Adverse fibrosis in the aging heart depends on signaling between myeloid and mesenchymal cells; role of inflammatory fibroblasts

J Mol Cell Cardiol. 2014 May:70:56-63. doi: 10.1016/j.yjmcc.2013.10.017. Epub 2013 Oct 31.

Abstract

Aging has been associated with adverse fibrosis. Here we formulate a new hypothesis and present new evidence that unresponsiveness of mesenchymal stem cells (MSC) and fibroblasts to transforming growth factor beta (TGF-β), due to reduced expression of TGF-β receptor I (TβRI), provides a foundation for cardiac fibrosis in the aging heart via two mechanisms. 1) TGF-β promotes expression of Nanog, a transcription factor that retains MSC in a primitive state. In MSC derived from the aging heart, Nanog expression is reduced and therefore MSC gradually differentiate and the number of mesenchymal fibroblasts expressing collagen increases. 2) As TGF-β signaling pathway components negatively regulate transcription of monocyte chemoattractant protein-1 (MCP-1), a reduced expression of TβRI prevents aging mesenchymal cells from shutting down their own MCP-1 expression. Elevated MCP-1 levels that originated from MSC attract transendothelial migration of mononuclear leukocytes from blood to the tissue. MCP-1 expressed by mesenchymal fibroblasts promotes further migration of monocytes and T lymphocytes away from the endothelial barrier and supports the monocyte transition into macrophages and finally into myeloid fibroblasts. Both myeloid and mesenchymal fibroblasts contribute to fibrosis in the aging heart via collagen synthesis. This article is part of a Special Issue entitled "Myocyte-Fibroblast Signalling in Myocardium ".

Keywords: Aging; Inflammatory fibroblast; MCP-1; Mesenchymal stem cell; TGF-β.

Publication types

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

MeSH terms

  • Aging / metabolism*
  • Aging / pathology
  • Cell Differentiation
  • Collagen / genetics
  • Collagen / metabolism
  • Fibroblasts / metabolism*
  • Fibroblasts / pathology
  • Fibrosis / metabolism*
  • Fibrosis / pathology
  • Fibrosis / physiopathology
  • Gene Expression Regulation
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Humans
  • Mesenchymal Stem Cells / metabolism*
  • Mesenchymal Stem Cells / pathology
  • Monocytes / metabolism
  • Monocytes / pathology
  • Myocardium / metabolism
  • Myocardium / pathology
  • Nanog Homeobox Protein
  • Receptors, Transforming Growth Factor beta / genetics
  • Receptors, Transforming Growth Factor beta / metabolism
  • Signal Transduction
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / pathology
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism

Substances

  • Homeodomain Proteins
  • NANOG protein, human
  • Nanog Homeobox Protein
  • Receptors, Transforming Growth Factor beta
  • Transforming Growth Factor beta
  • Collagen