Opposing roles of PARP-1 in MMP-9 and TIMP-2 expression and mast cell degranulation in dyslipidemic dilated cardiomyopathy

Cardiovasc Pathol. 2011 Mar-Apr;20(2):e57-68. doi: 10.1016/j.carpath.2010.03.007. Epub 2010 May 7.

Abstract

Introduction: Previously, we demonstrated that inhibition of poly(ADP-ribose) polymerase (PARP) exerts protective effects against high-fat (HF) diet-induced atherogenesis in part by increasing tissue inhibitor of metalloproteinase (TIMP)-2 expression. Given that characteristics of dilated cardiomyopathy closely associate with atherosclerosis and are mediated by an imbalance between matrix metalloproteinases (MMPs) and TIMPs, we hypothesized that PARP-1 gene deletion may protect against HF-induced cardiac hypertrophy and dilatations by altering TIMP-2/MMPs balance in favor of a maintenance of tissue homeostasis.

Methods and results: Hemodynamic parameters determined by echocardiography were similar in ApoE(-/-) mice and PARP-1-deficient ApoE(-/-) mice (DKO) fed a regular diet (RD). However, histological analysis revealed that cardiomyocytes of ApoE(-/-) mice on RD were hypertrophied, displaying an enlarged cell body and nucleus, traits that were absent in DKO animals. HF diet-fed ApoE(-/-) mice exhibited increased interventricular septum, left ventricular (LV) internal dimension, LV volume, and LV mass in addition to a separation of myocardial fibers suggestive of dilated cardiomyopathy. PARP-1 gene deletion protected against these degenerative changes. MMP activity was dramatically increased in hearts of ApoE(-/-) mice on HF diet and was accompanied by increased collagen degradation, mast cell degranulation, and increased myocyte cell death. PARP-1 gene knockout was associated with increased TIMP-2 expression antagonizing, as a result, the damaging effects of active MMPs.

Conclusions: The present study demonstrates that PARP-1 gene deletion exerts protective effects against HF diet-induced dilated cardiomyopathy by maintaining increased expression of TIMP-2. With additional protective effects against cell death and inflammation, PARP-1 deficiency preserves cardiac tissue homeostasis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / physiology
  • Blotting, Western
  • Cardiomyopathy, Dilated / enzymology*
  • Cardiomyopathy, Dilated / pathology
  • Cell Degranulation / physiology
  • Diet, Atherogenic
  • Dyslipidemias / enzymology
  • Dyslipidemias / pathology
  • Immunohistochemistry
  • In Situ Nick-End Labeling
  • Mast Cells / enzymology*
  • Matrix Metalloproteinase 9 / biosynthesis*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Poly (ADP-Ribose) Polymerase-1
  • Poly(ADP-ribose) Polymerases / metabolism*
  • Polymerase Chain Reaction
  • Tissue Inhibitor of Metalloproteinase-2 / biosynthesis*
  • Transfection

Substances

  • Tissue Inhibitor of Metalloproteinase-2
  • Parp1 protein, mouse
  • Poly (ADP-Ribose) Polymerase-1
  • Poly(ADP-ribose) Polymerases
  • Matrix Metalloproteinase 9
  • Mmp9 protein, mouse