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Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections

Author

Listed:
  • Jochen Mattner

    (University of Chicago)

  • Kristin L. DeBord

    (University of Chicago)

  • Nahed Ismail

    (University of Texas Medical Branch)

  • Randal D. Goff

    (Brigham Young University)

  • Carlos Cantu

    (The Scripps Research Institute)

  • Dapeng Zhou

    (University of Chicago)

  • Pierre Saint-Mezard

    (University of Chicago)

  • Vivien Wang

    (University of Chicago)

  • Ying Gao

    (Brigham Young University)

  • Ning Yin

    (Brigham Young University)

  • Kasper Hoebe

    (The Scripps Research Institute)

  • Olaf Schneewind

    (University of Chicago)

  • David Walker

    (University of Texas Medical Branch)

  • Bruce Beutler

    (The Scripps Research Institute)

  • Luc Teyton

    (The Scripps Research Institute)

  • Paul B. Savage

    (Brigham Young University)

  • Albert Bendelac

    (University of Chicago)

Abstract

CD1d-restricted natural killer T (NKT) cells are innate-like lymphocytes that express a conserved T-cell receptor and contribute to host defence against various microbial pathogens1,2. However, their target lipid antigens have remained elusive. Here we report evidence for microbial, antigen-specific activation of NKT cells against Gram-negative, lipopolysaccharide (LPS)-negative alpha-Proteobacteria such as Ehrlichia muris and Sphingomonas capsulata. We have identified glycosylceramides from the cell wall of Sphingomonas that serve as direct targets for mouse and human NKT cells, controlling both septic shock reaction and bacterial clearance in infected mice. In contrast, Gram-negative, LPS-positive Salmonella typhimurium activates NKT cells through the recognition of an endogenous lysosomal glycosphingolipid, iGb3, presented by LPS-activated dendritic cells. These findings identify two novel antigenic targets of NKT cells in antimicrobial defence, and show that glycosylceramides are an alternative to LPS for innate recognition of the Gram-negative, LPS-negative bacterial cell wall.

Suggested Citation

  • Jochen Mattner & Kristin L. DeBord & Nahed Ismail & Randal D. Goff & Carlos Cantu & Dapeng Zhou & Pierre Saint-Mezard & Vivien Wang & Ying Gao & Ning Yin & Kasper Hoebe & Olaf Schneewind & David Walke, 2005. "Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections," Nature, Nature, vol. 434(7032), pages 525-529, March.
    • Handle: RePEc:nat:nature:v:434:y:2005:i:7032:d:10.1038_nature03408
    DOI: 10.1038/nature03408
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    Cited by:

    1. Phillip M. Brailey & Lauren Evans & Juan Carlos López-Rodríguez & Anthony Sinadinos & Victoria Tyrrel & Gavin Kelly & Valerie O’Donnell & Peter Ghazal & Susan John & Patricia Barral, 2022. "CD1d-dependent rewiring of lipid metabolism in macrophages regulates innate immune responses," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Channakeshava Sokke Umeshappa & Patricia Solé & Jun Yamanouchi & Saswat Mohapatra & Bas G. J. Surewaard & Josep Garnica & Santiswarup Singha & Debajyoti Mondal & Elena Cortés-Vicente & Charlotte D’Mel, 2022. "Re-programming mouse liver-resident invariant natural killer T cells for suppressing hepatic and diabetogenic autoimmunity," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    3. Norimasa Iwanami & Andreas S. Richter & Katarzyna Sikora & Thomas Boehm, 2023. "Tnpo3 controls splicing of the pre-mRNA encoding the canonical TCR α chain of iNKT cells," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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