Podocyte histone deacetylase activity regulates murine and human glomerular diseases

J Clin Invest. 2019 Mar 1;129(3):1295-1313. doi: 10.1172/JCI124030. Epub 2019 Feb 18.

Abstract

We identified 2 genes, histone deacetylase 1 (HDAC1) and HDAC2, contributing to the pathogenesis of proteinuric kidney diseases, the leading cause of end-stage kidney disease. mRNA expression profiling from proteinuric mouse glomeruli was linked to Connectivity Map databases, identifying HDAC1 and HDAC2 with the differentially expressed gene set reversible by HDAC inhibitors. In numerous progressive glomerular disease models, treatment with valproic acid (a class I HDAC inhibitor) or SAHA (a pan-HDAC inhibitor) mitigated the degree of proteinuria and glomerulosclerosis, leading to a striking increase in survival. Podocyte HDAC1 and HDAC2 activities were increased in mice podocytopathy models, and podocyte-associated Hdac1 and Hdac2 genetic ablation improved proteinuria and glomerulosclerosis. Podocyte early growth response 1 (EGR1) was increased in proteinuric patients and mice in an HDAC1- and HDAC2-dependent manner. Loss of EGR1 in mice reduced proteinuria and glomerulosclerosis. Longitudinal analysis of the multicenter Veterans Aging Cohort Study demonstrated a 30% reduction in mean annual loss of estimated glomerular filtration rate, and this effect was more pronounced in proteinuric patients receiving valproic acid. These results strongly suggest that inhibition of HDAC1 and HDAC2 activities may suppress the progression of human proteinuric kidney diseases through the regulation of EGR1.

Keywords: Cell Biology; Molecular biology; Nephrology.

Publication types

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

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Early Growth Response Protein 1 / genetics
  • Early Growth Response Protein 1 / metabolism
  • Female
  • Glomerulosclerosis, Focal Segmental* / enzymology
  • Glomerulosclerosis, Focal Segmental* / genetics
  • Glomerulosclerosis, Focal Segmental* / pathology
  • Histone Deacetylase 1* / antagonists & inhibitors
  • Histone Deacetylase 1* / genetics
  • Histone Deacetylase 1* / metabolism
  • Histone Deacetylase 2* / antagonists & inhibitors
  • Histone Deacetylase 2* / genetics
  • Histone Deacetylase 2* / metabolism
  • Histone Deacetylase Inhibitors / pharmacology*
  • Humans
  • Male
  • Mice, Knockout
  • Podocytes* / enzymology
  • Podocytes* / pathology
  • Proteinuria / drug therapy
  • Proteinuria / enzymology
  • Proteinuria / genetics
  • Proteinuria / pathology

Substances

  • EGR1 protein, human
  • Early Growth Response Protein 1
  • Egr1 protein, mouse
  • Histone Deacetylase Inhibitors
  • HDAC1 protein, human
  • HDAC2 protein, human
  • Hdac1 protein, mouse
  • Hdac2 protein, mouse
  • Histone Deacetylase 1
  • Histone Deacetylase 2