Sp3/REST/HDAC1/HDAC2 Complex Represses and Sp1/HIF-1/p300 Complex Activates ncx1 Gene Transcription, in Brain Ischemia and in Ischemic Brain Preconditioning, by Epigenetic Mechanism

J Neurosci. 2015 May 13;35(19):7332-48. doi: 10.1523/JNEUROSCI.2174-14.2015.

Abstract

The Na(+)-Ca(2+) exchanger 1 (NCX1) is reduced in stroke by the RE1-silencing transcription factor (REST), whereas it is increased in ischemic brain preconditioning (PC) by hypoxia-inducible factor 1 (HIF-1). Because ncx1 brain promoter (ncx1-Br) has five putative consensus sequences, named Sp1A-E, for the specificity protein (Sp) family of transcription factors (Sp1-4), we investigated the role of this family in regulating ncx1 transcription in rat cortical neurons. Here we found that Sp1 is a transcriptional activator, whereas Sp3 is a transcriptional repressor of ncx1, and that both bind ncx1-Br in a sequence-specific manner, modulating ncx1 transcription through the Sp1 sites C-E. Furthermore, by transient middle cerebral artery occlusion (tMCAO) in rats, the transcriptional repressors Sp3 and REST colocalized with the two histone-deacetylases (HDACs) HDAC1 and HDAC2 on the ncx1-Br, with a consequent hypoacetylation. Contrarily, in PC+tMCAO the transcriptional activators Sp1 and HIF-1 colocalized with histone acetyltransferase p300 on ncx1-Br with a consequent hyperacetylation. In addition, in neurons silenced with siRNA of NCX1 and subjected to oxygen and glucose deprivation (OGD) (3 h) plus reoxygenation (RX) (24 h), the neuroprotection of Class I HDAC inhibitor MS-275 was counteracted, whereas in neurons overexpressing NCX1 and subjected to ischemic preconditioning (PC+OGD/RX), the neurotoxic effect of p300 inhibitor C646 was prevented. Collectively, these results demonstrate that NCX1 expression is regulated by the Sp3/REST/HDAC1/HDAC2 complex in tMCAO and by the Sp1/HIF-1/p300 complex in PC+tMCAO and that epigenetic intervention, by modulating the acetylation of ncx1-Br, may be a strategy for the development of innovative therapeutic intervention in stroke.

Keywords: REST\NRSF; acetylation; brain ischemia; epigenetic; ischemic brain preconditioning; sodium/calcium exchanger.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Benzoates / pharmacology
  • Brain Ischemia / pathology*
  • Brain Ischemia / prevention & control
  • Cerebral Cortex / cytology
  • Disease Models, Animal
  • Enzyme Inhibitors / pharmacology
  • Epigenesis, Genetic*
  • Histone Deacetylase 1 / genetics
  • Humans
  • Ischemic Preconditioning*
  • Male
  • Neurons / metabolism*
  • Nitrobenzenes
  • Pyrazoles / pharmacology
  • Pyrazolones
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Repressor Proteins
  • Sodium-Calcium Exchanger / genetics
  • Sodium-Calcium Exchanger / metabolism*
  • Transcriptional Activation
  • Transfection
  • p300-CBP Transcription Factors / metabolism

Substances

  • 4-(4-((5-(4,5-dimethyl-2-nitrophenyl)-2-furanyl)methylene)-4,5-dihydro-3-methyl-5-oxo-1H-pyrazol-1-yl)benzoic acid
  • Benzoates
  • Enzyme Inhibitors
  • Nitrobenzenes
  • Pyrazoles
  • Pyrazolones
  • RE1-silencing transcription factor
  • RNA, Small Interfering
  • Repressor Proteins
  • Sodium-Calcium Exchanger
  • sodium-calcium exchanger 1
  • p300-CBP Transcription Factors
  • HDAC1 protein, human
  • Histone Deacetylase 1