α-1 Antitrypsin Enhances Islet Engraftment by Suppression of Instant Blood-Mediated Inflammatory Reaction

Diabetes. 2017 Apr;66(4):970-980. doi: 10.2337/db16-1036. Epub 2017 Jan 9.

Abstract

Islet cell transplantation has limited effectiveness because of an instant blood-mediated inflammatory reaction (IBMIR) that occurs immediately after cell infusion and leads to dramatic β-cell death. In intraportal islet transplantation models using mouse and human islets, we demonstrated that α-1 antitrypsin (AAT; Prolastin-C), a serine protease inhibitor used for the treatment of AAT deficiency, inhibits IBMIR and cytokine-induced inflammation in islets. In mice, more diabetic recipients reached normoglycemia after intraportal islet transplantation when they were treated with AAT compared with mice treated with saline. AAT suppressed blood-mediated coagulation pathways by diminishing tissue factor production, reducing plasma thrombin-antithrombin complex levels and fibrinogen deposition on islet grafts, which correlated with less graft damage and apoptosis. AAT-treated mice showed reduced serum tumor necrosis factor-α levels, decreased lymphocytic infiltration, and decreased nuclear factor (NF)-κB activation compared with controls. The potent anti-inflammatory effect of AAT is possibly mediated by suppression of c-Jun N-terminal kinase (JNK) phosphorylation. Blocking JNK activation failed to further reduce cytokine-induced apoptosis in β-cells. Taken together, AAT significantly improves islet graft survival after intraportal islet transplantation by mitigation of coagulation in IBMIR and suppression of cytokine-induced JNK and NF-κB activation. AAT-based therapy has the potential to improve graft survival in human islet transplantation and other cellular therapies on the horizon.

Publication types

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

MeSH terms

  • Animals
  • Antithrombin III / drug effects
  • Antithrombin III / metabolism
  • Apoptosis / drug effects*
  • Apoptosis / immunology
  • Blood Glucose / metabolism
  • Cell Death / drug effects
  • Cytokines / drug effects*
  • Cytokines / immunology
  • Diabetes Mellitus, Experimental / metabolism
  • Diabetes Mellitus, Experimental / surgery*
  • Fibrinogen / drug effects
  • Fibrinogen / metabolism
  • Graft Survival / drug effects
  • Graft Survival / immunology
  • Humans
  • Inflammation / immunology
  • Insulin-Secreting Cells / drug effects*
  • Islets of Langerhans / drug effects*
  • Islets of Langerhans / immunology
  • Islets of Langerhans / metabolism
  • Islets of Langerhans Transplantation*
  • JNK Mitogen-Activated Protein Kinases / drug effects
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Mice
  • NF-kappa B / drug effects
  • NF-kappa B / immunology
  • Peptide Hydrolases / drug effects
  • Peptide Hydrolases / metabolism
  • Phosphorylation / drug effects
  • Serine Proteinase Inhibitors / pharmacology*
  • Thromboplastin / drug effects
  • Thromboplastin / metabolism
  • Transplantation, Heterologous
  • Transplantation, Homologous
  • Tumor Necrosis Factor-alpha / drug effects
  • Tumor Necrosis Factor-alpha / immunology
  • alpha 1-Antitrypsin / pharmacology*

Substances

  • Blood Glucose
  • Cytokines
  • NF-kappa B
  • Serine Proteinase Inhibitors
  • Tumor Necrosis Factor-alpha
  • alpha 1-Antitrypsin
  • antithrombin III-protease complex
  • Antithrombin III
  • Fibrinogen
  • Thromboplastin
  • JNK Mitogen-Activated Protein Kinases
  • Peptide Hydrolases