IRX2 activated by jumonji domain-containing protein 2A is crucial for cardiac hypertrophy and dysfunction in response to the hypertrophic stimuli

Int J Cardiol. 2023 Jan 15:371:332-344. doi: 10.1016/j.ijcard.2022.09.070. Epub 2022 Sep 29.

Abstract

Background: Iroquois homeobox 2 (IRX2) is a member of the Iroquois family whose upregulation has been potentially correlated to cardiac hypertrophy. This work studied the function of IRX2 and its related molecules in hypertrophic cardiomyopathy (HCM).

Methods: A GEO dataset GSE32453 was analyzed to identify aberrantly expressed genes in HCM. Altered expression of IRX2 was induced in mice by lentivirus injection, followed by angiotensin II (Ang II) treatment to induce HCM. The function of IRX2 knockdown in ventricular dysfunction, heart volume and pathological changes in mice, and in surface area, oxidative stress and apoptosis of isolated cardiomyocytes were examined. Binding relationship between jumonji domain-containing protein 2A (JMJD2A) and IRX2 was predicted by online tools and validated. The interaction between JMJD2A and IRX2 in HCM development was examined by joint interventions.

Results: IRX2 was highly expressed in heart tissues with HCM. IRX2 knockdown prevented mice from Ang II-induced ventricular dysfunction, cardiac hypertrophy, inflammation and fibrosis in mouse heart, and it decreased the levels of cardiac hypertrophy-related markers, oxidative stress response, and apoptosis of Ang II-treated cardiomyocytes. JMJD2A catalyzed demethylation of H3K9me3 near the IRX2 promoter to activate its transcription. JMJD2A knockdown similarly exerted protective functions against cardiac hypertrophy in vivo and in vitro, but the protection was blocked upon further IRX2 upregulation. IRX2 was found to increase the Wnt/β-catenin signaling activation.

Conclusion: This work reports that JMJD2A activates IRX2 transcription and the Wnt/β-catenin signaling to induce cardiac hypertrophy and dysfunction in HCM.

Keywords: Cardiac hypertrophy; H3K9me3; IRX2; JMJD2A; Wnt/β-catenin signaling pathway.

MeSH terms

  • Angiotensin II / metabolism
  • Angiotensin II / toxicity
  • Animals
  • Cardiomegaly / metabolism
  • Cardiomyopathy, Hypertrophic* / genetics
  • Cardiomyopathy, Hypertrophic* / pathology
  • Homeodomain Proteins* / genetics
  • Homeodomain Proteins* / metabolism
  • Jumonji Domain-Containing Histone Demethylases* / genetics
  • Jumonji Domain-Containing Histone Demethylases* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Myocytes, Cardiac / metabolism
  • Transcription Factors / genetics
  • Ventricular Dysfunction* / genetics
  • Ventricular Dysfunction* / pathology
  • beta Catenin / metabolism

Substances

  • Angiotensin II
  • beta Catenin
  • Jumonji Domain-Containing Histone Demethylases
  • Homeodomain Proteins
  • Irx2 protein, mouse
  • JMJD2A protein, mouse
  • Transcription Factors