A Three-Gene Assay for Monitoring Immune Quiescence in Kidney Transplantation

J Am Soc Nephrol. 2015 Aug;26(8):2042-53. doi: 10.1681/ASN.2013111239. Epub 2014 Nov 26.

Abstract

Organ transplant recipients face life-long immunosuppression and consequently are at high risk of comorbidities. Occasionally, kidney transplant recipients develop a state of targeted immune quiescence (operational tolerance) against an HLA-mismatched graft, allowing them to withdraw all immunosuppression and retain stable graft function while resuming immune responses to third-party antigens. Methods to better understand and monitor this state of alloimmune quiescence by transcriptional profiling may reveal a gene signature that identifies patients for whom immunosuppression could be titrated to reduce patient and graft morbidities. Therefore, we investigated 571 unique peripheral blood samples from 348 HLA-mismatched renal transplant recipients and 101 nontransplant controls in a four-stage study including microarray, quantitative PCR, and flow cytometry analyses. We report a refined and highly validated (area under the curve, 0.95; 95% confidence interval, 0.92 to 0.97) peripheral blood three-gene assay (KLF6, BNC2, CYP1B1) to detect the state of operational tolerance by quantitative PCR. The frequency of predicted alloimmune quiescence in stable renal transplant patients receiving long-term immunosuppression (n=150) was 7.3% by the three-gene assay. Targeted cell sorting of peripheral blood from operationally tolerant patients showed a significant shift in the ratio of circulating monocyte-derived dendritic cells with significantly different expression of the genes constituting the three-gene assay. Our results suggest that incorporation of patient screening by specific cellular and gene expression assays may support the safety of drug minimization trials and protocols.

Keywords: immunosuppression; kidney transplantation; profiling; tolerance; transcriptional.

Publication types

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

MeSH terms

  • Adolescent
  • Adult
  • Biomarkers / blood*
  • Blood Cell Count
  • CD11c Antigen / metabolism
  • Case-Control Studies
  • Child
  • Cytochrome P-450 CYP1B1 / genetics
  • Cytochrome P-450 CYP1B1 / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Dendritic Cells / metabolism
  • Female
  • Gene Expression Profiling
  • Humans
  • Immunosuppression Therapy*
  • Kidney Transplantation*
  • Kruppel-Like Factor 6
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism
  • Male
  • Middle Aged
  • Oligonucleotide Array Sequence Analysis
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Transplantation Immunology / genetics*
  • Young Adult

Substances

  • BNC2 protein, human
  • Biomarkers
  • CD11c Antigen
  • DNA-Binding Proteins
  • KLF6 protein, human
  • Kruppel-Like Factor 6
  • Kruppel-Like Transcription Factors
  • Proto-Oncogene Proteins
  • CYP1B1 protein, human
  • Cytochrome P-450 CYP1B1