Natural Killer Cell Inhibition by HLA-E Molecules on Induced Pluripotent Stem Cell-Derived Retinal Pigment Epithelial Cells

Invest Ophthalmol Vis Sci. 2018 Apr 1;59(5):1719-1731. doi: 10.1167/iovs.17-22703.

Abstract

Purpose: To determine whether human induced pluripotent stem (iPS) cell-derived retinal pigment epithelial (RPE) cells (iPS-RPE) can suppress natural killer (NK) cell activation.

Methods: iPS-RPE cells were cocultured with peripheral blood mononuclear cells (PBMCs) or purified NK cells from healthy donors after stimulation with cytokines. To confirm expression of NK cell-specific markers, flow cytometry and quantitative RT-PCR (qRT-PCR) were performed. NK cells (or PBMCs) cocultured with iPS-RPE cells were assessed for proliferation by Ki-67 expression with flow cytometry, and NK suppression by RPE cells was assessed for granzyme B production with ELISA. Human leukocyte antigen (HLA) expression including HLA-E on iPS-RPE cells was evaluated with flow cytometry and qRT-PCR. The effect of HLA-E downregulation was also investigated using small interfering RNA (siRNA) systems. Following iPS-RPE cell transplantation in vivo, we evaluated NK cell invasion in the retina with immunohistochemistry.

Results: Activated NK cells expressed NK-related markers such as CD16, CD56, and CD11b, and NK cells produced cytotoxic agents such as granzyme B, perforin, and TNF-α. Human iPS-RPE cells inhibited cell proliferation and production of these cytotoxic agents by activated NK cells in vitro. iPS-RPE cells constitutively expressed HLA-E and suppressed NK cell activation through an interaction between HLA-E and CD94/NKG2A. Moreover, immunohistochemical evaluation of monkey RPE transplantation into in vivo immune rejection models showed no NK cell invasion in the retina in allografts or xenografts except for one xenografted eye.

Conclusions: Cultured iPS cell-derived RPE cells greatly suppress NK cell activation. Thus, NK cells might be inactivated when exposed to this type of retinal cell.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD / metabolism
  • Biomarkers / metabolism
  • Blotting, Western
  • Cell Proliferation
  • Cells, Cultured
  • Coculture Techniques
  • Cytokines / metabolism
  • Flow Cytometry
  • Granzymes / metabolism
  • HLA-E Antigens
  • Histocompatibility Antigens Class I / pharmacology*
  • Humans
  • Immunohistochemistry
  • Induced Pluripotent Stem Cells / cytology*
  • Ki-67 Antigen / metabolism
  • Killer Cells, Natural / immunology*
  • Lymphocyte Activation / drug effects*
  • Macaca
  • RNA, Small Interfering / genetics
  • Real-Time Polymerase Chain Reaction
  • Retinal Pigment Epithelium / immunology*
  • Retinal Pigment Epithelium / transplantation
  • Transfection
  • beta 2-Microglobulin / genetics

Substances

  • Antigens, CD
  • Biomarkers
  • Cytokines
  • Histocompatibility Antigens Class I
  • Ki-67 Antigen
  • RNA, Small Interfering
  • beta 2-Microglobulin
  • Granzymes