Electroconvulsive seizure, but not imipramine, rapidly up-regulates pro-BDNF and t-PA, leading to mature BDNF production, in the rat hippocampus

Int J Neuropsychopharmacol. 2013 Mar;16(2):339-50. doi: 10.1017/S1461145712000053. Epub 2012 Feb 6.

Abstract

Electroconvulsive therapy is the most effective treatment for antidepressant-resistant depression, although its mechanism has not been fully elucidated. Previous studies have demonstrated that electroconvulsive seizures (ECS) induce expression of brain-derived neurotrophic factor (BDNF) in the rat hippocampus. However, in contrast with mature BDNF (mBDNF) known to have antidepressant effects, its precursor (pro-BDNF) has harmful effects on neurons. We therefore hypothesized that efficient processing of pro-BDNF is a critical requirement for the antidepressant effects of ECS. We found that single administration of ECS rapidly increased not only hippocampal levels of pro-BDNF but also those of prohormone convertase 1 (PC1) and tissue-plasminogen activator (t-PA), which are proteases involved in intra- and extracellular pro-BDNF processing, respectively. Interestingly, pro-BDNF and t-PA levels were increased in hippocampal synaptosomes after single ECS, suggesting their transport to secretory sites. In rats receiving 10-d repeated ECS, accumulation of pro-BDNF and a resultant increase in mBDNF levels were observed. While t-PA levels increased and accumulated following repeated ECS, PC1 levels did not, suggesting that intracellular processing capacity is limited. Finally, chronic administration of imipramine significantly increased mBDNF levels, but not pro-BDNF and protease levels, indicating that the therapeutic mechanism of imipramine differs from that of ECS. Taken together, these results suggest that, while intra- and extracellular proteases are involved in pro-BDNF processing in single ECS, t-PA plays a dominant role following repeated ECS. Such efficient pro-BDNF processing as well as strong induction of BDNF expression may contribute to the antidepressant effects of ECS.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antidepressive Agents, Tricyclic / pharmacology
  • Brain-Derived Neurotrophic Factor / genetics
  • Brain-Derived Neurotrophic Factor / metabolism*
  • Disease Models, Animal
  • Electroshock / adverse effects
  • Hippocampus / diagnostic imaging
  • Hippocampus / drug effects
  • Hippocampus / metabolism*
  • Hippocampus / pathology
  • Imipramine / pharmacology
  • Immunoprecipitation
  • Male
  • Proprotein Convertase 1 / genetics
  • Proprotein Convertase 1 / metabolism
  • Protein Precursors / genetics
  • Protein Precursors / metabolism*
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Seizures / etiology
  • Seizures / pathology*
  • Synaptosomes / drug effects
  • Synaptosomes / metabolism
  • Time Factors
  • Tissue Plasminogen Activator / metabolism*
  • Ultrasonography
  • Up-Regulation / drug effects
  • Up-Regulation / physiology*

Substances

  • Antidepressive Agents, Tricyclic
  • Brain-Derived Neurotrophic Factor
  • Protein Precursors
  • RNA, Messenger
  • brain-derived neurotrophic factor precursor
  • Tissue Plasminogen Activator
  • Proprotein Convertase 1
  • Imipramine