Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis

Am J Pathol. 2010 Jan;176(1):85-97. doi: 10.2353/ajpath.2010.090517. Epub 2009 Dec 11.

Abstract

Understanding the origin of myofibroblasts in kidney is of great interest because these cells are responsible for scar formation in fibrotic kidney disease. Recent studies suggest epithelial cells are an important source of myofibroblasts through a process described as the epithelial-to-mesenchymal transition; however, confirmatory studies in vivo are lacking. To quantitatively assess the contribution of renal epithelial cells to myofibroblasts, we used Cre/Lox techniques to genetically label and fate map renal epithelia in models of kidney fibrosis. Genetically labeled primary proximal epithelial cells cultured in vitro from these mice readily induce markers of myofibroblasts after transforming growth factor beta(1) treatment. However, using either red fluorescent protein or beta-galactosidase as fate markers, we found no evidence that epithelial cells migrate outside of the tubular basement membrane and differentiate into interstitial myofibroblasts in vivo. Thus, although renal epithelial cells can acquire mesenchymal markers in vitro, they do not directly contribute to interstitial myofibroblast cells in vivo. Lineage analysis shows that during nephrogenesis, FoxD1-positive((+)) mesenchymal cells give rise to adult CD73(+), platelet derived growth factor receptor beta(+), smooth muscle actin-negative interstitial pericytes, and these FoxD1-derivative interstitial cells expand and differentiate into smooth muscle actin(+) myofibroblasts during fibrosis, accounting for a large majority of myofibroblasts. These data indicate that therapeutic strategies directly targeting pericyte differentiation in vivo may productively impact fibrotic kidney disease.

Publication types

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

MeSH terms

  • Actins / metabolism
  • Animals
  • Cell Lineage*
  • Cell Movement
  • Cells, Cultured
  • Disease Models, Animal
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology*
  • Fibroblasts / metabolism
  • Fibroblasts / pathology*
  • Fibrosis
  • Forkhead Transcription Factors / metabolism
  • Green Fluorescent Proteins
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Integrases / metabolism
  • Kidney / metabolism
  • Kidney / pathology*
  • Kidney Tubules / metabolism
  • Kidney Tubules / pathology
  • Mesoderm / metabolism
  • Mesoderm / pathology
  • Mice
  • Pericytes / metabolism
  • Pericytes / pathology*
  • Promoter Regions, Genetic / genetics
  • S100 Calcium-Binding Protein A4
  • S100 Proteins / metabolism
  • Transcription Factors / genetics
  • Up-Regulation

Substances

  • Actins
  • Forkhead Transcription Factors
  • Foxd1 protein, mouse
  • Homeodomain Proteins
  • Hoxb7 protein, mouse
  • S100 Calcium-Binding Protein A4
  • S100 Proteins
  • S100a4 protein, mouse
  • Six2 protein, mouse
  • Transcription Factors
  • Green Fluorescent Proteins
  • Cre recombinase
  • Integrases