evsyutina, D. V., Kardonsky, D. A., Vorobeva, E. A., Silantiev, A. S., Kazakova, V. D., Kolesnikova, I. V., et al. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1495971 · Cited by 2
“Polysaccharide A is located on the surface of Bacteroides fragilis (Bf) vesicles, which contribute to immune response suppression during intestinal inflammation (Shen et al., 2012).”
Palanivelu, L., Chen, Y.-Y., Liang, Y., Li, S., Chang, C.-W., Huang, Y.-T., & Lo, Y. (2025) · NeuroImage · doi:10.1016/j.neuroimage.2025.121344 · Cited by 2
Interaction of bacterial extracellular microvesicles with eukaryotic cells.
Shlykova, D. S., Писарев, В. М., Михайлович, Г. А., & Tutelyan, A. V. (2021) · Medical Immunology (Russia) · doi:10.15789/1563-0625-iob-2079 · Cited by 2
Skivka, L. M. (2015) · Biotechnologia Acta · doi:10.15407/biotech8.03.028 · Cited by 2
“Disturbances of intestinal microflora lead to the derangement of alkaline phosphatase biosynthesis and decrease of LPS detoxification [44].”
Metadata
- Authors
- Shen, Y., Torchia, M. L. G., Lawson, G. W., Karp, C. L., Ashwell, J. D., & Mazmanian, S. K.
- Affiliations
- California Institute of Technology (US)
- National Institutes of Health (US)
- University of California, Los Angeles (US)
- Cincinnati Children's Hospital Medical Center (US)
- Corresponding author
- Mazmanian, Sarkis K.
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2012-10
- Volume
- 12
- Issue
- 4
- Pages
- 509-520
- ISSN
- 1931-3128 (ISSN-L)
- PMC
- PMC3895402
- OpenAlex
- W2051349444
- Cited by
- 714
- References
- 41
- Citations by year
- 2026: 59 · 2025: 84 · 2024: 60 · 2023: 61 · 2022: 69 · 2021: 83 · 2020: 61 · 2019: 48 · 2018: 34 · 2017: 40 · 2016: 30 · 2015: 27 · 2014: 33 · 2013: 23 · 2012: 1
- FWCI
- 11.75
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Host & Microbe (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (T32GM007616, GM007616)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 078938, R01DK078938, R21DK083633, R56DK078938)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- 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
- Keywords
- outer membrane vesicles, Bacteroides fragilis, capsular polysaccharide, commensal bacteria, regulatory T cells, dendritic cells, TLR2, GADD45A, experimental colitis, mucosal tolerance, immunomodulation, interkingdom communication, gut microbiota, anti-inflammatory cytokines
- MeSH terms
- GADD45 Proteins, Animals, Bacteroides fragilis, Dendritic Cells, Immunologic Factors, Mice, Inbred BALB C, Mice, Inbred C57BL, Nuclear Proteins, Polysaccharides, Bacterial, Cytokines, Mice, Knockout, Cell Cycle Proteins, Gene Expression Profiling, T-Lymphocytes, Regulatory, Toll-Like Receptor 2, Mice, Exosomes
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