AGO2 Protects Against Diabetic Cardiomyopathy by Activating Mitochondrial Gene Translation

Circulation. 2024 Apr 2;149(14):1102-1120. doi: 10.1161/CIRCULATIONAHA.123.065546. Epub 2023 Dec 21.

Abstract

Background: Diabetes is associated with cardiovascular complications. microRNAs translocate into subcellular organelles to modify genes involved in diabetic cardiomyopathy. However, functional properties of subcellular AGO2 (Argonaute2), a core member of miRNA machinery, remain elusive.

Methods: We elucidated the function and mechanism of subcellular localized AGO2 on mouse models for diabetes and diabetic cardiomyopathy. Recombinant adeno-associated virus type 9 was used to deliver AGO2 to mice through the tail vein. Cardiac structure and functions were assessed by echocardiography and catheter manometer system.

Results: AGO2 was decreased in mitochondria of diabetic cardiomyocytes. Overexpression of mitochondrial AGO2 attenuated diabetes-induced cardiac dysfunction. AGO2 recruited TUFM, a mitochondria translation elongation factor, to activate translation of electron transport chain subunits and decrease reactive oxygen species. Malonylation, a posttranslational modification of AGO2, reduced the importing of AGO2 into mitochondria in diabetic cardiomyopathy. AGO2 malonylation was regulated by a cytoplasmic-localized short isoform of SIRT3 through a previously unknown demalonylase function.

Conclusions: Our findings reveal that the SIRT3-AGO2-CYTB axis links glucotoxicity to cardiac electron transport chain imbalance, providing new mechanistic insights and the basis to develop mitochondria targeting therapies for diabetic cardiomyopathy.

Keywords: Sirtuin 3, argonaute; diabetic cardiomyopathies; mitochondria; therapeutics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Diabetes Mellitus* / metabolism
  • Diabetic Cardiomyopathies*
  • Genes, Mitochondrial
  • Mice
  • MicroRNAs* / genetics
  • Mitochondria / genetics
  • Myocytes, Cardiac / metabolism
  • Sirtuin 3* / genetics

Substances

  • Sirtuin 3
  • MicroRNAs