Myocardial fibrosis induced by exposure to subclinical lipopolysaccharide is associated with decreased miR-29c and enhanced NOX2 expression in mice

PLoS One. 2014 Sep 18;9(9):e107556. doi: 10.1371/journal.pone.0107556. eCollection 2014.

Abstract

Background: Exposure to subclinical levels of lipopolysaccharide (LPS) occurs commonly and is seemingly well tolerated. However, recurrent LPS exposure induces cardiac fibrosis over 2 to 3 months in a murine model, not mediated by the renin-angiotensin system. Subclinical LPS induces cardiac fibrosis by unique mechanisms.

Methods: In C57/Bl6 mice, LPS (10 mg/kg) or saline (control) were injected intraperitoneally once a week for 1-4 weeks. Mice showed no signs of distress, change in activity, appetite, or weight loss. Mice were euthanized after 3 days, 1, 2, or 4 weeks to measure cardiac expression of fibrosis-related genes and potential mediators (measured by QRT-PCR), including micro-RNA (miR) and NADPH oxidase (NOX). Collagen fraction area of the left ventricle was measured with picrosirius red staining. Cardiac fibroblasts isolated from adult mouse hearts were incubated with 0, 0.1, 1.0 or 10 ng/ml LPS for 48 hours.

Results: Cardiac miR expression profiling demonstrated decreased miR-29c after 3 and 7 days following LPS, which were confirmed by QRT-PCR. The earliest changes in fibrosis-related genes and mediators that occurred 3 days after LPS were increased cardiac expression of TIMP-1 and NOX-2 (but not of NOX-4). This persisted at 1 and 2 weeks, with additional increases in collagen Iα1, collagen IIIα1, MMP2, MMP9, TIMP1, TIMP2, and periostin. There was no change in TGF-β or connective tissue growth factor. Collagen fraction area of the left ventricle increased after 2 and 4 weeks of LPS. LPS decreased miR-29c and increased NOX-2 in isolated cardiac fibroblasts.

Conclusions: Recurrent exposure to subclinical LPS induces cardiac fibrosis after 2-4 weeks. Early changes 3 days after LPS were decreased miR-29c and increased NOX2 and TIMP1, which persisted at 1 and 2 weeks, along with widespread activation of fibrosis-related genes. Decreased miR-29c and increased NOX2, which induce cardiac fibrosis in other conditions, may uniquely mediate LPS-induced cardiac fibrosis.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Cardiomyopathies / chemically induced*
  • Cell Adhesion Molecules / biosynthesis
  • Cells, Cultured
  • Collagen Type I / biosynthesis
  • Endomyocardial Fibrosis / chemically induced*
  • Hypertrophy, Left Ventricular / chemically induced*
  • Lipopolysaccharides
  • Male
  • Matrix Metalloproteinase 2 / biosynthesis
  • Matrix Metalloproteinase 9 / biosynthesis
  • Membrane Glycoproteins / biosynthesis*
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / biosynthesis
  • MicroRNAs / genetics*
  • NADPH Oxidase 2
  • NADPH Oxidases / biosynthesis*
  • Tissue Inhibitor of Metalloproteinase-1 / biosynthesis
  • Tissue Inhibitor of Metalloproteinase-2 / biosynthesis

Substances

  • Cell Adhesion Molecules
  • Collagen Type I
  • Lipopolysaccharides
  • MIRN29 microRNA, mouse
  • Membrane Glycoproteins
  • MicroRNAs
  • Postn protein, mouse
  • Timp1 protein, mouse
  • Tissue Inhibitor of Metalloproteinase-1
  • Tissue Inhibitor of Metalloproteinase-2
  • Cybb protein, mouse
  • NADPH Oxidase 2
  • NADPH Oxidases
  • Matrix Metalloproteinase 2
  • Mmp2 protein, mouse
  • Matrix Metalloproteinase 9
  • Mmp9 protein, mouse

Grants and funding

This research was supported by the Medical Research Service, Department of Veterans Affairs (0007, P.I. WYWL) www.research.va.gov; the Veterans Medical Research Foundation, San Diego, California (08254, P.I. WYWL) www.vmrf.org; and the American Heart Association (11GRNT17390014, P.I. WYWL) www.heart.org. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.