Dissecting the complement pathway in hepatic injury and regeneration with a novel protective strategy

J Exp Med. 2014 Aug 25;211(9):1793-805. doi: 10.1084/jem.20131902. Epub 2014 Aug 11.

Abstract

Liver resection is commonly performed under ischemic conditions, resulting in two types of insult to the remnant liver: ischemia reperfusion injury (IRI) and loss of liver mass. Complement inhibition is recognized as a potential therapeutic modality for IRI, but early complement activation products are also essential for liver regeneration. We describe a novel site-targeted murine complement inhibitor, CR2-CD59, which specifically inhibits the terminal membrane attack complex (MAC), and we use this protein to investigate the complement-dependent balance between liver injury and regeneration in a clinical setting of pharmacological inhibition. CR2-CD59 did not impact in vivo generation of C3 and C5 activation products but was as effective as the C3 activation inhibitor CR2-Crry at ameliorating hepatic IRI, indicating that the MAC is the principle mediator of hepatic IRI. Furthermore, unlike C3 or C5 inhibition, CR2-CD59 was not only protective but significantly enhanced hepatocyte proliferation after partial hepatectomy, including when combined with ischemia and reperfusion. Remarkably, CR2-CD59 also enhanced regeneration after 90% hepatectomy and improved long-term survival from 0 to 70%. CR2-CD59 functioned by increasing hepatic TNF and IL-6 levels with associated STAT3 and Akt activation, and by preventing mitochondrial depolarization and allowing recovery of ATP stores.

Publication types

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

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • CD59 Antigens / administration & dosage
  • CD59 Antigens / metabolism
  • Complement Activation*
  • Complement Membrane Attack Complex / antagonists & inhibitors
  • Cytokines / metabolism
  • Disease Models, Animal
  • Hepatectomy / adverse effects
  • Kinetics
  • Liver / immunology
  • Liver / injuries*
  • Liver / physiopathology
  • Liver Failure, Acute / etiology
  • Liver Failure, Acute / immunology
  • Liver Failure, Acute / therapy
  • Liver Regeneration / immunology*
  • Liver Regeneration / physiology*
  • Liver Transplantation / adverse effects
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitochondria, Liver / metabolism
  • Receptors, Complement 3d / administration & dosage
  • Receptors, Complement 3d / metabolism
  • Recombinant Fusion Proteins / administration & dosage
  • Recombinant Fusion Proteins / metabolism
  • Reperfusion Injury / immunology
  • Reperfusion Injury / physiopathology
  • Reperfusion Injury / prevention & control*
  • Signal Transduction
  • Tissue Distribution

Substances

  • CD59 Antigens
  • CR2-Crry fusion protein, mouse
  • Complement Membrane Attack Complex
  • Cytokines
  • Receptors, Complement 3d
  • Recombinant Fusion Proteins
  • Adenosine Triphosphate