Bone marrow angiotensin AT2 receptor deficiency aggravates atherosclerosis development by eliminating macrophage liver X receptor-mediated anti-atherogenic actions

J Renin Angiotensin Aldosterone Syst. 2015 Dec;16(4):936-46. doi: 10.1177/1470320314561138. Epub 2014 Dec 8.

Abstract

Background: Bone marrow (BM) Angiotensin II (Ang II) type 1 (AT1) receptor plays a crucial role in atherosclerosis development; however, the effect of BM Ang II type 2 (AT2) receptor on atherogenesis remains undefined.

Methods and results: We generated BM chimera apoE-deficient (apoE(-/-)) mice whose BM cells were repopulated with AT2-deficient (Agtr2(-/-)) or wild-type (Agtr2(+/+)) cells. After 2 months of a high-cholesterol diet, the atherosclerotic lesion area was significantly increased in the apoE(-/-)/BM-Agtr2(-/-) mice compared with the apoE(-/-)/BM-Agtr2(+/+) mice (51%, P < 0.05), accompanied by an augmented accumulation of lesion macrophages. Although phenotypic polarization in BM-derived macrophages and lipopolysaccharide-induced expression of proinflammatory cytokines in thioglycollate-induced peritoneal macrophages (TGPMs) were not affected by AT2-deficiency, mRNA and protein expression levels of macrophage liver X receptor β (LXRβ) were significantly decreased in Agtr2(-/-) TGPMs compared with Agtr2(+/+) TGPMs. Anti-inflammatory effects of LXR agonist (GW3965) were markedly inhibited in Agtr2(-/-) TGPMs. Furthermore, the expression levels of ATP-binding cassette transporter ABCA1 and CCR7 were much lower in Agtr2(-/-) TGPMs than Agtr2(+/+) TGPMs, accompanied by a significantly reduced cholesterol efflux.

Conclusions: Our findings demonstrate that BM-AT2 deficiency aggravates atherosclerosis, at least in part, by eliminating the anti-atherogenic properties of macrophages elicited by LXRβ activation.

Keywords: Angiotensin; atherosclerosis; liver X receptor; macrophage; receptor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter 1 / genetics
  • ATP Binding Cassette Transporter 1 / metabolism
  • Animals
  • Apolipoproteins E / deficiency
  • Atherosclerosis / genetics
  • Atherosclerosis / metabolism*
  • Atherosclerosis / pathology*
  • Biological Transport
  • Bone Marrow / drug effects
  • Bone Marrow / metabolism*
  • Cell Polarity
  • Cholesterol / metabolism
  • Gene Expression Regulation
  • Inflammation / pathology
  • Liver X Receptors
  • Macrophages, Peritoneal / metabolism*
  • Mice, Inbred C57BL
  • Orphan Nuclear Receptors / metabolism*
  • Phenotype
  • Receptor, Angiotensin, Type 2 / deficiency*
  • Receptor, Angiotensin, Type 2 / metabolism
  • Receptors, CCR7 / genetics
  • Receptors, CCR7 / metabolism
  • Thioglycolates

Substances

  • ABCA1 protein, mouse
  • ATP Binding Cassette Transporter 1
  • Apolipoproteins E
  • Ccr7 protein, mouse
  • Liver X Receptors
  • Orphan Nuclear Receptors
  • Receptor, Angiotensin, Type 2
  • Receptors, CCR7
  • Thioglycolates
  • 2-mercaptoacetate
  • Cholesterol