CRISPR/Cas9-Engineered HLA-Deleted Glomerular Endothelial Cells as a Tool to Predict Pathogenic Non-HLA Antibodies in Kidney Transplant Recipients

J Am Soc Nephrol. 2021 Dec;32(12):3231-3251. doi: 10.1681/ASN.2021050689.

Abstract

Background: After kidney transplantation, donor-specific antibodies against human leukocyte antigen donor-specific antibodies (HLA-DSAs) drive antibody-mediated rejection (ABMR) and are associated with poor transplant outcomes. However, ABMR histology (ABMRh) is increasingly reported in kidney transplant recipients (KTRs) without HLA-DSAs, highlighting the emerging role of non-HLA antibodies (Abs).

Methods: W e designed a non-HLA Ab detection immunoassay (NHADIA) using HLA class I and II-deficient glomerular endothelial cells (CiGEnCΔHLA) that had been previously generated through CRISPR/Cas9-induced B2M and CIITA gene disruption. Flow cytometry assessed the reactivity to non-HLA antigens of pretransplantation serum samples from 389 consecutive KTRs. The intensity of the signal observed with the NHADIA was associated with post-transplant graft histology assessed in 951 adequate biopsy specimens.

Results: W e sequentially applied CRISPR/Cas9 to delete the B2M and CIITA genes to obtain a CiGEnCΔHLA clone. CiGEnCΔHLA cells remained indistinguishable from the parental cell line, CiGEnC, in terms of morphology and phenotype. Previous transplantation was the main determinant of the pretransplantation NHADIA result (P<0.001). Stratification of 3-month allograft biopsy specimens (n=298) according to pretransplantation NHADIA tertiles demonstrated that higher levels of non-HLA Abs positively correlated with increased glomerulitis (P=0.002), microvascular inflammation (P=0.003), and ABMRh (P=0.03). A pretransplantation NHADIA threshold of 1.87 strongly discriminated the KTRs with the highest risk of ABMRh (P=0.005, log-rank test). A multivariate Cox model confirmed that NHADIA status and HLA-DSAs were independent, yet synergistic, predictors of ABMRh.

Conclusion: The NHADIA identifies non-HLA Abs and strongly predicts graft endothelial injury independent of HLA-DSAs.

Keywords: CRISPR-Cas systems; antibodies; antibody-mediated rejection; endothelial cells; endothelial inflammation; kidney rejection; kidney transplantation; non-HLA antibodies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • CRISPR-Cas Systems / genetics*
  • Cells, Cultured
  • Endothelial Cells / immunology
  • Female
  • Gene Deletion
  • Graft Rejection / etiology*
  • HLA Antigens / genetics
  • HLA Antigens / immunology*
  • Humans
  • Isoantibodies / immunology*
  • Kidney Glomerulus / immunology*
  • Kidney Transplantation / adverse effects*
  • Male
  • Middle Aged
  • Nuclear Proteins / genetics
  • Reoperation
  • Retrospective Studies
  • Tissue Donors*
  • Trans-Activators / genetics
  • beta 2-Microglobulin / genetics

Substances

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