Costimulation-adhesion blockade is superior to cyclosporine A and prednisone immunosuppressive therapy for preventing rejection of differentiated human embryonic stem cells following transplantation

Stem Cells. 2013 Nov;31(11):2354-63. doi: 10.1002/stem.1501.

Abstract

Rationale: Human embryonic stem cell (hESC) derivatives are attractive candidates for therapeutic use. The engraftment and survival of hESC derivatives as xenografts or allografts require effective immunosuppression to prevent immune cell infiltration and graft destruction.

Objective: To test the hypothesis that a short-course, dual-agent regimen of two costimulation-adhesion blockade agents can induce better engraftment of hESC derivatives compared to current immunosuppressive agents.

Methods and results: We transduced hESCs with a double fusion reporter gene construct expressing firefly luciferase (Fluc) and enhanced green fluorescent protein, and differentiated these cells to endothelial cells (hESC-ECs). Reporter gene expression enabled longitudinal assessment of cell engraftment by bioluminescence imaging. Costimulation-adhesion therapy resulted in superior hESC-EC and mouse EC engraftment compared to cyclosporine therapy in a hind limb model. Costimulation-adhesion therapy also promoted robust hESC-EC and hESC-derived cardiomyocyte survival in an ischemic myocardial injury model. Improved hESC-EC engraftment had a cardioprotective effect after myocardial injury, as assessed by magnetic resonance imaging. Mechanistically, costimulation-adhesion therapy is associated with systemic and intragraft upregulation of T-cell immunoglobulin and mucin domain 3 (TIM3) and a reduced proinflammatory cytokine profile.

Conclusions: Costimulation-adhesion therapy is a superior alternative to current clinical immunosuppressive strategies for preventing the post-transplant rejection of hESC derivatives. By extending the window for cellular engraftment, costimulation-adhesion therapy enhances functional preservation following ischemic injury. This regimen may function through a TIM3-dependent mechanism.

Keywords: Costimulation blockade; Embryonic stem cells; Endothelial cells; Immune tolerance; Immunosuppressive drugs; Myocardial infarction.

Publication types

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

MeSH terms

  • Abatacept
  • Animals
  • Antibodies, Monoclonal / pharmacology*
  • Cardiotonic Agents / pharmacology
  • Cell Differentiation / drug effects
  • Cell Differentiation / immunology
  • Cyclosporine / pharmacology*
  • Embryonic Stem Cells / cytology
  • Embryonic Stem Cells / immunology
  • Embryonic Stem Cells / transplantation*
  • Endothelial Cells / immunology
  • Endothelial Cells / transplantation
  • Graft Rejection / immunology
  • Graft Rejection / prevention & control*
  • Humans
  • Immune Tolerance
  • Immunoconjugates / pharmacology*
  • Immunosuppression Therapy / methods
  • Immunosuppressive Agents / pharmacology*
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Myocardial Infarction / immunology
  • Myocardial Infarction / pathology
  • Myocardial Infarction / surgery
  • Prednisone / pharmacology*
  • Random Allocation

Substances

  • Antibodies, Monoclonal
  • Cardiotonic Agents
  • Immunoconjugates
  • Immunosuppressive Agents
  • anti-LFA-1 monoclonal antibody
  • Abatacept
  • Cyclosporine
  • Prednisone