Gallbladder-derived surfactant protein D regulates gut commensal bacteria for maintaining intestinal homeostasis

Hana Sarashina-Kida, Hideo Negishi, Junko Nishio, Wataru Suda, Yuki Nakajima, Mika Yasui-Kato, Keiko Iwaisako, Sujin Kang, Nobuyasu Endo, Hideyuki Yanai, Masataka Asagiri, Hiroshi Kida, Masahira Hattori, Atsushi Kumanogoh, Tadatsugu Taniguchi

    Research output: Contribution to journalArticle

    8 Citations (Scopus)

    Abstract

    The commensal microbiota within the gastrointestinal tract is essential in maintaining homeostasis. Indeed, dysregulation in the repertoire of microbiota can result in the development of intestinal immune–inflammatory diseases. Further, this immune regulation by gut microbiota is important systemically, impacting health and disease of organ systems beyond the local environment of the gut. What has not been explored is how distant organs might in turn shape the microbiota via microbe-targeted molecules. Here, we provide evidence that surfactant protein D (SP-D) synthesized in the gallbladder and delivered into intestinal lumen binds selectively to species of gut commensal bacteria. SP-D–deficient mice manifest intestinal dysbiosis and show a susceptibility to dextran sulfate sodium-induced colitis. Further, fecal transfer from SP-D–deficient mice to wild-type, germ-free mice conveyed colitis susceptibility. Interestingly, colitis caused a notable increase in Sftpd gene expression in the gallbladder, but not in the lung, via the activity of glucocorticoids produced in the liver. These findings describe a unique mechanism of interorgan regulation of intestinal immune homeostasis by SP-D with potential clinical implications such as cholecystectomy.

    Original languageEnglish
    Pages (from-to)10178-10183
    Number of pages6
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume114
    Issue number38
    DOIs
    Publication statusPublished - 2017 Sep 19

    Fingerprint

    Pulmonary Surfactant-Associated Protein D
    Microbiota
    Colitis
    Gallbladder
    Homeostasis
    Bacteria
    Dysbiosis
    Intestinal Diseases
    Dextran Sulfate
    Cholecystectomy
    Glucocorticoids
    Gastrointestinal Tract
    Gene Expression
    Lung
    Liver
    Health

    Keywords

    • Colitis
    • Gallbladder
    • Glucocorticoids
    • Gut microbiota
    • Surfactant protein D

    ASJC Scopus subject areas

    • General

    Cite this

    Gallbladder-derived surfactant protein D regulates gut commensal bacteria for maintaining intestinal homeostasis. / Sarashina-Kida, Hana; Negishi, Hideo; Nishio, Junko; Suda, Wataru; Nakajima, Yuki; Yasui-Kato, Mika; Iwaisako, Keiko; Kang, Sujin; Endo, Nobuyasu; Yanai, Hideyuki; Asagiri, Masataka; Kida, Hiroshi; Hattori, Masahira; Kumanogoh, Atsushi; Taniguchi, Tadatsugu.

    In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 38, 19.09.2017, p. 10178-10183.

    Research output: Contribution to journalArticle

    Sarashina-Kida, H, Negishi, H, Nishio, J, Suda, W, Nakajima, Y, Yasui-Kato, M, Iwaisako, K, Kang, S, Endo, N, Yanai, H, Asagiri, M, Kida, H, Hattori, M, Kumanogoh, A & Taniguchi, T 2017, 'Gallbladder-derived surfactant protein D regulates gut commensal bacteria for maintaining intestinal homeostasis' Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 38, pp. 10178-10183. https://doi.org/10.1073/pnas.1712837114
    Sarashina-Kida, Hana ; Negishi, Hideo ; Nishio, Junko ; Suda, Wataru ; Nakajima, Yuki ; Yasui-Kato, Mika ; Iwaisako, Keiko ; Kang, Sujin ; Endo, Nobuyasu ; Yanai, Hideyuki ; Asagiri, Masataka ; Kida, Hiroshi ; Hattori, Masahira ; Kumanogoh, Atsushi ; Taniguchi, Tadatsugu. / Gallbladder-derived surfactant protein D regulates gut commensal bacteria for maintaining intestinal homeostasis. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 38. pp. 10178-10183.
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