Targeting of tumour-infiltrating macrophages via CCL2/CCR2 signalling as a therapeutic strategy against hepatocellular carcinoma

Gut. 2017 Jan;66(1):157-167. doi: 10.1136/gutjnl-2015-310514. Epub 2015 Oct 9.

Abstract

Objective: Hepatocellular carcinoma (HCC) is an aggressive malignancy with limited effective treatment options. An alternative strategy is to target cells, such as tumour-infiltrating macrophages, in the HCC tumour microenvironment. The CCL2/CCR2 axis is required for recruitment of monocytes/macrophages and is implicated in various aspects of liver pathology, including HCC. We investigated the feasibility of CCL2/CCR2 as a therapeutic target against HCC.

Design: CCL2 expression was analysed in two independent HCC cohorts. Growth of three murine HCC cells was evaluated in an orthotopic model, a postsurgical recurrence model and a subcutaneous model in mice after blocking CCL2/CCR2 axis by a novel CCR2 antagonist or knocking out of host CCR2. In vivo macrophage or T cell depletion and in vitro cell coculture were further conducted to investigate CCL2/CCR2-mediated crosstalk between tumour-associated macrophages (TAMs) and tumour cells.

Result: CCL2 is overexpressed in human liver cancers and is prognostic for patients with HCC. Blockade of CCL2/CCR2 signalling with knockout of CCR2 or with a CCR2 antagonist inhibits malignant growth and metastasis, reduces postsurgical recurrence, and enhances survival. Further, therapeutic blocking of the CCL2/CCR2 axis inhibits the recruitment of inflammatory monocytes, infiltration and M2-polarisation of TAMs, resulting in reversal of the immunosuppression status of the tumour microenvironment and activation of an antitumorous CD8+ T cell response.

Conclusions: In patients with liver cancer, CCL2 is highly expressed and is a prognostic factor. Blockade of CCL2/CCR2 signalling suppresses murine liver tumour growth via activating T cell antitumour immune response. The results demonstrate the translational potential of CCL2/CCR2 blockade for treatment of HCCs.

Keywords: CELL BIOLOGY; CHEMOKINES; HEPATOCELLULAR CARCINOMA; IMMUNOLOGY IN HEPATOLOGY; MACROPHAGES.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / immunology
  • Carcinoma, Hepatocellular / drug therapy
  • Carcinoma, Hepatocellular / immunology*
  • Carcinoma, Hepatocellular / metabolism*
  • Cell Communication
  • Cell Line, Tumor
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism*
  • Coculture Techniques
  • Disease Models, Animal
  • Gene Knockout Techniques
  • Humans
  • Liver Neoplasms / drug therapy
  • Liver Neoplasms / immunology*
  • Liver Neoplasms / metabolism*
  • Liver Neoplasms, Experimental / drug therapy
  • Liver Neoplasms, Experimental / immunology*
  • Liver Neoplasms, Experimental / metabolism*
  • Lymphocyte Activation / drug effects
  • Lymphocyte Depletion
  • Lymphocytes, Tumor-Infiltrating / drug effects
  • Macrophages / immunology*
  • Mice
  • Neoplasm Recurrence, Local / prevention & control*
  • Prognosis
  • Receptors, CCR2 / antagonists & inhibitors
  • Receptors, CCR2 / genetics
  • Receptors, CCR2 / metabolism*
  • Retrospective Studies
  • Signal Transduction / drug effects
  • Tumor Escape
  • Tumor Microenvironment

Substances

  • CCL2 protein, human
  • CCR2 protein, human
  • Ccl2 protein, mouse
  • Ccr2 protein, mouse
  • Chemokine CCL2
  • Receptors, CCR2