Deubiquitinase JOSD2 improves calcium handling and attenuates cardiac hypertrophy and dysfunction by stabilizing SERCA2a in cardiomyocytes

Nat Cardiovasc Res. 2023 Aug;2(8):764-777. doi: 10.1038/s44161-023-00313-y. Epub 2023 Aug 7.

Abstract

Cardiac hypertrophy leads to myocardial dysfunction and represents a serious threat to global public health security. Deubiquitinating enzymes (DUBs) mainly maintain the stability of substrate proteins and are essential to cardiac pathophysiology. Here, we explored the role and regulating mechanism of a DUB, Josephin domain-containing protein 2 (JOSD2), in cardiac hypertrophy. We found that JOSD2 expression was significantly upregulated in hypertrophic myocardium. Josd2 gene knockout aggravated cardiac dysfunction and hypertrophy in mice, whereas cardiac overexpression of JOSD2 mediated by the AAV9 vector prevented angiotensin II-induced cardiac hypertrophy. A comprehensive proteome-wide quantitative analysis identified sarco/endoplasmic reticulum calcium ATPase 2a (SERCA2a) as a key substrate of JOSD2. Mechanistically, JOSD2 mediates SERCA2a deubiquitination, enhancing the stability of SERCA2a. By regulating SERCA2a, JOSD2 deficiency impairs calcium handling and promotes hypertrophy in primary cardiomyocytes. Our findings highlight the promise of JOSD2 as a beneficial therapeutic target for hypertrophic cardiomyopathy and provide an additional strategy for SERCA2a-targeted therapy.

MeSH terms

  • Animals
  • Calcium / metabolism
  • Calcium Signaling
  • Cardiomegaly / genetics
  • Cardiomegaly / metabolism
  • Cells, Cultured
  • Deubiquitinating Enzymes / genetics
  • Deubiquitinating Enzymes / metabolism
  • Disease Models, Animal
  • Enzyme Stability
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Myocytes, Cardiac* / metabolism
  • Myocytes, Cardiac* / pathology
  • Rats
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases* / genetics
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases* / metabolism
  • Ubiquitination

Substances

  • Atp2a2 protein, mouse
  • Atp2a2 protein, rat
  • Calcium
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases
  • Deubiquitinating Enzymes