Failure of transplantation tolerance induction by autologous regulatory T cells in the pig-to-non-human primate islet xenotransplantation model

Xenotransplantation. 2016 Jul;23(4):300-9. doi: 10.1111/xen.12246. Epub 2016 Jul 7.

Abstract

Background: Islet allotransplantation is a promising way to treat some type 1 diabetic (T1D) patients with frequent hypoglycemic unawareness, and islet xenotransplantation is emerging to overcome the problem of donor organ shortage. Our recent study showing reproducible long-term survival of porcine islets in non-human primates (NHPs) allows us to examine whether autologous regulatory T-cell (Treg) infusion at peri-transplantation period would induce transplantation tolerance in xenotransplantation setting.

Methods: Two diabetic rhesus monkeys were transplanted with porcine islets from wild-type adult Seoul National University (SNU) miniature pigs with immunosuppression by anti-thymoglobulin (ATG), cobra venom factor, anti-CD154 monoclonal antibody (mAb), and sirolimus. CD4(+) CD25(high) CD127(low) autologous regulatory T cells from the recipients were isolated, ex vivo expanded, and infused at the peri-transplantation period. Blood glucose and porcine C-peptide from the recipients were measured up to 1000 days. Maintenance immunosuppressants including a CD40-CD154 blockade were deliberately discontinued to confirm whether transplantation tolerance was induced by adoptively transferred Tregs.

Results: After pig islet transplantation via portal vein, blood glucose levels of diabetic recipients became normalized and maintained over 6 months while in immunosuppressive maintenance with a CD40-CD154 blockade and sirolimus. However, the engrafted pig islets in the long-term period were fully rejected by activated immune cells, particularly T cells, when immunosuppressants were stopped, showing a failure of transplantation tolerance induction by autologous Tregs.

Conclusions: Taken together, autologous Tregs infused at the peri-transplantation period failed to induce transplantation tolerance in pig-to-NHP islet xenotransplantation setting.

Keywords: Tregs; non-human primates; pig islet transplantation.

MeSH terms

  • Animals
  • Diabetes Mellitus, Experimental
  • Graft Survival / immunology*
  • Immune Tolerance / drug effects
  • Immunosuppression Therapy / methods
  • Immunosuppressive Agents / pharmacology
  • Islets of Langerhans Transplantation
  • Primates
  • Swine
  • T-Lymphocytes, Regulatory / immunology*
  • Transplantation Tolerance / immunology*
  • Transplantation, Heterologous* / methods

Substances

  • Immunosuppressive Agents