A novel pro-angiogenic function for interferon-γ-secreting natural killer cells

Invest Ophthalmol Vis Sci. 2014 May 2;55(5):2885-92. doi: 10.1167/iovs.14-14093.

Abstract

Purpose: To explore the function of natural killer (NK) cells in inflammatory angiogenesis in mice.

Methods: To study ocular angiogenic responses we used the cornea BFGF micropellet and the laser-induced choroidal neovascularization (CNV) mouse models (C57BL/6). To deplete NK cells in these models, we injected an anti-NK1.1 antibody or an isotype antibody as a control. Corneas or choroids were immunohistochemically stained for blood vessels (CD31), macrophages (F4/80), or CNV (isolectin-IB4). Vascular endothelial growth factors (VEGF), IFN-γ, or TNF-α levels were measured by real-time quantitative PCR (qPCR) or flow cytometry. A coculture assay of macrophages, NK cells, and human umbilical vein endothelial cells (HUVECs) was analyzed morphometrically to examine the ability of NK cells to induce angiogenesis in vitro.

Results: Our data demonstrate that in vivo depletion of NK cells leads to a significant reduction of corneal angiogenesis and CNV. Furthermore, NK cell depletion reduces macrophage infiltration into the cornea and mRNA expression levels of VEGF-A, VEGF-C, and VEGFR3 at day 7 after micropellet insertion. In the laser-induced CNV model, our data show that NK cell depletion leads to decreased areas of CNV and significantly reduced mRNA expression of VEGFs and IFN-γ in the choroid. An in vitro coculture assay shows an IFN-γ-dependent increase in VEGF expression levels, thereby increasing endothelial cell proliferation.

Conclusions: Our findings demonstrate a novel pro-angiogenic function for NK cells, indicating that IFN-γ-secreting NK cells can induce angiogenesis by promoting enhanced VEGF expression by macrophages.

Keywords: NK cells; endothelial cells; interferons; macrophages; neovascularization.

Publication types

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

MeSH terms

  • Animals
  • Choroidal Neovascularization / metabolism
  • Choroidal Neovascularization / pathology
  • Choroidal Neovascularization / physiopathology*
  • Cornea / blood supply
  • Cornea / metabolism
  • Disease Models, Animal
  • Immunohistochemistry
  • Interferon-gamma / genetics
  • Interferon-gamma / metabolism*
  • Killer Cells, Natural / metabolism
  • Killer Cells, Natural / physiology*
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Neovascularization, Pathologic / etiology*
  • RNA, Messenger / metabolism
  • Vascular Endothelial Growth Factors / metabolism*

Substances

  • RNA, Messenger
  • Vascular Endothelial Growth Factors
  • Interferon-gamma