Activated invariant natural killer T cells directly recognize leukemia cells in a CD1d-independent manner

Cancer Sci. 2020 Jul;111(7):2223-2233. doi: 10.1111/cas.14428. Epub 2020 Jun 19.

Abstract

Invariant natural killer T (iNKT) cells are innate-like CD1d-restricted T cells that express the invariant T cell receptor (TCR) composed of Vα24 and Vβ11 in humans. iNKT cells specifically recognize glycolipid antigens such as α-galactosylceramide (αGalCer) presented by CD1d. iNKT cells show direct cytotoxicity toward CD1d-positive tumor cells, especially when CD1d presents glycolipid antigens. However, iNKT cell recognition of CD1d-negative tumor cells is unknown, and direct cytotoxicity of iNKT cells toward CD1d-negative tumor cells remains controversial. Here, we demonstrate that activated iNKT cells recognize leukemia cells in a CD1d-independent manner, however still in a TCR-mediated way. iNKT cells degranulated and released Th1 cytokines toward CD1d-negative leukemia cells (K562, HL-60, REH) as well as αGalCer-loaded CD1d-positive Jurkat cells. The CD1d-independent cytotoxicity was enhanced by natural killer cell-activating receptors such as NKG2D, 2B4, DNAM-1, LFA-1 and CD2, but iNKT cells did not depend on these receptors for the recognition of CD1d-negative leukemia cells. In contrast, TCR was essential for CD1d-independent recognition and cytotoxicity. iNKT cells degranulated toward patient-derived leukemia cells independently of CD1d expression. iNKT cells targeted myeloid malignancies more than acute lymphoblastic leukemia. These findings reveal a novel anti-tumor mechanism of iNKT cells in targeting CD1d-negative tumor cells and indicate the potential of iNKT cells for clinical application to treat leukemia independently of CD1d.

Keywords: CD1d; CD2; LFA-1; leukemia; natural killer T-Cells.

MeSH terms

  • Animals
  • Antigens, CD1d / genetics
  • Antigens, CD1d / metabolism*
  • Biomarkers
  • Cell Degranulation
  • Cell Line, Tumor
  • Costimulatory and Inhibitory T-Cell Receptors / metabolism
  • Cytokines / metabolism
  • Cytotoxicity, Immunologic
  • Disease Models, Animal
  • Female
  • Gene Editing
  • Heterografts
  • Humans
  • Immunophenotyping
  • Leukemia / genetics
  • Leukemia / immunology*
  • Leukemia / metabolism*
  • Leukemia / pathology
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology*
  • Mice
  • Natural Killer T-Cells / immunology*
  • Natural Killer T-Cells / metabolism*
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / metabolism
  • Receptors, Natural Cytotoxicity Triggering / metabolism

Substances

  • Antigens, CD1d
  • Biomarkers
  • CD1D protein, human
  • Costimulatory and Inhibitory T-Cell Receptors
  • Cytokines
  • Receptors, Antigen, T-Cell
  • Receptors, Natural Cytotoxicity Triggering