Proangiogenic M2-type macrophages and choroidal neovascularization

NIH RePORTER · NIH · R01 · $454,331 · view on reporter.nih.gov ↗

Abstract

SUMMARY Macrophages infiltrate the site of inflammation and polarize to either antiangiogenic M1-type macrophages or proangiogenic M2-type macrophages, depending on the presence of various cytokines and other external factors. Proangiogenic M2-type macrophages are major contributors to inflammatory angiogenesis in many common diseases, in part by secreting proangiogenic factors, such as VEGF-A or IL-1b. Notably, M2-type macrophages accumulate in areas of choroidal neovascularization (CNV) in patients with neovascular AMD. The increase in M2-type macrophage-derived cytokines in eyes of patients with neovascular AMD has implicated this cell population as a major driver of CNV pathogenesis. This hypothesis is further supported by the observation of an accumulation of M2-type macrophages in laser-induced CNV or in a genetic VEGF-A-induced mouse model of neovascular AMD. Ablation of macrophages in laser-induced CNV, which are predominantly M2-type macrophages, blocked CNV, whereas administration of M2-type macrophages in the eye promoted CNV. Based on these findings we propose that pharmacologic therapies that prevent M2-type polarization of macrophages can serve as a novel approach to potently inhibit CNV progression in patients with neovascular AMD. The limited understanding of the signaling mechanisms that are regulating M1- versus M2-type polarization of macrophages has hindered the identification of molecular targets and pharmacologic inhibitors to selectively block M2-type macrophage polarization. To address this unmet need, we have performed global quantitative time-course proteomics and phosphoproteomics and identified kinase activation events that are associated with M1- versus M2-type macrophage polarization. Furthermore, we identified in chemical screens pharmacologic inhibitors of M2-type polarization that selectively block M2- but not M1-type polarization. Thus, the combination of these two approaches provides us now with a unique resource to establish novel therapies that selectively block proangiogenic M2- but not antiangiogenic M1-type macrophages in CNV. In proof-of-principle experiments we can show that two of the identified inhibitors, the MEK inhibitor trametinib and the HDAC inhibitor panobinostat, blocked M2-type macrophage polarization in CNV lesions and potently inhibited CNV lesion formation in laser- induced CNV experiments. Our proposed experiments will test identified kinase and non-kinase inhibitors in a systematic manner for their ability to selectively block M2-type polarization in detailed in vitro experiments as well as in three well-established mouse models of neovascular AMD. Our proposal is based on extensive preliminary data that provide a strong scientific premise. The proposed experiments have high rigor and important clinical relevance and will likely lead to novel therapeutic approaches for neovascular AMD.

Key facts

NIH application ID
10893015
Project number
5R01EY033360-03
Recipient
MASSACHUSETTS GENERAL HOSPITAL
Principal Investigator
Alexander Georg Marneros
Activity code
R01
Funding institute
NIH
Fiscal year
2024
Award amount
$454,331
Award type
5
Project period
2022-09-01 → 2026-07-31