NFAT regulates the expression of AIF-1 and IRT-1: yin and yang splice variants of neointima formation and atherosclerosis

Cardiovasc Res. 2012 Mar 1;93(3):414-23. doi: 10.1093/cvr/cvr309. Epub 2011 Nov 23.

Abstract

Aims: Alternative transcription and splicing of the allograft inflammatory factor-1 (AIF-1) gene results in the expression of two different proteins: AIF-1 and interferon responsive transcript-1 (IRT-1). Here, we explore the impact of AIF-1 and IRT-1 on vascular smooth muscle cell (VSMC) activation and neointima formation, the mechanisms underlying their alternative splicing, and associations of AIF-1 and IRT-1 mRNA with parameters defining human atherosclerotic plaque phenotype.

Methods and results: Translation of AIF-1 and IRT-1 results in different products with contrasting cellular distribution and functions. Overexpression of AIF-1 stimulates migration and proliferation of human VSMCs, whereas IRT-1 exerts opposite effects. Adenoviral infection of angioplasty-injured rat carotid arteries with AdAIF-1 exacerbates intima hyperplasia, whereas infection with AdIRT-1 reduces neointima. Expression of these variants is modulated by changes in nuclear factor of activated T-cells (NFAT) activity. Pharmacological inhibition of NFAT or targeting of NFATc3 with small interfering RNA (siRNA) lowers the AIF-1/IRT-1 ratio and favours an anti-proliferative outcome. NFAT acts as a repressor on the IRT-1 transcriptional start site, which is also sensitive to interferon-γ stimulation. Expression of AIF-1 mRNA in human carotid plaques associates with less extracellular matrix and a more pro-inflammatory plaque and plasma profile, features that may predispose to plaque rupture. In contrast, expression of IRT-1 mRNA associates with a less aggressive phenotype and less VSMCs at the most stenotic region of the plaque.

Conclusion: Inhibition of NFAT signalling, by shifting the AIF-1/IRT-1 ratio, may be an attractive target to regulate the VSMC response to injury and manipulate plaque stability in atherosclerosis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing / physiology*
  • Angioplasty, Balloon, Coronary / adverse effects
  • Animals
  • Calcium-Binding Proteins
  • Carotid Arteries / pathology
  • Carotid Artery Diseases* / genetics
  • Carotid Artery Diseases* / metabolism
  • Carotid Artery Diseases* / pathology
  • Carotid Artery Injuries / metabolism
  • Carotid Artery Injuries / pathology
  • Coronary Artery Disease* / genetics
  • Coronary Artery Disease* / metabolism
  • Coronary Artery Disease* / pathology
  • Coronary Restenosis / metabolism
  • Coronary Restenosis / pathology
  • Coronary Vessels / pathology
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Disease Models, Animal
  • Female
  • Humans
  • Male
  • Microfilament Proteins
  • Muscle, Smooth, Vascular / pathology
  • Myometrium / blood supply
  • NFATC Transcription Factors / metabolism*
  • Neointima* / genetics
  • Neointima* / metabolism
  • Neointima* / pathology
  • Organ Culture Techniques
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction / physiology

Substances

  • AIF1 protein, human
  • Calcium-Binding Proteins
  • DNA-Binding Proteins
  • Microfilament Proteins
  • NFATC Transcription Factors
  • NFATC2 protein, human