Paracrine modulation of CXCR4 by IGF-1 and VEGF: implications for choroidal neovascularization

Invest Ophthalmol Vis Sci. 2010 May;51(5):2697-704. doi: 10.1167/iovs.09-4137. Epub 2009 Dec 10.

Abstract

Purpose: Modulators of angiogenesis typically work in an orchestrated manner. The authors examined the interaction between insulinlike growth factor (IGF)-1, vascular endothelial growth factor (VEGF), and stromal derived factor (SDF)-1 in vivo and in vitro using angiogenesis models.

Methods: The angiogenic effect of SDF-1, alone or in combination with IGF-1 and VEGF, was assessed in human lung microvascular endothelial cells using capillary tube formation and thymidine incorporation. Immunohistochemical analysis for CD31, SDF-1, and CXCR4 was performed on mouse eyes 2 weeks after the initiation of laser rupture of Bruch's membrane, a choroidal neovascularization (CNV) model. CXCR4 antagonist and CXCR4 blocking antibody were tested on inhibition of CNV lesion size in this model. Real-time PCR was used to determine mRNA levels for SDF-1, VEGF, IGF-1, and their cognate receptors in the retinal pigment epithelium/choroid complex of mice that underwent this CNV model.

Results: IGF-1 and VEGF demonstrated an additive effect on SDF-1-induced in vitro angiogenesis. CXCR4 immunoreactivity was present in both normal and laser-injured mice at the laser burn site and at the ganglion cell layer, the anterior portion of the inner nuclear layer, photoreceptors, and choroidal stroma. SDF-1 was observed in identical locations but was not seen in photoreceptors. mRNA levels for SDF-1, VEGF, and IGF-1 and their receptors were increased after laser injury. CXCR4-neutralizing antibody reduced neovascularization when injected subretinally but not intraperitoneally or intravitreally.

Conclusions: The potent proangiogenic factors IGF-1 and VEGF both stimulate SDF-1-induced angiogenesis. Local inhibition of CXCR4 is required for an antiangiogenic effect in CNV lesions.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Angiogenic Proteins / pharmacology*
  • Animals
  • Chemokine CXCL12 / genetics
  • Chemokine CXCL12 / pharmacology
  • Choroidal Neovascularization / metabolism*
  • Choroidal Neovascularization / pathology
  • Disease Models, Animal
  • Endothelium, Vascular / drug effects*
  • Endothelium, Vascular / pathology
  • Humans
  • Injections
  • Injections, Intraperitoneal
  • Insulin-Like Growth Factor I / genetics
  • Insulin-Like Growth Factor I / pharmacology*
  • Laser Coagulation
  • Lung / cytology
  • Mice
  • Mice, Inbred C57BL
  • Paracrine Communication / physiology*
  • Platelet Endothelial Cell Adhesion Molecule-1 / genetics
  • Platelet Endothelial Cell Adhesion Molecule-1 / metabolism
  • RNA, Messenger / metabolism
  • Receptors, CXCR4 / antagonists & inhibitors
  • Receptors, CXCR4 / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Vascular Endothelial Growth Factor A / genetics
  • Vascular Endothelial Growth Factor A / pharmacology*
  • Vitreous Body

Substances

  • Angiogenic Proteins
  • CXCR4 protein, mouse
  • Chemokine CXCL12
  • Platelet Endothelial Cell Adhesion Molecule-1
  • RNA, Messenger
  • Receptors, CXCR4
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse
  • Insulin-Like Growth Factor I