Targeting Unc5b in macrophages drives atherosclerosis regression and pro-resolving immune cell function

Proc Natl Acad Sci U S A. 2024 Oct 29;121(44):e2412690121. doi: 10.1073/pnas.2412690121. Epub 2024 Oct 22.

Abstract

Atherosclerosis results from lipid-driven inflammation of the arterial wall that fails to resolve. Imbalances in macrophage accumulation and function, including diminished migratory capacity and defective efferocytosis, fuel maladaptive inflammation and plaque progression. The neuroimmune guidance cue netrin-1 has dichotomous roles in inflammation partly due to its multiple receptors; in atherosclerosis, netrin-1 promotes macrophage survival and retention via its receptor Unc5b. To minimize the pleiotropic effects of targeting netrin-1, we tested the therapeutic potential of deleting Unc5b in mice with advanced atherosclerosis. We generated Unc5bfl/flCx3cr1creERT2/WT mice, which allowed conditional deletion of Un5b (∆Unc5b) in monocytes and macrophages by tamoxifen injection. After inducing advanced atherosclerosis by hepatic PCSK9 overexpression and western diet feeding for 20 wk, Unc5b was deleted and hypercholesterolemia was normalized to simulate clinical lipid management. Deletion of myeloid Unc5b led to a 40% decrease in atherosclerotic plaque burden and reduced plaque complexity compared to Unc5bfl/flCx3cr1WT/WT littermate controls (Ctrl). Consistently, plaque macrophage content was reduced by 50% in ∆Unc5b mice due to reduced plaque Ly6Chi monocyte recruitment and macrophage retention. Compared to Ctrl mice, plaques in ∆Unc5b mice had reduced necrotic area and fewer apoptotic cells, which correlated with improved efferocytotic capacity by Unc5b-deficient macrophages in vivo and in vitro. Beneficial changes in macrophage dynamics in the plaque upon Unc5b deletion were accompanied by an increase in atheroprotective T cell populations, including T-regulatory and Th2 cells. Our data identify Unc5b in advanced atherosclerosis as a therapeutic target to induce pro-resolving restructuring of the plaque immune cells and to promote atherosclerosis regression.

Keywords: Treg; atherosclerosis; efferocytosis; inflammation; regression.

MeSH terms

  • Animals
  • Atherosclerosis* / immunology
  • Atherosclerosis* / metabolism
  • Atherosclerosis* / pathology
  • Inflammation / immunology
  • Inflammation / metabolism
  • Inflammation / pathology
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Male
  • Mice
  • Mice, Knockout
  • Monocytes / immunology
  • Monocytes / metabolism
  • Netrin Receptors* / metabolism
  • Netrin-1 / genetics
  • Netrin-1 / metabolism
  • Plaque, Atherosclerotic* / metabolism
  • Plaque, Atherosclerotic* / pathology
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism

Substances

  • Ly-6C antigen, mouse
  • Netrin Receptors
  • Netrin-1
  • Receptors, Cell Surface
  • Unc5b protein, mouse