Preservation of Glucagon-Like Peptide-1 Level Attenuates Angiotensin II-Induced Tissue Fibrosis by Altering AT1/AT 2 Receptor Expression and Angiotensin-Converting Enzyme 2 Activity in Rat Heart

Cardiovasc Drugs Ther. 2015 Jun;29(3):243-55. doi: 10.1007/s10557-015-6592-7.

Abstract

Purpose: The glucagon-like peptide-1 (GLP-1) has been shown to exert cardioprotective effects in animals and patients. This study tests the hypothesis that preservation of GLP-1 by the GLP-1 receptor agonist liraglutide or the dipeptidyl peptidase-4 (DPP-4) inhibitor linagliptin is associated with a reduction of angiotensin (Ang) II-induced cardiac fibrosis.

Methods and results: Sprague-Dawley rats were subjected to Ang II (500 ng/kg/min) infusion using osmotic minipumps for 4 weeks. Liraglutide (0.3 mg/kg) was subcutaneously injected twice daily or linagliptin (8 mg/kg) was administered via oral gavage daily during Ang II infusion. Relative to the control, liraglutide, but not linagliptin decreased MAP (124 ± 4 vs. 200 ± 7 mmHg in control, p < 0.003). Liraglutide and linagliptin comparatively reduced the protein level of the Ang II AT1 receptor and up-regulated the AT2 receptor as identified by a reduced AT1/AT2 ratio (0.4 ± 0.02 and 0.7 ± 0.01 vs. 1.4 ± 0.2 in control, p < 0.05), coincident with the less locally-expressed AT1 receptor and enhanced AT2 receptor in the myocardium and peri-coronary vessels. Both drugs significantly reduced the populations of macrophages (16 ± 6 and 19 ± 7 vs. 61 ± 29 number/HPF in control, p < 0.05) and α-SMA expressing myofibroblasts (17 ± 7 and 13 ± 4 vs. 66 ± 29 number/HPF in control, p < 0.05), consistent with the reduction in expression of TGFβ1 and phospho-Smad2/3, and up-regulation of Smad7. Furthermore, ACE2 activity (334 ± 43 and 417 ± 51 vs. 288 ± 19 RFU/min/μg protein in control, p < 0.05) and GLP-1 receptor expression were significantly up-regulated. Along with these modulations, the synthesis of collagen I and tissue fibrosis were inhibited as determined by the smaller collagen-rich area and more viable myocardium.

Conclusion: These results demonstrate for the first time that preservation of GLP-1 using liraglutide or linagliptin is effective in inhibiting Ang II-induced cardiac fibrosis, suggesting that these drugs could be selected as an adjunctive therapy to improve clinical outcomes in the fibrosis-derived heart failure patients with or without diabetes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / adverse effects*
  • Angiotensin-Converting Enzyme 2
  • Animals
  • Blood Pressure / drug effects
  • Collagen / metabolism
  • Fibrosis / chemically induced
  • Fibrosis / drug therapy
  • Fibrosis / metabolism
  • Fibrosis / pathology*
  • Gene Expression / drug effects*
  • Glucagon-Like Peptide 1 / metabolism*
  • Linagliptin / pharmacology
  • Linagliptin / therapeutic use
  • Liraglutide / pharmacology
  • Liraglutide / therapeutic use
  • Male
  • Myocardium / enzymology
  • Myocardium / metabolism*
  • Myocardium / pathology
  • Peptidyl-Dipeptidase A / metabolism*
  • Rats
  • Receptor, Angiotensin, Type 1 / biosynthesis*
  • Receptor, Angiotensin, Type 1 / metabolism
  • Receptor, Angiotensin, Type 2 / biosynthesis*
  • Receptor, Angiotensin, Type 2 / metabolism
  • Smad Proteins / metabolism
  • Transforming Growth Factor beta1 / biosynthesis

Substances

  • Receptor, Angiotensin, Type 1
  • Receptor, Angiotensin, Type 2
  • Smad Proteins
  • Transforming Growth Factor beta1
  • Angiotensin II
  • Linagliptin
  • Liraglutide
  • Glucagon-Like Peptide 1
  • Collagen
  • Peptidyl-Dipeptidase A
  • Ace2 protein, rat
  • Angiotensin-Converting Enzyme 2