Neuronal gene repression in Niemann-Pick type C models is mediated by the c-Abl/HDAC2 signaling pathway

Biochim Biophys Acta. 2016 Feb;1859(2):269-79. doi: 10.1016/j.bbagrm.2015.11.006. Epub 2015 Nov 19.

Abstract

Background: Niemann-Pick type C (NPC) disease is a fatal neurodegenerative disorder characterized by the accumulation of free cholesterol in lysosomes. There are currently no effective FDA-approved treatments for NPC, although in the last years the inhibition of histone deacetylases (HDACs) has emerged as a potential treatment for this disease. However, the molecular mechanisms that deregulate HDAC activity in NPC disease are unknown. Previously our group had shown that the proapoptotic tyrosine kinase c-Abl signaling is activated in NPC neurons. Here, we demonstrate that c-Abl activity increases HDAC2 levels inducing neuronal gene repression of key synaptic genes in NPC models.

Results: Our data show that: i) HDAC2 levels and activity are increased in NPC neuronal models and in Npc1(-/-) mice; ii) inhibition of c-Abl or c-Abl deficiency prevents the increase of HDAC2 protein levels and activity in NPC neuronal models; iii) c-Abl inhibition decreases the levels of HDAC2 tyrosine phosphorylation; iv) treatment with methyl-β-cyclodextrin and vitamin E decreases the activation of the c-Abl/HDAC2 pathway in NPC neurons; v) in vivo treatment with two c-Abl inhibitors prevents the increase of HDAC2 protein levels in the brain of Npc1(-/-) mice; and vi) c-Abl inhibition prevents HDAC2 recruitment to the promoter of neuronal genes, triggering an increase in their expression.

Conclusion: Our data show the involvement of the c-Abl/HDAC2 signaling pathway in the regulation of neuronal gene expression in NPC neuronal models. Thus, inhibition of c-Abl could be a pharmacological target for preventing the deleterious effects of increased HDAC2 levels in NPC disease.

Keywords: GNF2; Histone deacetylase 2; Imatinib; Neuronal genes; Niemann–Pick type C disease; Tyrosine kinase c-Abl.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cholesterol / genetics
  • Cholesterol / metabolism
  • Cyclodextrins / administration & dosage
  • Disease Models, Animal
  • Gene Expression Regulation / drug effects
  • Histone Deacetylase 2 / biosynthesis
  • Histone Deacetylase 2 / genetics*
  • Humans
  • Lysosomes / metabolism
  • Mice
  • Neurons / metabolism*
  • Neurons / pathology
  • Niemann-Pick Disease, Type C / drug therapy
  • Niemann-Pick Disease, Type C / genetics*
  • Niemann-Pick Disease, Type C / pathology
  • Proto-Oncogene Proteins c-abl / biosynthesis
  • Proto-Oncogene Proteins c-abl / genetics*
  • Signal Transduction / drug effects
  • Vitamin E / administration & dosage

Substances

  • Cyclodextrins
  • Vitamin E
  • Cholesterol
  • Proto-Oncogene Proteins c-abl
  • HDAC2 protein, human
  • Histone Deacetylase 2