Inhibition of nuclear factor of activated T-cells (NFAT) suppresses accelerated atherosclerosis in diabetic mice

PLoS One. 2013 Jun 3;8(6):e65020. doi: 10.1371/journal.pone.0065020. Print 2014.

Abstract

Objective of the study: Diabetic patients have a much more widespread and aggressive form of atherosclerosis and therefore, higher risk for myocardial infarction, peripheral vascular disease and stroke, but the molecular mechanisms leading to accelerated damage are still unclear. Recently, we showed that hyperglycemia activates the transcription factor NFAT in the arterial wall, inducing the expression of the pro-atherosclerotic protein osteopontin. Here we investigate whether NFAT activation may be a link between diabetes and atherogenesis.

Methodology and principal findings: Streptozotocin (STZ)-induced diabetes in apolipoprotein E(-/-) mice resulted in 2.2 fold increased aortic atherosclerosis and enhanced pro-inflammatory burden, as evidenced by elevated blood monocytes, endothelial activation- and inflammatory markers in aorta, and pro-inflammatory cytokines in plasma. In vivo treatment with the NFAT blocker A-285222 for 4 weeks completely inhibited the diabetes-induced aggravation of atherosclerosis, having no effect in non-diabetic mice. STZ-treated mice exhibited hyperglycemia and higher plasma cholesterol and triglycerides, but these were unaffected by A-285222. NFAT-dependent transcriptional activity was examined in aorta, spleen, thymus, brain, heart, liver and kidney, but only augmented in the aorta of diabetic mice. A-285222 completely blocked this diabetes-driven NFAT activation, but had no impact on the other organs or on splenocyte proliferation or cytokine secretion, ruling out systemic immunosuppression as the mechanism behind reduced atherosclerosis. Instead, NFAT inhibition effectively reduced IL-6, osteopontin, monocyte chemotactic protein 1, intercellular adhesion molecule 1, CD68 and tissue factor expression in the arterial wall and lowered plasma IL-6 in diabetic mice.

Conclusions: Targeting NFAT signaling may be a novel and attractive approach for the treatment of diabetic macrovascular complications.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aorta, Thoracic / metabolism
  • Aorta, Thoracic / pathology
  • Apolipoproteins E / deficiency
  • Apolipoproteins E / metabolism
  • Atherosclerosis / blood
  • Atherosclerosis / complications*
  • Atherosclerosis / pathology*
  • Biomarkers / metabolism
  • Blood Glucose / metabolism
  • Body Weight / drug effects
  • Cholesterol / blood
  • Diabetes Mellitus, Experimental / blood
  • Diabetes Mellitus, Experimental / complications*
  • Diabetes Mellitus, Experimental / metabolism*
  • Diabetes Mellitus, Experimental / pathology
  • Disease Progression*
  • Inflammation / pathology
  • Interleukin-6 / blood
  • Mice, Inbred C57BL
  • Monocytes / metabolism
  • NFATC Transcription Factors / antagonists & inhibitors*
  • NFATC Transcription Factors / metabolism
  • Plaque, Atherosclerotic / metabolism
  • Plaque, Atherosclerotic / pathology
  • Pyrazoles / pharmacokinetics
  • Pyrazoles / pharmacology
  • Signal Transduction / drug effects
  • Transcription, Genetic / drug effects

Substances

  • A 285222
  • Apolipoproteins E
  • Biomarkers
  • Blood Glucose
  • Interleukin-6
  • NFATC Transcription Factors
  • Pyrazoles
  • Cholesterol

Grants and funding

This work was supported by the Swedish Heart and Lung Foundation [HLF20080843; HLF20100532]; the Swedish Research Council [#2009-4120; #2011-3900; #2009-1039], Lund University Diabetes Centre, the Swedish Medical Society; the Swedish Society for Medical Research, the Royal Physiographic Society in Lund, Skåne Hospital Research Funds, and Crafoord; Albert Påhlsson; Lars Hierta Memorial; and the Knut & Alice Wallenberg foundations. This work was also supported by Innovative Medicines Initiative Joint Undertaking [#115006], comprising funds from the European Union's Seventh Framework Programme [FP7/2007-2013] and EFPIA companies’ in kind contribution. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.