Autoimmune pancreatitis in MRL/Mp mice is a T cell-mediated disease responsive to cyclosporine A and rapamycin treatment

Gut. 2014 Mar;63(3):494-505. doi: 10.1136/gutjnl-2012-303635. Epub 2013 Apr 5.

Abstract

Background: Autoimmune pancreatitis (AIP) in humans invariably responds to steroid treatment, but little is known about the underlying pathogenesis and the benefits of alternative treatments.

Objective: To study the pathogenesis, and the efficacy of alternative immunosuppressant agents in the MRL/Mp mouse model of AIP.

Design: MRL/Mp mice were pretreated for 4 weeks with polyinosinic:polycytidylic acid to induce AIP. Pancreatic sections of mice genetically deleted for CTLA-4 were analysed. Blockage of CTLA-4 was achieved by intraperitoneal antibody treatment with 2 μg/g anti-mouse-CD152. Subsequent therapeutic studies were performed for a period of 4 weeks using cyclosporine A (40 μg/g), rapamycin (1 μg/g) or azathioprine (15 μg/g).

Results: Blockage of CTLA-4 in MRL/Mp mice suppressed regulatory T cell (Treg) function and raised the effector T cell (Teff) response with subsequent histomorphological organ destruction, indicating that AIP is a T cell-driven disease. Using an established histopathological score, we found that dexamethasone, cyclosporine A and rapamycin, but less so azathioprine, reduced pancreatic damage. However, the beneficial effects of cyclosporine A and rapamycin were achieved via different mechanisms: cyclosporine A inhibited Teff activation and proliferation whereas rapamycin led to selective expansion of Tregs which subsequently suppressed the Teff response.

Conclusions: The calcineurin inhibitor cyclosporine A and the mammalian target of rapamycin (mTOR) inhibitor, rapamycin, improve the course of AIP in MRL/Mp mice via different mechanisms. These findings further support the concept of autoreactive T cells as key players in the pathogenesis of AIP and suggest that cyclosporine A and rapamycin should be considered for treatment of AIP in humans.

Keywords: Keywords: MRL/Mp mice, Treg, CTLA-4, Teff, rapamycin, cyclosporine A, azathioprine.

Publication types

  • Evaluation Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autoimmune Diseases / chemically induced
  • Autoimmune Diseases / drug therapy*
  • Autoimmune Diseases / immunology
  • Autoimmune Diseases / pathology
  • Azathioprine / therapeutic use
  • Biomarkers / metabolism
  • CTLA-4 Antigen / antagonists & inhibitors
  • Cell Proliferation / drug effects
  • Cyclosporine / pharmacology
  • Cyclosporine / therapeutic use*
  • Dexamethasone / therapeutic use
  • Drug Administration Schedule
  • Female
  • Flow Cytometry
  • Immunosuppressive Agents / pharmacology
  • Immunosuppressive Agents / therapeutic use*
  • Lymphocyte Activation / drug effects
  • Mice
  • Mice, Inbred Strains
  • Pancreas / drug effects
  • Pancreas / immunology*
  • Pancreas / pathology
  • Pancreatitis, Chronic / chemically induced
  • Pancreatitis, Chronic / drug therapy*
  • Pancreatitis, Chronic / immunology
  • Pancreatitis, Chronic / pathology
  • Poly I-C
  • Random Allocation
  • Sirolimus / pharmacology
  • Sirolimus / therapeutic use*
  • T-Lymphocyte Subsets / drug effects
  • T-Lymphocyte Subsets / metabolism*
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / metabolism
  • Treatment Outcome

Substances

  • Biomarkers
  • CTLA-4 Antigen
  • Ctla4 protein, mouse
  • Immunosuppressive Agents
  • Dexamethasone
  • Cyclosporine
  • Azathioprine
  • Poly I-C
  • Sirolimus