Ectopic colonization of oral bacteria in the intestine drives T1 cell induction and inflammation

Koji Atarashi; Wataru Suda; Chengwei Luo; Takaaki Kawaguchi; Iori Motoo; Seiko Narushima; Yuya Kiguchi; Keiko Yasuma; Eiichiro Watanabe; Takeshi Tanoue; Christoph A Thaiss; Mayuko Sato; Kiminori Toyooka; Heba S Said; Hirokazu Yamagami; Scott A Rice; Dirk Gevers; Ryan C Johnson; Julia A Segre; Kong Chen; Jay K Kolls; Eran Elinav; Hidetoshi Morita; Ramnik J Xavier; Masahira Hattori; Kenya Honda

doi:10.1126/science.aan4526

Ectopic colonization of oral bacteria in the intestine drives T1 cell induction and inflammation

Koji Atarashi, Wataru Suda, Chengwei Luo, Takaaki Kawaguchi, Iori Motoo, Seiko Narushima, Yuya Kiguchi, Keiko Yasuma, Eiichiro Watanabe, Takeshi Tanoue, Christoph A Thaiss, Mayuko Sato, Kiminori Toyooka, Heba S Said, Hirokazu Yamagami, Scott A Rice, Dirk Gevers, Ryan C Johnson, Julia A Segre, Kong ChenJay K Kolls, Eran Elinav, Hidetoshi Morita, Ramnik J Xavier, Masahira Hattori, Kenya Honda

Research output: Contribution to journal › Article

124 Citations (Scopus)

Abstract

Intestinal colonization by bacteria of oral origin has been correlated with several negative health outcomes, including inflammatory bowel disease. However, a causal role of oral bacteria ectopically colonizing the intestine remains unclear. Using gnotobiotic techniques, we show that strains of Klebsiella spp. isolated from the salivary microbiota are strong inducers of T helper 1 (TH1) cells when they colonize in the gut. These Klebsiella strains are resistant to multiple antibiotics, tend to colonize when the intestinal microbiota is dysbiotic, and elicit a severe gut inflammation in the context of a genetically susceptible host. Our findings suggest that the oral cavity may serve as a reservoir for potential intestinal pathobionts that can exacerbate intestinal disease.

Original language	English
Pages (from-to)	359-365
Number of pages	7
Journal	Science
Volume	358
Issue number	6361
DOIs	https://doi.org/10.1126/science.aan4526
Publication status	Published - Oct 20 2017
Externally published	Yes

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Keywords

Animals
Anti-Bacterial Agents/pharmacology
Drug Resistance, Bacterial
Dysbiosis/immunology
Germ-Free Life
Inflammatory Bowel Diseases/immunology
Intestines/immunology
Klebsiella/drug effects
Mice
Mice, Inbred BALB C
Mice, Inbred C57BL
Microbiota/immunology
Mouth/microbiology
Saliva/microbiology
Th1 Cells/immunology

Cite this

Atarashi, K., Suda, W., Luo, C., Kawaguchi, T., Motoo, I., Narushima, S., Kiguchi, Y., Yasuma, K., Watanabe, E., Tanoue, T., Thaiss, C. A., Sato, M., Toyooka, K., Said, H. S., Yamagami, H., Rice, S. A., Gevers, D., Johnson, R. C., Segre, J. A., ... Honda, K. (2017). Ectopic colonization of oral bacteria in the intestine drives T1 cell induction and inflammation. Science, 358(6361), 359-365. https://doi.org/10.1126/science.aan4526

Ectopic colonization of oral bacteria in the intestine drives T1 cell induction and inflammation. / Atarashi, Koji; Suda, Wataru; Luo, Chengwei; Kawaguchi, Takaaki; Motoo, Iori; Narushima, Seiko; Kiguchi, Yuya; Yasuma, Keiko; Watanabe, Eiichiro; Tanoue, Takeshi; Thaiss, Christoph A; Sato, Mayuko; Toyooka, Kiminori; Said, Heba S; Yamagami, Hirokazu; Rice, Scott A; Gevers, Dirk; Johnson, Ryan C; Segre, Julia A; Chen, Kong; Kolls, Jay K; Elinav, Eran; Morita, Hidetoshi; Xavier, Ramnik J; Hattori, Masahira; Honda, Kenya.

