Interleukin-1alpha promotes angiogenesis in vivo via VEGFR-2 pathway by inducing inflammatory cell VEGF synthesis and secretion

FASEB J. 2002 Sep;16(11):1471-3. doi: 10.1096/fj.02-0134fje. Epub 2002 Jul 18.

Abstract

During inflammation, functional changes occur in the vasculature, including extensive endothelial cell mitotic activity and remodeling of capillaries. Interleukin-1alpha (IL-1alpha)is a prototypical proinflammatory cytokine. Vascular endothelial growth factor (VEGF) is a strong endothelial cell-specific mitogen that exerts a pivotal role in angiogenesis under physiological and pathological conditions. We show that IL-1alpha stimulates VEGF secretion by human peripheral blood mononuclear cells (PBMNCs) in a dose-dependent manner. This represents induction of de novo VEGF synthesis, as an induction of VEGF mRNA was observed. Also, the release of VEGF was blocked by cycloheximide. Reverse transcription-polymerase chain reaction (RT-PCR) detected four VEGF splice variants in unstimulated and in IL-1alpha-stimulated PBMNCs. In vivo in mice, subcutaneously administered IL-1alpha caused a strong local angiogenic response, which was accompanied by an infiltrate of VEGF-expressing inflammatory cells. The angiogenic effect of IL-1a was blocked when the mice were treated with VEGF receptor 2 (VEGFR-2) neutralizing antibodies. VEGFR-1 blocking antibodies had a marginal inhibitory effect on IL-1alpha-induced angiogenesis. These observations indicate that IL-1alpha induces angiogenesis by activating the VEGF-VEGFR-2 signaling pathway between inflammatory cells and blood vessel endothelial cells. This novel mechanism of IL-1alpha-action may enhance the shift to angiogenic phenotype in various conditions designated by excessive angiogenesis.

MeSH terms

  • Alternative Splicing
  • Animals
  • Blood Vessels / anatomy & histology
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Endothelial Growth Factors / biosynthesis
  • Endothelial Growth Factors / genetics
  • Endothelial Growth Factors / metabolism*
  • Humans
  • Interleukin-1 / pharmacology*
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / metabolism*
  • Lymphokines / biosynthesis
  • Lymphokines / genetics
  • Lymphokines / metabolism*
  • Mice
  • Models, Biological
  • Neovascularization, Physiologic*
  • RNA, Messenger / biosynthesis
  • Receptor Protein-Tyrosine Kinases / physiology*
  • Receptors, Growth Factor / physiology*
  • Receptors, Vascular Endothelial Growth Factor
  • Signal Transduction
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors

Substances

  • Endothelial Growth Factors
  • Interleukin-1
  • Lymphokines
  • RNA, Messenger
  • Receptors, Growth Factor
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors
  • Receptor Protein-Tyrosine Kinases
  • Receptors, Vascular Endothelial Growth Factor