Significance of AT1 receptor independent activation of mineralocorticoid receptor in murine diabetic cardiomyopathy

PLoS One. 2014 Mar 24;9(3):e93145. doi: 10.1371/journal.pone.0093145. eCollection 2014.

Abstract

Background: Diabetes mellitus (DM) has deleterious influence on cardiac performance independent of coronary artery disease and hypertension. The objective of the present study was to investigate the role of the renin-angiotensin-aldosterone system, especially angiotensin II type 1a receptor (AT1aR) and mineralocorticoid receptor (MR) signaling, in left ventricular (LV) dysfunction induced by diabetes mellitus (DM).

Methods and results: DM was induced by intraperitoneal injection of streptozotocin (200 mg/kg BW) in wild-type (WT) or AT1aR knockout (KO) male mice, and they were bred during 6 or 12 weeks. Some KO mice were administered the MR antagonist eplerenone (100 mg/kg body weight). At 6 weeks, LV diastolic function was impaired in WT-DM, but preserved in KO-DM. At that time point MR mRNA expression was upregulated, NADPH oxidase subunit (p47phox) and glutathione peroxidase (GPx1) mRNA expression were upregulated, the staining intensities of LV tissue for 4-hydroxy-2-nonenal was stronger in immunohistochemistry, the number of terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling (TUNEL) positive cells was increased, Bcl-2 protein expression was significantly downregulated, and the expression of SERCA2a and phosphorylated phospholamban was depressed in WT-DM, while these changes were not seen in KO-DM. At 12 weeks, however, these changes were also noted in KO-DM. Eplerenone arrested those changes. The plasma aldosterone concentration was elevated in WT-DM but not in KO-DM at 6 weeks. It showed 3.7-fold elevation at 12 weeks even in KO-DM, which suggests "aldosterone breakthrough" phenomenon. However, the aldosterone content in LV tissue was unchanged in KO-DM.

Conclusions: DM induced diastolic dysfunction was observed even in KO at 12 weeks, which was ameliorated by minelarocorticoid receptor antagonist, eplerenone. AT1-independent MR activation in the LV might be responsible for the pathogenesis of diabetic cardiomyopathy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Diabetes Mellitus, Experimental / genetics
  • Diabetes Mellitus, Experimental / metabolism*
  • Diabetes Mellitus, Experimental / pathology
  • Diabetic Cardiomyopathies / genetics
  • Diabetic Cardiomyopathies / metabolism*
  • Diabetic Cardiomyopathies / pathology
  • Eplerenone
  • Male
  • Mice
  • Mice, Knockout
  • Mineralocorticoid Receptor Antagonists / pharmacology
  • Receptor, Angiotensin, Type 1 / genetics
  • Receptor, Angiotensin, Type 1 / metabolism*
  • Receptors, Mineralocorticoid / genetics
  • Receptors, Mineralocorticoid / metabolism*
  • Spironolactone / analogs & derivatives
  • Spironolactone / pharmacology
  • Ventricular Dysfunction, Left / genetics
  • Ventricular Dysfunction, Left / metabolism*
  • Ventricular Dysfunction, Left / pathology

Substances

  • Mineralocorticoid Receptor Antagonists
  • Receptor, Angiotensin, Type 1
  • Receptors, Mineralocorticoid
  • Spironolactone
  • Eplerenone

Grants and funding

This work was supported by a grant from the Japanese Ministry of Education, Culture, Sports, Science and Technology (No. 17790500; http://www.mext.go.jp/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.