Targeted complement inhibitors protect against posttransplant cardiac ischemia and reperfusion injury and reveal an important role for the alternative pathway of complement activation

J Immunol. 2010 Dec 1;185(11):7007-13. doi: 10.4049/jimmunol.1001504. Epub 2010 Oct 20.

Abstract

Ischemia reperfusion injury (IRI) is an unavoidable event during solid organ transplantation and is a major contributor to early graft dysfunction and subsequent graft immunogenicity. In a therapeutic paradigm using targeted complement inhibitors, we investigated the role of complement, and specifically the alternative pathway of complement, in IRI to heart isografts. Mouse heterotopic isograft heart transplants were performed in C57BL/6 mice treated with a single injection of either CR2-Crry (inhibits all complement pathways) or CR2-fH (inhibits alternative complement pathway) immediately posttransplantation. Transplanted hearts were harvested at 12 and 48 h for analysis. Both inhibitors resulted in a significant reduction in myocardial IRI, as measured by histology and serum cardiac troponin I levels. Furthermore, compared with untreated controls, both inhibitors reduced graft complement deposition, neutrophil and macrophage infiltration, adhesion molecule expression (P-selectin, E-selectin, and I-CAM-1), and proinflammatory cytokine expression (TNF-α, IL-1β, KC, and MCP-1). The reduction in myocardial damage and cellular infiltration was not significantly different between CR2-Crry- and CR2-fH-treated mice, although adhesion molecule and cytokine levels were significantly lower in CR2-Crry-treated mice compared with CR2-fH-treated mice. In conclusion, the alternative complement pathway plays a major contributing role in myocardial IRI after heart transplantation, and local (targeted) complement inhibition has the potential to provide an effective and safe therapeutic strategy to reduce graft injury. Although total complement blockade may be somewhat more efficacious in terms of reducing inflammation, specific blockade of the alternative pathway is likely to be less immunosuppressive in an already immunocompromised recipient.

Publication types

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

MeSH terms

  • Animals
  • Complement Factor H / physiology*
  • Complement Factor H / therapeutic use
  • Complement Inactivator Proteins / physiology*
  • Complement Inactivator Proteins / therapeutic use
  • Complement Pathway, Alternative / immunology*
  • Cytokines / antagonists & inhibitors
  • Cytokines / biosynthesis
  • Drug Delivery Systems / methods
  • Heart Transplantation / immunology*
  • Heart Transplantation / pathology
  • Leukocyte Count
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Myocardial Reperfusion Injury / immunology
  • Myocardial Reperfusion Injury / pathology
  • Myocardial Reperfusion Injury / prevention & control*
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Neutrophils / pathology
  • Random Allocation
  • Receptors, Complement 3d / physiology
  • Receptors, Complement 3d / therapeutic use
  • Recombinant Fusion Proteins / physiology*
  • Recombinant Fusion Proteins / therapeutic use
  • Transplantation, Homologous

Substances

  • CR2-Crry fusion protein, mouse
  • Complement Inactivator Proteins
  • Cytokines
  • Receptors, Complement 3d
  • Recombinant Fusion Proteins
  • Complement Factor H