Pharmacological inhibition of the chemokine CCL2 (MCP-1) diminishes liver macrophage infiltration and steatohepatitis in chronic hepatic injury

Gut. 2012 Mar;61(3):416-26. doi: 10.1136/gutjnl-2011-300304. Epub 2011 Aug 3.

Abstract

Objective: Monocyte chemoattractant protein-1 (MCP-1, CCL2), the primary ligand for chemokine receptor C-C chemokine receptor 2 (CCR2), is increased in livers of patients with non-alcoholic steatohepatitis (NASH) and murine models of steatohepatitis and fibrosis. It was recently shown that monocyte/macrophage infiltration into the liver upon injury is critically regulated by the CCL2/CCR2 axis and is functionally important for perpetuating hepatic inflammation and fibrogenesis. The structured L-enantiomeric RNA oligonucleotide mNOX-E36 (a so-called Spiegelmer) potently binds and inhibits murine MCP-1. Pharmacological inhibition of MCP-1 with mNOX-E36 was investigated in two murine models of chronic liver diseases.

Methods: Pharmacological inhibition of MCP-1 by thrice-weekly mNOX-E36 subcutaneously was tested in murine models of acute or chronic carbon tetrachloride (CCl(4))- and methionine-choline-deficient (MCD) diet-induced chronic hepatic injury in vivo.

Results: Antagonising MCP-1 by mNOX-E36 efficiently inhibited murine monocyte chemotaxis in vitro as well as migration of Gr1(+) (Ly6C(+)) blood monocytes into the liver upon acute toxic injury in vivo. In murine models of CCl(4)- and MCD diet-induced hepatic injury, the infiltration of macrophages into the liver was significantly decreased in anti-MCP-1-treated mice as found by fluorescence-activated cell sorting (FACS) analysis and immunohistochemistry. In line with lower levels of intrahepatic macrophages, proinflammatory cytokines (tumour necrosis factor α, interferon γ and interleukin 6) were significantly reduced in liver tissue. Overall fibrosis progression over 6 (CCl(4)) or 8 weeks (MCD diet) was not significantly altered by anti-MCP-1 treatment. However, upon MCD diet challenge a lower level of fatty liver degeneration (histology score, Oil red O staining, hepatic triglyceride content, lipogenesis genes) was detected in mNOX-E36-treated animals. mNOX-E36 also ameliorated hepatic steatosis upon therapeutic administration.

Conclusions: These results demonstrate the successful pharmacological inhibition of hepatic monocyte/macrophage infiltration by blocking MCP-1 during chronic liver damage in two in vivo models. The associated ameliorated steatosis development suggests that inhibition of MCP-1 is an interesting novel approach for pharmacological treatment in liver inflammation and steatohepatitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Disease
  • Animals
  • Aptamers, Nucleotide / pharmacology*
  • Aptamers, Nucleotide / therapeutic use
  • Bone Marrow Cells / drug effects
  • Bone Marrow Cells / physiology
  • Carbon Tetrachloride
  • Cells, Cultured
  • Chemical and Drug Induced Liver Injury / complications
  • Chemical and Drug Induced Liver Injury / drug therapy
  • Chemical and Drug Induced Liver Injury / pathology
  • Chemical and Drug Induced Liver Injury, Chronic / complications*
  • Chemical and Drug Induced Liver Injury, Chronic / drug therapy
  • Chemical and Drug Induced Liver Injury, Chronic / pathology
  • Chemokine CCL2 / antagonists & inhibitors*
  • Chemokine CCL2 / physiology
  • Chemotaxis / drug effects
  • Cytokines / metabolism
  • Disease Progression
  • Drug Evaluation, Preclinical / methods
  • Fatty Liver / drug therapy
  • Fatty Liver / etiology
  • Fatty Liver / prevention & control*
  • Liver / metabolism
  • Liver / pathology
  • Liver Cirrhosis, Experimental / etiology
  • Liver Cirrhosis, Experimental / prevention & control
  • Macrophages / drug effects*
  • Macrophages / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Non-alcoholic Fatty Liver Disease

Substances

  • Aptamers, Nucleotide
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Cytokines
  • NOX-E36-3'PEG, mouse
  • Carbon Tetrachloride