Ectopic colonization of oral bacteria in the intestine drives TH1 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 & 6 others Jay K. Kolls, Eran Elinav, Hidetoshi Morita, Ramnik J. Xavier, Masahira Hattori, Kenya Honda

    Research output: Contribution to journalArticle

    79 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 languageEnglish
    Pages (from-to)359-365
    Number of pages7
    JournalScience
    Volume358
    Issue number6361
    DOIs
    Publication statusPublished - 2017 Oct 20

    Fingerprint

    Th1 Cells
    Klebsiella
    Intestines
    Germ-Free Life
    Inflammation
    Bacteria
    Intestinal Diseases
    Microbiota
    Inflammatory Bowel Diseases
    Mouth
    Anti-Bacterial Agents
    Health
    Gastrointestinal Microbiome

    ASJC Scopus subject areas

    • General

    Cite this

    Atarashi, K., Suda, W., Luo, C., Kawaguchi, T., Motoo, I., Narushima, S., ... Honda, K. (2017). Ectopic colonization of oral bacteria in the intestine drives TH1 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 TH1 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 journalArticle

    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 TH1 cell induction and inflammation', Science, vol. 358, no. 6361, pp. 359-365. https://doi.org/10.1126/science.aan4526
    Atarashi K, Suda W, Luo C, Kawaguchi T, Motoo I, Narushima S et al. Ectopic colonization of oral bacteria in the intestine drives TH1 cell induction and inflammation. Science. 2017 Oct 20;358(6361):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 TH1 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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