Maintenance of long-term potentiation in hippocampal mossy fiber-CA3 pathway requires fine-tuned MMP-9 proteolytic activity

Hippocampus. 2013 Jun;23(6):529-43. doi: 10.1002/hipo.22112. Epub 2013 Apr 5.

Abstract

Mechanisms of synaptic plasticity involve proteolytic activity mediated by a complex system of proteases, including members of metalloproteinase (MMP) family. In particular, MMP-9 is critical in LTP maintenance in the Schaffer collateral-CA1 pathway and in the acquisition of hippocampus-dependent memory. Recent studies from this laboratory revealed that in the mossy fiber-CA3 (MF-CA3) projection, where LTP induction and expression are largely presynaptic, MMPs blockade disrupts LTP maintenance and that LTP induction is associated with increased MMP-9 expression. Here we used acute brain slices from MMP-9 knock-out mice and transgenic rats overexpressing MMP-9 to determine how manipulations in endogenous MMP-9 affect LTP in the MF-CA3 projection. Both types of transgenic models showed a normal basal synaptic transmission and short-term plasticity. Interestingly, the maintenance of LTP induced in slices from knock-out mice and overexpressing rats was nearly abolished. However, in the presence of active MMP-9, a gradual fEPSP autopotentiation was observed and tetanization evoked a marked LTP in knock-out mice. Additionally, in MMP-9-treated slices from wild-type mice, fEPSP autopotentiation also occurred and partially occluded LTP. This indicates that exogenous protease can restore LTP in null mice whereas in the wild-type, MMP-9 excess impairs LTP. We expected that LTP maintenance in transgenic rats could be re-established by a partial MMP blockade but non-saturating concentrations of MMP inhibitor were ineffective. In conclusion, we demonstrate that LTP maintenance in MF-CA3 pathway requires fine-tuned MMP-9 activity and raises the possibility that altered MMP-9 level might be detrimental for cognitive processes as observed in some neuropathologies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CA3 Region, Hippocampal / enzymology*
  • Enzyme Activation / physiology
  • Long-Term Potentiation / physiology*
  • Male
  • Matrix Metalloproteinase 9 / biosynthesis*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mossy Fibers, Hippocampal / enzymology*
  • Neural Pathways / physiology
  • Organ Culture Techniques
  • Proteolysis
  • Rats
  • Rats, Transgenic
  • Rats, Wistar

Substances

  • Matrix Metalloproteinase 9
  • Mmp9 protein, mouse