Superiority of rapamycin over tacrolimus in preserving nonhuman primate Treg half-life and phenotype after adoptive transfer

Am J Transplant. 2014 Dec;14(12):2691-703. doi: 10.1111/ajt.12934. Epub 2014 Oct 30.

Abstract

Many critical issues remain concerning how best to deploy adoptive regulatory T cell (Treg) immunotherapy to the clinic. These include a determination of their pharmacokinetic characteristics, their optimal dose, their phenotypic stability and the best therapies with which to pair Tregs. By performing a CFSE-labeled autologous Treg pulse experiment, we determined that the accessible peripheral blood Treg pool in rhesus macaques is quite large (75 ± 11 × 10(6) Tregs/kg). Pharmacokinetic analysis revealed that Tregs have two phases of elimination: an α phase, with a T1/2 in the peripheral blood of 32.4 ± 11.3 h and a β phase with a T1/2 of 120.4 ± 19.7 h. In addition to their short initial half-life, Tregs underwent rapid phenotypic shifts after infusion, with significant loss of both CD25 and FoxP3 by day +6. While tacrolimus stabilized CD25 expression, it did not improve T1/2 , nor mitigate the loss of FoxP3. In contrast, rapamycin significantly stabilized both CD25 and FoxP3, and supported an increased half-life, with an α phase of 67.7 ± 6.9 h and a β phase of 252.1 ± 54.9 h. These results suggest that rapamycin may be a necessary addition to Treg immunotherapy, and that tacrolimus may be deleterious to Treg integrity posttransfer.

Keywords: Basic (laboratory) research/science; T cell biology; immunobiology; immunosuppression/immune modulation; lymphocyte biology: trafficking; tolerance: experimental; translational research/science.

Publication types

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

MeSH terms

  • Adoptive Transfer*
  • Animals
  • CD4-Positive T-Lymphocytes / immunology*
  • Cell Proliferation
  • Cells, Cultured
  • Flow Cytometry
  • Fluoresceins
  • Fluorescent Dyes
  • Forkhead Transcription Factors / metabolism
  • Half-Life
  • Immunosuppressive Agents / pharmacokinetics
  • Immunosuppressive Agents / pharmacology*
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Macaca mulatta
  • Phenotype
  • Sirolimus / pharmacokinetics
  • Sirolimus / pharmacology*
  • Succinimides
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / transplantation
  • Tacrolimus / pharmacokinetics
  • Tacrolimus / pharmacology*
  • Tissue Distribution
  • Transplantation, Autologous

Substances

  • 5-(6)-carboxyfluorescein diacetate succinimidyl ester
  • Fluoresceins
  • Fluorescent Dyes
  • Forkhead Transcription Factors
  • Immunosuppressive Agents
  • Interleukin-2 Receptor alpha Subunit
  • Succinimides
  • Sirolimus
  • Tacrolimus