Genomic Mismatch at LIMS1 Locus and Kidney Allograft Rejection

N Engl J Med. 2019 May 16;380(20):1918-1928. doi: 10.1056/NEJMoa1803731.

Abstract

Background: In the context of kidney transplantation, genomic incompatibilities between donor and recipient may lead to allosensitization against new antigens. We hypothesized that recessive inheritance of gene-disrupting variants may represent a risk factor for allograft rejection.

Methods: We performed a two-stage genetic association study of kidney allograft rejection. In the first stage, we performed a recessive association screen of 50 common gene-intersecting deletion polymorphisms in a cohort of kidney transplant recipients. In the second stage, we replicated our findings in three independent cohorts of donor-recipient pairs. We defined genomic collision as a specific donor-recipient genotype combination in which a recipient who was homozygous for a gene-intersecting deletion received a transplant from a nonhomozygous donor. Identification of alloantibodies was performed with the use of protein arrays, enzyme-linked immunosorbent assays, and Western blot analyses.

Results: In the discovery cohort, which included 705 recipients, we found a significant association with allograft rejection at the LIMS1 locus represented by rs893403 (hazard ratio with the risk genotype vs. nonrisk genotypes, 1.84; 95% confidence interval [CI], 1.35 to 2.50; P = 9.8×10-5). This effect was replicated under the genomic-collision model in three independent cohorts involving a total of 2004 donor-recipient pairs (hazard ratio, 1.55; 95% CI, 1.25 to 1.93; P = 6.5×10-5). In the combined analysis (discovery cohort plus replication cohorts), the risk genotype was associated with a higher risk of rejection than the nonrisk genotype (hazard ratio, 1.63; 95% CI, 1.37 to 1.95; P = 4.7×10-8). We identified a specific antibody response against LIMS1, a kidney-expressed protein encoded within the collision locus. The response involved predominantly IgG2 and IgG3 antibody subclasses.

Conclusions: We found that the LIMS1 locus appeared to encode a minor histocompatibility antigen. Genomic collision at this locus was associated with rejection of the kidney allograft and with production of anti-LIMS1 IgG2 and IgG3. (Funded by the Columbia University Transplant Center and others.).

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics*
  • Adaptor Proteins, Signal Transducing / immunology
  • Cohort Studies
  • DNA Copy Number Variations*
  • Genetic Association Studies
  • Genotype
  • Graft Rejection / genetics*
  • HLA Antigens / genetics
  • Histocompatibility Testing
  • Humans
  • Immunoglobulin G / blood
  • Kidney Transplantation*
  • LIM Domain Proteins / genetics*
  • LIM Domain Proteins / immunology
  • Membrane Proteins / genetics
  • Membrane Proteins / immunology
  • Polymorphism, Single Nucleotide
  • Tissue Donors

Substances

  • Adaptor Proteins, Signal Transducing
  • HLA Antigens
  • Immunoglobulin G
  • LIM Domain Proteins
  • LIMS1 protein, human
  • Membrane Proteins