Thioredoxin 1 negatively regulates angiotensin II-induced cardiac hypertrophy through upregulation of miR-98/let-7

Circ Res. 2011 Feb 4;108(3):305-13. doi: 10.1161/CIRCRESAHA.110.228437. Epub 2010 Dec 23.

Abstract

Rationale: Thioredoxin (Trx)1 inhibits pathological cardiac hypertrophy. MicroRNAs (miRNAs) are small noncoding RNAs that downregulate posttranscriptional expression of target molecules.

Objectives: We investigated the role of miRNAs in mediating the antihypertrophic effect of Trx1 on angiotensin II (Ang II)-induced cardiac hypertrophy.

Methods and results: Microarray analyses of mature rodent microRNAs and quantitative RT-PCR/Northern blot analyses showed that Trx1 upregulates members of the let-7 family, including miR-98, in the heart and the cardiomyocytes therein. Adenovirus-mediated expression of miR-98 in cardiomyocytes reduced cell size both at baseline and in response to Ang II. Knockdown of miR-98, and of other members of the let-7 family, augmented Ang II-induced cardiac hypertrophy, and attenuated Trx1-mediated inhibition of Ang II-induced cardiac hypertrophy, suggesting that endogenous miR-98/let-7 mediates the antihypertrophic effect of Trx1. Cyclin D2 is one of the predicted targets of miR-98. Ang II significantly upregulated cyclin D2, which in turn plays an essential role in mediating Ang II-induced cardiac hypertrophy, whereas overexpression of Trx1 inhibited Ang II-induced upregulation of cyclin D2. miR-98 decreased both expression of cyclin D2 and the activity of a cyclin D2 3'UTR luciferase reporter, suggesting that both Trx1 and miR-98 negatively regulate cyclin D2. Overexpression of cyclin D2 attenuated the suppression of Ang II-induced cardiac hypertrophy by miR-98, suggesting that the antihypertrophic actions of miR-98 are mediated in part by downregulation of cyclin D2.

Conclusions: These results suggest that Trx1 upregulates expression of the let-7 family, including miR-98, which in turn inhibits cardiac hypertrophy, in part through downregulation of cyclin D2.

MeSH terms

  • Adenoviridae / genetics
  • Angiotensin II / pharmacology
  • Angiotensin II / physiology*
  • Animals
  • Cardiomegaly / physiopathology*
  • Cells, Cultured
  • Cyclin D2 / physiology
  • Disease Models, Animal
  • Mice
  • Mice, Transgenic
  • MicroRNAs / genetics
  • MicroRNAs / physiology*
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism
  • Rats
  • Rats, Wistar
  • Signal Transduction / physiology
  • Thioredoxins / genetics
  • Thioredoxins / physiology*
  • Up-Regulation / physiology*

Substances

  • Cyclin D2
  • MIRN98 microRNA, mouse
  • MIRN98 microRNA-98, rat
  • MicroRNAs
  • mirnlet7 microRNA, mouse
  • Angiotensin II
  • Thioredoxins