Matrix metalloproteinase (MMP) 9 transcription in mouse brain induced by fear learning

J Biol Chem. 2013 Jul 19;288(29):20978-20991. doi: 10.1074/jbc.M113.457903. Epub 2013 May 28.

Abstract

Memory formation requires learning-based molecular and structural changes in neurons, whereas matrix metalloproteinase (MMP) 9 is involved in the synaptic plasticity by cleaving extracellular matrix proteins and, thus, is associated with learning processes in the mammalian brain. Because the mechanisms of MMP-9 transcription in the brain are poorly understood, this study aimed to elucidate regulation of MMP-9 gene expression in the mouse brain after fear learning. We show here that contextual fear conditioning markedly increases MMP-9 transcription, followed by enhanced enzymatic levels in the three major brain structures implicated in fear learning, i.e. the amygdala, hippocampus, and prefrontal cortex. To reveal the role of AP-1 transcription factor in MMP-9 gene expression, we have used reporter gene constructs with specifically mutated AP-1 gene promoter sites. The constructs were introduced into the medial prefrontal cortex of neonatal mouse pups by electroporation, and the regulation of MMP-9 transcription was studied after contextual fear conditioning in the adult animals. Specifically, -42/-50- and -478/-486-bp AP-1 binding motifs of the mouse MMP-9 promoter sequence have been found to play a major role in MMP-9 gene activation. Furthermore, increases in MMP-9 gene promoter binding by the AP-1 transcription factor proteins c-Fos and c-Jun have been demonstrated in all three brain structures under investigation. Hence, our results suggest that AP-1 acts as a positive regulator of MMP-9 transcription in the brain following fear learning.

Keywords: AP1 Transcription Factor; Amygdala; Electroporation; Fear Learning; Fos; Gene Regulation; Hippocampus; Jun Transcription Factor; Matrix Metalloproteinase 9; Medial Prefrontal Cortex.

Publication types

  • Research Support, Non-U.S. Gov't
  • Retracted Publication

MeSH terms

  • Animals
  • Base Pairing / genetics
  • Base Sequence
  • Brain / enzymology*
  • Brain / physiology*
  • Conditioning, Psychological
  • Dystroglycans / metabolism
  • Fear*
  • Gene Expression Regulation, Enzymologic
  • Learning*
  • Male
  • Matrix Metalloproteinase 9 / genetics*
  • Matrix Metalloproteinase 9 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Molecular Sequence Data
  • Nucleotide Motifs / genetics
  • Promoter Regions, Genetic / genetics
  • Protein Binding / genetics
  • Proto-Oncogene Proteins c-fos / metabolism
  • Proto-Oncogene Proteins c-jun / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Transcription Factor AP-1 / metabolism
  • Transcription, Genetic*

Substances

  • Proto-Oncogene Proteins c-fos
  • Proto-Oncogene Proteins c-jun
  • RNA, Messenger
  • Transcription Factor AP-1
  • Dystroglycans
  • Matrix Metalloproteinase 9
  • Mmp9 protein, mouse