Genetic investigation of MHC-independent missing-self recognition by mouse NK cells using an in vivo bone marrow transplantation model

J Immunol. 2015 Mar 15;194(6):2909-18. doi: 10.4049/jimmunol.1401523. Epub 2015 Feb 13.

Abstract

MHC-I-specific receptors play a vital role in NK cell-mediated "missing-self" recognition, which contributes to NK cell activation. In contrast, MHC-independent NK recognition mechanisms are less well characterized. In this study, we investigated the role of NKR-P1B:Clr-b (Klrb1:Clec2d) interactions in determining the outcome of murine hematopoietic cell transplantation in vivo. Using a competitive transplant assay, we show that Clr-b(-/-) bone marrow (BM) cells were selectively rejected by wild-type B6 recipients, to a similar extent as H-2D(b-/-) MHC-I-deficient BM cells. Selective rejection of Clr-b(-/-) BM cells was mitigated by NK depletion of recipient mice. Competitive rejection of Clr-b(-/-) BM cells also occurred in allogeneic transplant recipients, where it was reversed by selective depletion of NKR-P1B(hi) NK cells, leaving the remaining NKR-P1B(lo) NK subset and MHC-I-dependent missing-self recognition intact. Moreover, competitive rejection of Clr-b(-/-) hematopoietic cells was abrogated in Nkrp1b-deficient recipients, which lack the receptor for Clr-b. Of interest, similar to MHC-I-deficient NK cells, Clr-b(-/-) NK cells were hyporesponsive to both NK1.1 (NKR-P1C)-stimulated and IL-12/18 cytokine-primed IFN-γ production. These findings support a unique and nonredundant role for NKR-P1B:Clr-b interactions in missing-self recognition of normal hematopoietic cells and suggest that optimal BM transplant success relies on MHC-independent tolerance mechanisms. These findings provide a model for human NKR-P1A:LLT1 (KLRB1:CLEC2D) interactions in human hematopoietic cell transplants.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Marrow Cells / immunology
  • Bone Marrow Cells / metabolism
  • Bone Marrow Transplantation / methods*
  • Cell Line, Tumor
  • Flow Cytometry
  • Gene Expression / immunology
  • Graft Rejection / genetics
  • Graft Rejection / immunology
  • Hematopoietic Stem Cell Transplantation / methods
  • Histocompatibility Antigen H-2D / genetics
  • Histocompatibility Antigen H-2D / immunology
  • Histocompatibility Antigen H-2D / metabolism
  • Humans
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Lectins, C-Type / deficiency
  • Lectins, C-Type / genetics
  • Lectins, C-Type / immunology*
  • Membrane Proteins / deficiency
  • Membrane Proteins / genetics
  • Membrane Proteins / immunology*
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Animal
  • NK Cell Lectin-Like Receptor Subfamily B / deficiency
  • NK Cell Lectin-Like Receptor Subfamily B / genetics
  • NK Cell Lectin-Like Receptor Subfamily B / immunology*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Transplantation, Homologous

Substances

  • Histocompatibility Antigen H-2D
  • Klrb1b protein, mouse
  • Lectins, C-Type
  • Membrane Proteins
  • NK Cell Lectin-Like Receptor Subfamily B
  • Ocil protein, mouse
  • Interferon-gamma