Complement Activation in Arterial and Venous Thrombosis is Mediated by Plasmin

EBioMedicine. 2016 Feb 6:5:175-82. doi: 10.1016/j.ebiom.2016.02.011. eCollection 2016 Mar.

Abstract

Thrombus formation leading to vaso-occlusive events is a major cause of death, and involves complex interactions between coagulation, fibrinolytic and innate immune systems. Leukocyte recruitment is a key step, mediated partly by chemotactic complement activation factors C3a and C5a. However, mechanisms mediating C3a/C5a generation during thrombosis have not been studied. In a murine venous thrombosis model, levels of thrombin-antithrombin complexes poorly correlated with C3a and C5a, excluding a central role for thrombin in C3a/C5a production. However, clot weight strongly correlated with C5a, suggesting processes triggered during thrombosis promote C5a generation. Since thrombosis elicits fibrinolysis, we hypothesized that plasmin activates C5 during thrombosis. In vitro, the catalytic efficiency of plasmin-mediated C5a generation greatly exceeded that of thrombin or factor Xa, but was similar to the recognized complement C5 convertases. Plasmin-activated C5 yielded a functional membrane attack complex (MAC). In an arterial thrombosis model, plasminogen activator administration increased C5a levels. Overall, these findings suggest plasmin bridges thrombosis and the immune response by liberating C5a and inducing MAC assembly. These new insights may lead to the development of strategies to limit thrombus formation and/or enhance resolution.

Keywords: Complement; FDP, fibrin degradation product; FeCl3, ferric chloride; Fibrinolysis; IL-8, interleukin-8; IVC, inferior vena cava; Leukocytes; MAC, membrane attack complex; MCP1-1, monocyte chemoattracant protein-1; NETs, neutrophil extracellular traps; PAR1, protease activated receptor 1; PPACK, Phe-Pro-Arg-chloromethylketone; R751, arginine 751; TAT, thrombin antithrombin; Thrombin; Thrombosis; VFKck, Val-Phe-Lys-chloromethylketone; VWF, von Willebrand factor; tPA, tissue-type plasminogen activator.

Publication types

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

MeSH terms

  • Animals
  • Antithrombin III / drug effects
  • Antithrombin III / immunology
  • Arteries / drug effects
  • Arteries / immunology*
  • Arteries / pathology
  • Complement Activation / drug effects
  • Complement Activation / immunology
  • Complement C3a / biosynthesis
  • Complement C3a / immunology
  • Complement C5a / biosynthesis
  • Complement C5a / immunology*
  • Complement Membrane Attack Complex / drug effects
  • Complement Membrane Attack Complex / immunology
  • Factor Xa / immunology
  • Factor Xa / metabolism
  • Fibrinolysin / immunology*
  • Fibrinolysin / metabolism
  • Humans
  • Mice
  • Peptide Hydrolases / drug effects
  • Peptide Hydrolases / immunology
  • Plasminogen Activators / administration & dosage
  • Thrombin / immunology
  • Thrombin / metabolism
  • Venous Thrombosis / drug therapy
  • Venous Thrombosis / immunology*
  • Venous Thrombosis / pathology

Substances

  • Complement Membrane Attack Complex
  • antithrombin III-protease complex
  • Complement C3a
  • Complement C5a
  • Antithrombin III
  • Peptide Hydrolases
  • Plasminogen Activators
  • Thrombin
  • Factor Xa
  • Fibrinolysin