Unique behavioral characteristics and microRNA signatures in a drug resistant epilepsy model

PLoS One. 2014 Jan 15;9(1):e85617. doi: 10.1371/journal.pone.0085617. eCollection 2014.

Abstract

Background: Pharmacoresistance is a major issue in the treatment of epilepsy. However, the mechanism underlying pharmacoresistance to antiepileptic drugs (AEDs) is still unclear, and few animal models have been established for studying drug resistant epilepsy (DRE). In our study, spontaneous recurrent seizures (SRSs) were investigated by video-EEG monitoring during the entire procedure.

Methods/principal findings: In the mouse pilocarpine-induced epilepsy model, we administered levetiracetam (LEV) and valproate (VPA) in sequence. AED-responsive and AED-resistant mice were naturally selected after 7-day treatment of LEV and VPA. Behavioral tests (open field, object exploration, elevated plus maze, and light-dark transition test) and a microRNA microarray test were performed. Among the 37 epileptic mice with SRS, 23 showed significantly fewer SRSs during administration of LEV (n = 16, LEV sensitive (LS) group) or VPA (n = 7, LEV resistant/VPA sensitive (LRVS) group), while 7 epileptic mice did not show any amelioration with either of the AEDs (n = 7, multidrug resistant (MDR) group). On the behavioral assessment, MDR mice displayed distinctive behaviors in the object exploration and elevated plus maze tests, which were not observed in the LS group. Expression of miRNA was altered in LS and MDR groups, and we identified 4 miRNAs (miR-206, miR-374, miR-468, and miR-142-5p), which were differently modulated in the MDR group versus both control and LS groups.

Conclusion: This is the first study to identify a pharmacoresistant subgroup, resistant to 2 AEDs, in the pilocarpine-induced epilepsy model. We hypothesize that modulation of the identified miRNAs may play a key role in developing pharmacoresistance and behavioral alterations in the MDR group.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anticonvulsants / therapeutic use*
  • Behavior, Animal*
  • Disease Models, Animal*
  • Drug Resistance
  • Electroencephalography
  • Epilepsy / drug therapy
  • Epilepsy / genetics
  • Epilepsy / physiopathology*
  • Gene Expression Profiling
  • Male
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / genetics*
  • Pilocarpine / administration & dosage
  • Pilocarpine / adverse effects

Substances

  • Anticonvulsants
  • MicroRNAs
  • Pilocarpine

Grants and funding

This study was supported by the Korean Health Technology R&D Project, Ministry of Health and Welfare, Republic of Korea (A111393; K.C.) and the Korea Health 21 R&D grant, Ministry of Health and Welfare, Republic of Korea (A120051; D. J.). K.C. was supported by Seoul National University Hospital Research Funds (0420120630). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.