Ecto-nucleoside triphosphate diphosphohydrolase 7 controls Th17 cell responses through regulation of luminal ATP in the small intestine
Open accessAbstract
Extracellular ATP is released from live cells in controlled conditions, as well as dying cells in inflammatory conditions, and, thereby, regulates T cell responses, including Th17 cell induction. The level of extracellular ATP is closely regulated by ATP hydrolyzing enzymes, such as ecto-nucleoside triphosphate diphosphohydrolases (ENTPDases). ENTPDase1/CD39, which is expressed in immune cells, was shown to regulate immune responses by downregulating the ATP level. In this study, we analyzed the immunomodulatory function of ENTPDase7, which is preferentially expressed in epithelial cells in the small intestine. The targeted deletion of Entpd7 encoding ENTPDase7 in mice resulted in increased ATP levels in the small intestinal lumen. The number of Th17 cells was selectively increased in the small intestinal lamina propria in Entpd7(-/-) mice. Th17 cells were decreased by oral administration of antibiotics or the ATP antagonist in Entpd7(-/-) mice, indicating that commensal microbiota-dependent ATP release mediates the enhanced Th17 cell development in the small intestinal lamina propria of Entpd7(-/-) mice. In accordance with the increased number of small intestinal Th17 cells, Entpd7(-/-) mice were resistant to oral infection with Citrobacter rodentium. Entpd7(-/-) mice suffered from severe experimental autoimmune encephalomyelitis, which was associated with increased numbers of CD4(+) T cells producing both IL-17 and IFN-γ. Taken together, these findings demonstrate that ENTPDase7 controls the luminal ATP level and, thereby, regulates Th17 cell development in the small intestine.
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Mice deficient for ENTPD7 have higher luminal ATP and an increase in TH17 cells in the small-intestinal lamina propria.
“mice deficient for the epithelial ATP-degrading enzyme ectonucleoside triphosphate diphosphohydrolase 7 (ENTPD7) exhibit higher levels of luminal ATP and an increase in TH17 cells in the lamina propria of the small-intestinal epithelium (Kusu et al., 2013).”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Kusu et al., 2013
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- Authors
- Kusu, T., Kayama, H., Kinoshita, M., Jeon, S. G., Ueda, Y., Goto, Y., Okumura, R., Saiga, H., Kurakawa, T., Ikeda, K., Maeda, Y., Nishimura, J.-I., Arima, Y., Atarashi, K., Honda, K., Murakami, M., Kunisawa, J., Kiyono, H., Okumura, M., Yamamoto, M., & Takeda, K.
- Affiliations
- The University of Osaka (JP)
- Japan Science and Technology Agency (JP)
- Immunology Frontier Research Center, The University of Osaka (JP)
- Institute of Medical Science, The University of Tokyo (JP)
- Laboratory of Immune Regulation, Department of Microbiology and Immunology, Graduate School of Medicine, Osaka University , Suita, Osaka 565-0871,
- National Institute of Biomedical Innovation, Health and Nutrition (JP)
- Corresponding author
- Takeda, Kiyoshi
- ORCID
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-01
- Volume
- 190
- Issue
- 2
- Pages
- 774-783
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC3539688
- OpenAlex
- W2129227303
- Cited by
- 73
- References
- 62
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 3 · 2022: 4 · 2021: 6 · 2020: 5 · 2019: 3 · 2018: 1 · 2017: 16 · 2016: 5 · 2015: 14 · 2014: 5 · 2013: 3
- FWCI
- 4.94
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Immunology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science (24249028, 24659217, 24390120)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Molecular Research
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- extracellular ATP, Th17 cells, small intestine, intestinal epithelial cells, commensal microbiota, ATP hydrolysis, lamina propria, experimental autoimmune encephalomyelitis, Citrobacter rodentium infection, IL-17, interferon-gamma, CD4+ T cells, immunomodulation
- MeSH terms
- Adenosine Triphosphate, Animals, Encephalomyelitis, Autoimmune, Experimental, Enterobacteriaceae Infections, Female, Gene Expression Regulation, Intestinal Mucosa, Intestine, Small, Pyrophosphatases, Mice, Knockout, Citrobacter rodentium, Mice, Metagenome, Th17 Cells
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