Progenitor-derived human endothelial cells evade alloimmunity by CRISPR/Cas9-mediated complete ablation of MHC expression

JCI Insight. 2019 Oct 17;4(20):e129739. doi: 10.1172/jci.insight.129739.

Abstract

Tissue engineering may address organ shortages currently limiting clinical transplantation. Off-the-shelf engineered vascularized organs will likely use allogeneic endothelial cells (ECs) to construct microvessels required for graft perfusion. Vasculogenic ECs can be differentiated from committed progenitors (human endothelial colony-forming cells or HECFCs) without risk of mutation or teratoma formation associated with reprogrammed stem cells. Like other ECs, these cells can express both class I and class II major histocompatibility complex (MHC) molecules, bind donor-specific antibody (DSA), activate alloreactive T effector memory cells, and initiate rejection in the absence of donor leukocytes. CRISPR/Cas9-mediated dual ablation of β2-microglobulin and class II transactivator (CIITA) in HECFC-derived ECs eliminates both class I and II MHC expression while retaining EC functions and vasculogenic potential. Importantly, dually ablated ECs no longer bind human DSA or activate allogeneic CD4+ effector memory T cells and are resistant to killing by CD8+ alloreactive cytotoxic T lymphocytes in vitro and in vivo. Despite absent class I MHC molecules, these ECs do not activate or elicit cytotoxic activity from allogeneic natural killer cells. These data suggest that HECFC-derived ECs lacking MHC molecule expression can be utilized for engineering vascularized grafts that evade allorejection.

Keywords: Antigen presentation; Immunology; NK cells; Transplantation; endothelial cells.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Allografts / blood supply
  • Allografts / immunology*
  • Allografts / supply & distribution
  • Animals
  • CD4-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • CRISPR-Cas Systems / genetics
  • Cell Differentiation
  • Cells, Cultured
  • Disease Models, Animal
  • Endothelial Cells / immunology*
  • Endothelial Cells / metabolism
  • Endothelial Progenitor Cells
  • Female
  • Fetal Blood / cytology
  • Gene Knockout Techniques
  • Graft Rejection / blood
  • Graft Rejection / immunology
  • Graft Rejection / prevention & control*
  • Healthy Volunteers
  • Humans
  • Isoantibodies / immunology
  • Killer Cells, Natural / immunology
  • Lymphocyte Activation / genetics
  • Mice
  • Microvessels / cytology
  • Microvessels / immunology
  • Microvessels / transplantation
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / immunology
  • Organ Transplantation / adverse effects
  • Organ Transplantation / methods
  • Primary Cell Culture
  • Tissue Engineering / methods*
  • Trans-Activators / genetics*
  • Trans-Activators / immunology
  • beta 2-Microglobulin / genetics*
  • beta 2-Microglobulin / immunology

Substances

  • B2M protein, human
  • Isoantibodies
  • MHC class II transactivator protein
  • Nuclear Proteins
  • Trans-Activators
  • beta 2-Microglobulin