Induction of Intestinal Th17 Cells by Segmented Filamentous Bacteria
Open accessAbstract
The gastrointestinal tract of mammals is inhabited by hundreds of distinct species of commensal microorganisms that exist in a mutualistic relationship with the host. How commensal microbiota influence the host immune system is poorly understood. We show here that colonization of the small intestine of mice with a single commensal microbe, segmented filamentous bacterium (SFB), is sufficient to induce the appearance of CD4(+) T helper cells that produce IL-17 and IL-22 (Th17 cells) in the lamina propria. SFB adhere tightly to the surface of epithelial cells in the terminal ileum of mice with Th17 cells but are absent from mice that have few Th17 cells. Colonization with SFB was correlated with increased expression of genes associated with inflammation and antimicrobial defenses and resulted in enhanced resistance to the intestinal pathogen Citrobacter rodentium. Thus, manipulation of this commensal-regulated pathway may provide new opportunities for enhancing mucosal immunity and treating autoimmune disease.
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Segmented filamentous bacteria fail to induce MAIT cells in GF mice.
“Segmented filamentous bacteria (SFB), a known inducer of Th17 cells that lacks riboflavin synthesis enzymes (Figs. 1J & S1G) (29, 30), also failed to induce MAIT cells (Fig. 1K).”
From MAIT cells are imprinted by the microbiota in early life and promote tissue repair (2019) · cites this paper as [29]
Th17 cells mediate tissue homeostasis by protecting mucosal barriers, influencing commensal microbiota, and modulating epithelial permeability.
“Th17 cells, besides being highly pathogenic and able to induce autoimmunity, have also been implicated in mediating tissue homeostasis, regulating tissue integrity by protecting mucosal barriers from potentially invasive microbes”
From TH17 cell heterogeneity and its role in tissue inflammation (2023) · cites this paper as [47]
Th17 cells play an important role in tissue homeostasis, especially in the intestinal mucosa.
“Th17 cells have been found to play an important role in tissue homeostasis, especially in the intestinal mucosa.”
From TH17 cell heterogeneity and its role in tissue inflammation (2023) · cites this paper as [47]
Segmented filamentous bacteria induce TH17 cells in the murine small intestine but do not produce high levels of ATP.
“segmented filamentous bacteria (SFB), which have been shown to induce TH17 cells in the lamina propria of the murine small intestine, do not produce high levels of ATP (Ivanov et al., 2009).”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Ivanov et al., 2009
Th17 cells are absent in GF mice and are inducible upon microbial colonization, most notably with segmented filamentous bacteria, but also other commensal bacteria.
“Th17 cells are absent in GF mice and are inducible upon microbial colonization, most notably with segmented filamentous bacteria (SFB),33,34 but also other commensal bacteria.35”
From Interaction between microbiota and immunity in health and disease (2020) · cites this paper as [34]
Th17 cells are markedly depleted in germ-free animals and can be induced by specific bacterial subsets such as segmented filamentous bacteria.
“Th17 cells are markedly depleted in GF animals and can be induced by specific bacterial subsets such as segmented filamentous bacteria (SFB)”
From The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy (2018) · cites this paper as Ivanov et al., 2009
Segmented filamentous bacteria are prominent inducers of Th17 differentiation.
“Prominent inducers of Th17 differentiation are segmented filamentous bacteria (SFB), spore-forming anaerobic Gram+ bacilli residing in the terminal ileum of some mouse strains [31, 32].”
From Antibiotic-Induced Changes in the Intestinal Microbiota and Disease (2016) · cites this paper as [31]
Microbiota-driven IL-17 acts on local epithelium to promote antimicrobial responses necessary and sufficient to maintain homeostatic balance without overt inflammation in the normal gut.
“This microbiota-driven IL-17 acts on local epithelium to promote anti-microbial responses that are necessary and sufficient to maintain a homeostatic balance but without causing overt inflammation in the normal gut”
From The IL-17 Family of Cytokines in Health and Disease (2019) · cites this paper as Ivanov et al., 2009
In mice, segmented filamentous bacteria (SFB) directly contact intestinal epithelial cells and promote intestinal IL-17 signature genes.
“In mice, segmented filamentous bacteria (SFB) form direct physical contact with mouse intestinal epithelial cells and thereby promote intestinal IL-17 signature genes”
From The IL-17 Family of Cytokines in Health and Disease (2019) · cites this paper as Ivanov et al., 2009
Segmented filamentous bacteria are critical promoters of intestinal mucosal IgA production and Th17 cell induction.
“segmented filamentous bacteria are critical promoters of intestinal mucosal IgA production (39, 40)and Th17 cell induction (41, 42)”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [41]
Intestinal infiltration of pro-inflammatory TH17 cells is induced by segmented filamentous bacteria.
“Intestinal infiltration of pro-inflammatory TH17 cells is induced by segmented filamentous bacteria66, and gut microbial diversity, particularly colonization by Bacteroidetes, is critical for balancing TH1 and TH2 responses64.”
From The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease (2018) · cites this paper as [66]
Gut bacteria influence the development of Th17 cells, Treg cells and memory T cells.
“Gut bacteria influence the development of Th17 cells [46], Treg cells [47] and memory T cells [48–50].”
From Evolution of the immune system in humans from infancy to old age (2015) · cites this paper as [47]
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- Authors
- Ivanov, I. I., Atarashi, K., Manel, N., Brodie, E. L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K. C., Santee, C. A., Lynch, S. V., Tanoue, T., Imaoka, A., Itoh, K., Takeda, K., Umesaki, Y., Honda, K., & Littman, D. R.
- Affiliations
- New York University (US)
- Immunology Frontier Research Center, The University of Osaka (JP)
- Lawrence Berkeley National Laboratory (US)
- Yakult Central Institute (JP)
- Carl Zeiss (United States) (US)
- University of California, San Francisco (US)
- The University of Tokyo (JP)
- Japan Science and Technology Agency (JP)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Honda, Kenya
- Littman, Dan R.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2009-10
- Volume
- 139
- Issue
- 3
- Pages
- 485-498
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC2796826
- OpenAlex
- W2107369528
- Cited by
- 4,554
- References
- 67
- Citations by year
- 2026: 178 · 2025: 229 · 2024: 275 · 2023: 260 · 2022: 275 · 2021: 372 · 2020: 315 · 2019: 351 · 2018: 307 · 2017: 313 · 2016: 289 · 2015: 293 · 2014: 279 · 2013: 253 · 2012: 200
- FWCI
- 74.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1385 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Allergy and Infectious Diseases (AI 33856, R01AI033856)
- National Institute of Diabetes and Digestive and Kidney Diseases (K99DK085329, P30DK043351)
- 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 › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
- Keywords
- segmented filamentous bacteria, Th17 cells, IL-17, IL-22, commensal microbiota, intestinal immune regulation, lamina propria, terminal ileum, Citrobacter rodentium, mucosal immunity, autoimmune disease
- MeSH terms
- Interleukin-22, Serum Amyloid A Protein, Animals, Cell Differentiation, Gram-Positive Bacteria, T-Lymphocytes, Helper-Inducer, Interleukins, Intestinal Mucosa, Mice, Inbred C57BL, Mucous Membrane, Specific Pathogen-Free Organisms, Symbiosis, Immunity, Mucosal, Interleukin-17, Citrobacter rodentium, Mice
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