In: Science, Vol. 358, No. 6361, 20.10.2017, p. 359-365.

Research output: Contribution to journal › Article

Atarashi, K, Suda, W, Luo, C, Kawaguchi, T, Motoo, I, Narushima, S, Kiguchi, Y, Yasuma, K, Watanabe, E, Tanoue, T, Thaiss, CA, Sato, M, Toyooka, K, Said, HS, Yamagami, H, Rice, SA, Gevers, D, Johnson, RC, Segre, JA, Chen, K, Kolls, JK, Elinav, E, Morita, H, Xavier, RJ, Hattori, M & Honda, K 2017, 'Ectopic colonization of oral bacteria in the intestine drives T1 cell induction and inflammation', Science, vol. 358, no. 6361, pp. 359-365. https://doi.org/10.1126/science.aan4526

Atarashi, Koji ; Suda, Wataru ; Luo, Chengwei ; Kawaguchi, Takaaki ; Motoo, Iori ; Narushima, Seiko ; Kiguchi, Yuya ; Yasuma, Keiko ; Watanabe, Eiichiro ; Tanoue, Takeshi ; Thaiss, Christoph A ; Sato, Mayuko ; Toyooka, Kiminori ; Said, Heba S ; Yamagami, Hirokazu ; Rice, Scott A ; Gevers, Dirk ; Johnson, Ryan C ; Segre, Julia A ; Chen, Kong ; Kolls, Jay K ; Elinav, Eran ; Morita, Hidetoshi ; Xavier, Ramnik J ; Hattori, Masahira ; Honda, Kenya. / Ectopic colonization of oral bacteria in the intestine drives T1 cell induction and inflammation. In: Science. 2017 ; Vol. 358, No. 6361. pp. 359-365.

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abstract = "Intestinal colonization by bacteria of oral origin has been correlated with several negative health outcomes, including inflammatory bowel disease. However, a causal role of oral bacteria ectopically colonizing the intestine remains unclear. Using gnotobiotic techniques, we show that strains of Klebsiella spp. isolated from the salivary microbiota are strong inducers of T helper 1 (TH1) cells when they colonize in the gut. These Klebsiella strains are resistant to multiple antibiotics, tend to colonize when the intestinal microbiota is dysbiotic, and elicit a severe gut inflammation in the context of a genetically susceptible host. Our findings suggest that the oral cavity may serve as a reservoir for potential intestinal pathobionts that can exacerbate intestinal disease.",

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AU - Motoo, Iori

AU - Narushima, Seiko

AU - Kiguchi, Yuya

AU - Yasuma, Keiko

AU - Watanabe, Eiichiro

AU - Tanoue, Takeshi

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AU - Toyooka, Kiminori

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AU - Rice, Scott A

AU - Gevers, Dirk

AU - Johnson, Ryan C

AU - Segre, Julia A

AU - Chen, Kong

AU - Kolls, Jay K

AU - Elinav, Eran

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AB - Intestinal colonization by bacteria of oral origin has been correlated with several negative health outcomes, including inflammatory bowel disease. However, a causal role of oral bacteria ectopically colonizing the intestine remains unclear. Using gnotobiotic techniques, we show that strains of Klebsiella spp. isolated from the salivary microbiota are strong inducers of T helper 1 (TH1) cells when they colonize in the gut. These Klebsiella strains are resistant to multiple antibiotics, tend to colonize when the intestinal microbiota is dysbiotic, and elicit a severe gut inflammation in the context of a genetically susceptible host. Our findings suggest that the oral cavity may serve as a reservoir for potential intestinal pathobionts that can exacerbate intestinal disease.

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10.1126/science.aan4526