Rapid copper acquisition by developing murine mesothelioma: decreasing bioavailable copper slows tumor growth, normalizes vessels and promotes T cell infiltration

PLoS One. 2013 Aug 27;8(8):e73684. doi: 10.1371/journal.pone.0073684. eCollection 2013.

Abstract

Copper, an essential trace element acquired through nutrition, is an important co-factor for pro-angiogenic factors including vascular endothelial growth factor (VEGF). Decreasing bioavailable copper has been used as an anti-angiogenic and anti-cancer strategy with promising results. However, the role of copper and its potential as a therapy in mesothelioma is not yet well understood. Therefore, we monitored copper levels in progressing murine mesothelioma tumors and analyzed the effects of lowering bioavailable copper. Copper levels in tumors and organs were assayed using atomic absorption spectrophotometry. Mesothelioma tumors rapidly sequestered copper at early stages of development, the copper was then dispersed throughout growing tumor tissues. These data imply that copper uptake may play an important role in early tumor development. Lowering bioavailable copper using the copper chelators, penicillamine, trientine or tetrathiomolybdate, slowed in vivo mesothelioma growth but did not provide any cures similar to using cisplatin chemotherapy or anti-VEGF receptor antibody therapy. The impact of copper lowering on tumor blood vessels and tumor infiltrating T cells was measured using flow cytometry and confocal microscopy. Copper lowering was associated with reduced tumor vessel diameter, reduced endothelial cell proliferation (reduced Ki67 expression) and lower surface ICAM/CD54 expression implying reduced endothelial cell activation, in a process similar to endothelial normalization. Copper lowering was also associated with a CD4(+) T cell infiltrate. In conclusion, these data suggest copper lowering is a potentially useful anti-mesothelioma treatment strategy that slows tumor growth to provide a window of opportunity for inclusion of other treatment modalities to improve patient outcomes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Proliferation / drug effects
  • Chelating Agents / pharmacology*
  • Copper / metabolism*
  • Endothelial Cells / immunology
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Female
  • Humans
  • Intercellular Adhesion Molecule-1 / metabolism
  • Ki-67 Antigen / metabolism
  • Mesothelioma* / drug therapy
  • Mesothelioma* / immunology
  • Mesothelioma* / metabolism
  • Mesothelioma* / pathology
  • Mice
  • Neoplasm Proteins / metabolism
  • Neovascularization, Pathologic* / drug therapy
  • Neovascularization, Pathologic* / immunology
  • Neovascularization, Pathologic* / metabolism
  • Neovascularization, Pathologic* / pathology
  • T-Lymphocytes* / immunology
  • T-Lymphocytes* / metabolism
  • T-Lymphocytes* / pathology

Substances

  • Chelating Agents
  • Ki-67 Antigen
  • Neoplasm Proteins
  • Intercellular Adhesion Molecule-1
  • Copper

Grants and funding

This work was supported by the Cancer Council of WA and the Dust Diseases Board of NSW. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.