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

    14 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

    Keywords

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

    ASJC Scopus subject areas

    • General

    Fingerprint Dive into the research topics of 'Gallbladder-derived surfactant protein D regulates gut commensal bacteria for maintaining intestinal homeostasis'. Together they form a unique fingerprint.

  • Cite this

    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, 114(38), 10178-10183. https://doi.org/10.1073/pnas.1712837114