Beneficial impact of CCL2 and CCL12 neutralization on experimental malignant pleural effusion

PLoS One. 2013 Aug 14;8(8):e71207. doi: 10.1371/journal.pone.0071207. eCollection 2013.

Abstract

Using genetic interventions, we previously determined that C-C motif chemokine ligand 2 (CCL2) promotes malignant pleural effusion (MPE) formation in mice. Here we conducted preclinical studies aimed at assessing the specific therapeutic potential of antibody-mediated CCL2 blockade against MPE. For this, murine MPEs or skin tumors were generated in C57BL/6 mice by intrapleural or subcutaneous delivery of lung (LLC) or colon (MC38) adenocarcinoma cells. Human lung adenocarcinoma cells (A549) were used to induce MPEs in severe combined immunodeficient mice. Intraperitoneal antibodies neutralizing mouse CCL2 and/or CCL12, a murine CCL2 ortholog, were administered at 10 or 50 mg/kg every three days. We found that high doses of CCL2/12 neutralizing antibody treatment (50 mg/kg) were required to limit MPE formation by LLC cells. CCL2 and CCL12 blockade were equally potent inhibitors of MPE development by LLC cells. Combined CCL2 and CCL12 neutralization was also effective against MC38-induced MPE and prolonged the survival of mice in both syngeneic models. Mouse-specific CCL2-blockade limited A549-caused xenogeneic MPE, indicating that host-derived CCL2 also contributes to MPE precipitation in mice. The impact of CCL2/12 antagonism was associated with inhibition of immune and vascular MPE-related phenomena, such as inflammation, new blood vessel assembly and plasma extravasation into the pleural space. We conclude that CCL2 and CCL12 blockade are effective against experimental MPE induced by murine and human adenocarcinoma in mice. These results suggest that CCL2-targeted therapies may hold promise for future use against human MPE.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / complications
  • Adenocarcinoma / pathology
  • Adenocarcinoma of Lung
  • Animals
  • Antibodies, Neutralizing / immunology*
  • Antibodies, Neutralizing / therapeutic use*
  • Cell Line, Tumor
  • Cell Proliferation
  • Chemokine CCL2 / immunology*
  • Colonic Neoplasms / complications
  • Colonic Neoplasms / pathology
  • Humans
  • Lung Neoplasms / complications
  • Lung Neoplasms / pathology
  • Mice
  • Mice, Inbred C57BL
  • Monocyte Chemoattractant Proteins / immunology*
  • Pleural Effusion, Malignant / etiology
  • Pleural Effusion, Malignant / metabolism
  • Pleural Effusion, Malignant / therapy*

Substances

  • Antibodies, Neutralizing
  • Ccl12 protein, mouse
  • Chemokine CCL2
  • Monocyte Chemoattractant Proteins

Grants and funding

This work was supported in part by a European Research Council (http://erc.europa.eu/) Starting Independent Investigator Grant (http://erc.europa.eu/starting-grants) under the European Community’s Seventh Framework Program (FP7-IDEAS-ERC-StG-2010-260524-KRASHIMPE to GTS; http://cordis.europa.eu/search/index.cfm?fuseaction=proj.document&PJ_LANG=EN&PJ_RCN=11789622&pid=0&q=61222D4F193AC74A3C679CD344AD41B0&type=sim) and by the ‘Thorax’ Foundation, Athens, Greece (to CAK, SM, IK, and GTS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.