Infiltration of COX-2-expressing macrophages is a prerequisite for IL-1 beta-induced neovascularization and tumor growth

J Clin Invest. 2005 Nov;115(11):2979-91. doi: 10.1172/JCI23298. Epub 2005 Oct 20.

Abstract

Inflammatory angiogenesis is a critical process in tumor progression and other diseases. The inflammatory cytokine IL-1beta promotes angiogenesis, tumor growth, and metastasis, but its mechanisms remain unclear. We examined the association between IL-1beta-induced angiogenesis and cell inflammation. IL-1beta induced neovascularization in the mouse cornea at rates comparable to those of VEGF. Neutrophil infiltration occurred on day 2. Macrophage infiltration occurred on days 4 and 6. The anti-Gr-1 Ab-induced depletion of infiltrating neutrophils did not affect IL-1beta- or VEGF-induced angiogenesis. The former was reduced in monocyte chemoattractant protein-1-deficient (MCP-1(-/-)) mice compared with wild-type mice. After day 4, clodronate liposomes, which kill macrophages, reduced IL-1beta-induced angiogenesis and partially inhibited VEGF-induced angiogenesis. Infiltrating macrophages near the IL-1beta-induced neovasculature were COX-2 positive. Lewis lung carcinoma cells expressing IL-1beta (LLC/IL-1beta) developed neovasculature with macrophage infiltration and enhanced tumor growth in wild-type but not MCP-1(-/-) mice. A COX-2 inhibitor reduced tumor growth, angiogenesis, and macrophage infiltration in LLC/IL-1beta. Thus, macrophage involvement might be a prerequisite for IL-1beta-induced neovascularization and tumor progression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Movement* / physiology
  • Chemokine CCL2 / deficiency
  • Chemokine CCL2 / genetics
  • Cornea / pathology
  • Cyclooxygenase 2 / biosynthesis
  • Cyclooxygenase 2 / genetics*
  • Interleukin-1 / physiology*
  • Macrophages / enzymology*
  • Macrophages / pathology*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasms / enzymology*
  • Neoplasms / pathology*
  • Neovascularization, Pathologic / metabolism*
  • Vascular Endothelial Growth Factor A / physiology

Substances

  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Interleukin-1
  • Vascular Endothelial Growth Factor A
  • Cyclooxygenase 2