Histone deacetylase 7 controls endothelial cell growth through modulation of beta-catenin

Circ Res. 2010 Apr 16;106(7):1202-11. doi: 10.1161/CIRCRESAHA.109.213165. Epub 2010 Mar 11.

Abstract

Rationale: Histone deacetylase (HDAC)7 is expressed in the early stages of embryonic development and may play a role in endothelial function.

Objective: This study aimed to investigate the role of HDAC7 in endothelial cell (EC) proliferation and growth and the underlying mechanism.

Methods and results: Overexpression of HDAC7 by adenoviral gene transfer suppressed human umbilical vein endothelial cell (HUVEC) proliferation by preventing nuclear translocation of beta-catenin and downregulation of T-cell factor-1/Id2 (inhibitor of DNA binding 2) and cyclin D1, leading to G(1) phase elongation. Further assays with the TOPFLASH reporter and quantitative RT-PCR for other beta-catenin target genes such as Axin2 confirmed that overexpression of HDAC7 decreased beta-catenin activity. Knockdown of HDAC7 by lentiviral short hairpin RNA transfer induced beta-catenin nuclear translocation but downregulated cyclin D1, cyclin E1 and E2F2, causing HUVEC hypertrophy. Immunoprecipitation assay and mass spectrometry analysis revealed that HDAC7 directly binds to beta-catenin and forms a complex with 14-3-3 epsilon, zeta, and eta proteins. Vascular endothelial growth factor treatment induced HDAC7 degradation via PLCgamma-IP3K (phospholipase Cgamma-inositol-1,4,5-trisphosphate kinase) signal pathway and partially rescued HDAC7-mediated suppression of proliferation. Moreover, vascular endothelial growth factor stimulation suppressed the binding of HDAC7 with beta-catenin, disrupting the complex and releasing beta-catenin to translocate into the nucleus.

Conclusions: These findings demonstrate that HDAC7 interacts with beta-catenin keeping ECs in a low proliferation stage and provides a novel insight into the mechanism of HDAC7-mediated signal pathways leading to endothelial growth.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / metabolism
  • Active Transport, Cell Nucleus
  • Adenoviridae / genetics
  • Cell Cycle
  • Cell Proliferation*
  • Cells, Cultured
  • Cyclin D1 / metabolism
  • Cyclin E / metabolism
  • E2F2 Transcription Factor / metabolism
  • Endothelial Cells / enzymology*
  • Endothelial Cells / pathology
  • Genetic Vectors
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism*
  • Humans
  • Hypertrophy
  • Immunoprecipitation
  • Inhibitor of Differentiation Protein 2 / metabolism
  • Mass Spectrometry
  • Neovascularization, Physiologic
  • Oncogene Proteins / metabolism
  • Phospholipase C gamma / metabolism
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Protein Binding
  • Protein Processing, Post-Translational
  • RNA Interference
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction*
  • Time Factors
  • Transduction, Genetic
  • Vascular Endothelial Growth Factor A / metabolism
  • beta Catenin / metabolism*

Substances

  • 14-3-3 Proteins
  • CCND1 protein, human
  • CCNE1 protein, human
  • CTNNB1 protein, human
  • Cyclin E
  • E2F2 Transcription Factor
  • E2F2 protein, human
  • ID2 protein, human
  • Inhibitor of Differentiation Protein 2
  • Oncogene Proteins
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • YWHAE protein, human
  • YWHAH protein, human
  • beta Catenin
  • Cyclin D1
  • Phosphotransferases (Alcohol Group Acceptor)
  • Inositol 1,4,5-trisphosphate 3-kinase
  • Phospholipase C gamma
  • HDAC7 protein, human
  • Histone Deacetylases