Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses

Eur Heart J. 2017 May 7;38(18):1402-1412. doi: 10.1093/eurheartj/ehw001.

Abstract

Aims: Circular RNAs are a subclass of non-coding RNAs detected within mammalian cells. This study was designed to test the roles of a circular RNA circ-Foxo3 in senescence using in vitro and in vivo approaches.

Methods and results: Using the approaches of molecular and cellular biology, we show that a circular RNA generated from a member of the forkhead family of transcription factors, Foxo3, namely circ-Foxo3, was highly expressed in heart samples of aged patients and mice, which was correlated with markers of cellular senescence. Doxorubicin-induced cardiomyopathy was aggravated by ectopic expression of circ-Foxo3 but was relieved by silencing endogenous circ-Foxo3. We also found that silencing circ-Foxo3 inhibited senescence of mouse embryonic fibroblasts and that ectopic expression of circ-Foxo3 induced senescence. We found that circ-Foxo3 was mainly distributed in the cytoplasm, where it interacted with the anti-senescent protein ID-1 and the transcription factor E2F1, as well as the anti-stress proteins FAK and HIF1α.

Conclusion: We conclude that ID-1, E2F1, FAK, and HIF1α interact with circ-Foxo3 and are retained in the cytoplasm and could no longer exert their anti-senescent and anti-stress roles, resulting in increased cellular senescence.

Keywords: Circular RNA; Foxo3; Heart senescence; Stress response.

MeSH terms

  • Aged
  • Animals
  • Antibiotics, Antineoplastic / pharmacology
  • Cell Line
  • Cellular Senescence / physiology*
  • Doxorubicin / toxicity
  • E2F1 Transcription Factor / metabolism
  • Focal Adhesion Kinase 1 / metabolism
  • Forkhead Box Protein O3 / physiology*
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Inhibitor of Differentiation Protein 1 / metabolism
  • Mice
  • Protein Transport
  • RNA / physiology*
  • RNA, Circular
  • Stress, Physiological / physiology

Substances

  • Antibiotics, Antineoplastic
  • E2F1 Transcription Factor
  • E2f1 protein, mouse
  • FOXO3 protein, human
  • Forkhead Box Protein O3
  • FoxO3 protein, mouse
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Idb1 protein, mouse
  • Inhibitor of Differentiation Protein 1
  • RNA, Circular
  • RNA
  • Doxorubicin
  • Focal Adhesion Kinase 1
  • Ptk2 protein, mouse