Vascular dysfunction elicited by a cross talk between periaortic adipose tissue and the vascular wall is reversed by pioglitazone

Cardiovasc Ther. 2018 Jun;36(3):e12322. doi: 10.1111/1755-5922.12322. Epub 2018 Mar 7.

Abstract

Aim: Perivascular adipose tissue (PVAT) is in intimate contact with the vessel wall and extravascular PVAT-derived inflammatory mediators may adversely influence atherosclerotic plaque formation and stability through outside-to-inside signaling. We sought to investigate the role of PVAT on the atheroma development in an experimental animal model of metabolic syndrome (MS) associated with oxidative stress and low-grade inflammatory state. We also studied the effect of pioglitazone an insulin sensitizer, on the aortic wall and its surrounding PVAT, considering a bi-directional communication between both layers.

Methods: Apolipoprotein E-deficient mice (ApoE-/- ) were fed with standard diet (CD, control diet) or fructose overload (10% w/v) (FD, fructose diet) for 8 weeks and treated with or without pioglitazone the latest 4 weeks.

Results: Biochemical variables show that glycemia and lipid peroxidation determined by thiobarbituric acid reactive species (TBARS) significantly increased in FD-fed ApoE-/- mice. FD significantly increased aortic PVAT expression of oxidative stress associated genes: p22phox , Nox1, Nox2, Nox4 and p47phox , and proinflammatory genes: Visfatin, MCP-1, and MMP-9. Pioglitazone diminished PVAT-oxidative damage elicited by fructose treatment and markedly down-regulated proinflammatory markers. Even pioglitazone did not prevent the development of the aortic atheroma plaques stimulated by FD, significantly diminished VCAM-1 expression, MMP-9 expression and activity in aortic media wall and significantly reduced the accumulation of lipids and macrophages in atheroma plaques.

Conclusion: Our results support the fact that PVAT contributes to the development and progression of cardiovascular disease by underlying mechanisms elicited by "outside-in" signaling. Treatment with pioglitazone may offer a new effect on the whole vessel wall, promoting the stability of advanced atherosclerotic plaques.

Keywords: adipose tissue; atherosclerosis; oxidative stress; pioglitazone.

MeSH terms

  • Adipose Tissue / pathology
  • Adipose Tissue / physiopathology*
  • Animals
  • Aorta / physiopathology*
  • Apolipoproteins E / genetics
  • Blood Glucose / metabolism
  • Blood Vessels / pathology
  • Blood Vessels / physiopathology*
  • Fructose / antagonists & inhibitors
  • Fructose / toxicity
  • Hypoglycemic Agents / therapeutic use*
  • Lipid Peroxidation / drug effects
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Oxidative Stress / drug effects
  • Oxidative Stress / genetics
  • Pioglitazone
  • Plaque, Atherosclerotic / pathology
  • Signal Transduction / drug effects
  • Thiazolidinediones / therapeutic use*
  • Vascular Diseases / drug therapy*
  • Vascular Diseases / etiology*
  • Vascular Diseases / pathology

Substances

  • Apolipoproteins E
  • Blood Glucose
  • Hypoglycemic Agents
  • Thiazolidinediones
  • Fructose
  • Pioglitazone