Data-Driven Kidney Transplant Phenotyping as a Histology-Independent Framework for Biomarker Discovery

J Am Soc Nephrol. 2021 Aug;32(8):1933-1945. doi: 10.1681/ASN.2020121685. Epub 2021 Jun 2.

Abstract

Background: In transplant medicine, clinical decision making largely relies on histology of biopsy specimens. However, histology suffers from low specificity, sensitivity, and reproducibility, leading to suboptimal stratification of patients. We developed a histology-independent immune framework of kidney graft homeostasis and rejection.

Methods: We applied tailored RNA deconvolution for leukocyte enumeration and coregulated gene network analysis to published bulk human kidney transplant RNA transcriptomes as input for unsupervised, high-dimensional phenotype clustering. We used framework-based graft survival analysis to identify a biomarker that was subsequently characterized in independent transplant biopsy specimens.

Results: We found seven immune phenotypes that confirm known rejection types and uncovered novel signatures. The molecular phenotypes allow for improved graft survival analysis compared with histology, and identify a high-risk group in nonrejecting transplants. Two fibrosis-related phenotypes with distinct immune features emerged with reduced graft survival. We identified lysyl oxidase-like 2 (LOXL2)-expressing peritubular CD68+ macrophages as a framework-derived biomarker of impaired allograft function. These cells precede graft fibrosis, as demonstrated in longitudinal biopsy specimens, and may be clinically useful as a biomarker for early fibrogenesis.

Conclusions: This study provides a comprehensive, data-driven atlas of human kidney transplant phenotypes and demonstrates its utility to identify novel clinical biomarkers.

Keywords: acute allograft rejection; immunology; kidney transplantation; transcriptional profiling; transplant pathology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Allografts / pathology
  • Allografts / physiopathology
  • Amino Acid Oxidoreductases / metabolism
  • Big Data
  • Biomarkers
  • Biopsy
  • Clinical Decision-Making
  • Databases, Genetic
  • Fibrosis
  • Gene Expression Profiling
  • Graft Rejection / immunology*
  • Graft Survival
  • Humans
  • Kidney / pathology*
  • Kidney / physiopathology*
  • Kidney Transplantation*
  • Leukocyte Count
  • Leukocytes
  • Macrophages / metabolism
  • Phenotype*
  • RNA / analysis
  • Support Vector Machine
  • Transcriptome*

Substances

  • Biomarkers
  • RNA
  • Amino Acid Oxidoreductases
  • LOXL2 protein, human