2015 Excel Annual Spt Application – Hippocampal sclerosis in pilocarpine epilepsy: survival of peptide-containing neurons and impairment of learning and memory in the adult NMRI mouse
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2015 Excel Annual Spt Application
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MTEP, a selective mGluR5 antagonist, had a neuroprotective effect but did not prevent the development of spontaneous recurrent seizures and behavioral disturbances in the rat lithium-pilocarpine model of epilepsy.
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By Alexandra V. Dyomina Alexandra V. Dyomina Scilit Preprints.org Google Scholar , Anna A. Kovalenko Anna A. Kovalenko Scilit Preprints.org Google Scholar , Maria V. Zakharova Maria V. Zakharova Scilit Preprints.org Google Scholar , Tatiana Yu. Postnikova Tatiana Yu. Postnikova Scilit Preprints.org Google Scholar, Alexandra V. Griflyuk Alexandra V. Griflyuk Scilit Preprints.org Google Scholar, Ilja V. Smolenski Ilya V. Smolensky Scilit Preprints.org Google Scholar †, Irina V. Antonova Irina V. Antonova Scilit Preprints org Google Scholar and Aleksey V. Zaitsev Aleksey V. Zaitsev Scilit Preprints.org Google Scholar *
Laboratory of Molecular Mechanisms of Neural Interactions, Sechenov Institute of Evolutionary Physiology and Biochemistry of RAS, 194223 St. Petersburg, Russia
Received: 9/12/2021 / Revised: 27/12/2021 / Approved: 30/12/2021 / Published: 2/1/2022
Metabotropic glutamate receptors (mGluRs) are mainly expressed in neurons and glial cells and are involved in the modulation of several signal transduction cascades. Therefore, different subtypes of mGluRs are considered promising targets in the treatment of various brain diseases. Previous studies have shown seizure-induced upregulation of mGluR5; however, its functional significance remains unclear. In this study, we aimed to elucidate the effect of treatment with the selective mGluR5 antagonist 3-[(2-methyl-1,3-thiazol-4-yl)ethynyl]pyridine (MTEP) on epileptogenesis and behavioral disorders in rats. using the lithium-pilocarpine model. We found that administration of MTEP during the latent phase of the model did not improve survival, prevent the development of epilepsy, or attenuate its manifestations in rats. However, MTEP treatment completely prevented neuronal loss and partially attenuated astrogliosis in the hippocampus. The increase in excitatory amino acid transporter 2 expression, which was demonstrated in treated rats, may prevent excitotoxicity and be a possible neuroprotective mechanism. We also found that MTEP administration did not prevent behavioral comorbidities such as depression-like behavior, motor hyperactivity, reduction in exploratory behavior, and cognitive impairment typical of the lithium-pilocarpine model. Despite the significant neuroprotective effect, MTEP treatment was not effective in preventing epilepsy.
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Temporal lobe epilepsy; excitatory amino acid transporter 2; glial fibrillary acidic protein; open field test; novel target recognition test; hippocampus; Immunohistochemistry; loss of nerve cells
Temporal lobe epilepsy (TLE) is a severe neurological disorder that manifests as spontaneous recurrent seizures and is often associated with psychiatric comorbidities such as depression, anxiety, psychosis, and cognitive impairment [1, 2, 3]. Treatment for this type of epilepsy is often difficult to find, and nearly 30% of cases are resistant to drug therapy [4, 5]. However, since TLE is often the result of a primary brain injury, preventing the development of TLE after injury is considered the optimal therapeutic strategy for the treatment of acquired TLE [ 6 , 7 ].
However, there is still no preventive treatment for epilepsy [5]. Epileptogenesis refers to the series of events that change a normal brain into one that can support a seizure. Seizures are hypothesized when the mechanisms that normally create a balance between excitation and inhibition are disrupted [8].
Metabotropic glutamate receptors (mGluRs) are not directly involved in fast excitatory synaptic transmission, unlike ionotropic α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA), N-methyl-d-aspartate (NMDA) and kainite receptors. However, since they are present on the membranes of pre- and postsynaptic neurons and glial cells, they can modulate synaptic transmission, membrane properties and metabolism of different cell types, thus playing a crucial role in the balance between excitation and inhibition [9]. In addition, mGluRs are also involved in the pathogenesis of various neurological and psychiatric disorders, such as Alzheimer’s disease, Parkinson’s disease, anxiety, depression and schizophrenia [10]. Group I and II mGluR-targeted drugs show beneficial effects in these conditions [11, 12].
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The eight mGluR subtypes are divided into three groups based on sequence homology, G protein binding, and ligand selectivity [ 10 ]. Group I includes mGluR1 and 5, which are linked to G
Concentration and promotes NMDA receptor activation [13]. Group II (mGluR2, mGluR3) and III (mGluR4, mGluR6-8) receptors are coupled to G
Proteins. The main effect of activation of these receptors is reduced neurotransmitter release and NMDA receptor activity [9, 10].
Group I mGluR expression has previously been shown to be increased in the hippocampus of epileptic patients and in a rat model of epilepsy [ 14 , 15 , 16 ], indicating that this group of mGluRs may contribute to seizure susceptibility. In addition, agonists acting on mGluR1 or mGluR5 are convulsant; therefore, negative modulators of group I mGluRs may be promising drugs for the treatment of epilepsy [ 17 , 18 ].
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The selective mGluR1 antagonist, LY456236, has dose-dependent anticonvulsant effects on limbic seizures in a 6 Hz focal seizure model and inhibition of tonic extensor seizures in an electric shock threshold model, suggesting that mGluR1 blockade may be a clinically useful treatment modality. varicose veins. Epilepsy [19]. The mGluR5 antagonist, 2-methyl-6-(phenylethynyl)pyridine (MPEP), produces dose-dependent protection against tonic prolongation seizures in the 6 Hz seizure test in mice [20] and protection against sound-induced seizures in a mouse model of Fragile X syndrome [21]. However, no significant anticonvulsant activity was observed for the highly selective mGluR5 antagonist 3-[(2-methyl-1,3-thiazol-4-yl)ethynyl]pyridine (MTEP) in the 6 Hz electroshock model [ 22 ].
Using the kainite model of epilepsy, Umpierre et al. (2019) showed that mGluR5 expression in astrocytes determines the development of epilepsy and modulates the interaction between astrocytes and neurons [23]. MTEP showed a strong neuroprotective effect against excitotoxicity induced by intrahippocampal administration of kainic acid in rats [24]. MTEP was neuroprotective even when applied 1-6 hours after exposure to kainic acid; However, the authors did not investigate its antiepileptogenic effect [24]. In addition, administration of MTEP has anxiolytic [25] and antidepressant [26] effects that may be relevant to these comorbidities in epilepsy models [27] .
Therefore, we hypothesized that mGluR5 blockade could significantly alter epileptogenesis, produce a neuroprotective effect, and reduce spontaneous recurrent seizures (SRS) and concomitant behavioral difficulties. The specific aim of this study was to investigate the effect of MTEP treatment on epileptogenesis in the rat lithium-pilocarpine model. We chose this model because it is considered the most appropriate model for the epileptogenesis of TLE [ 28 , 29 ]. Furthermore, it reproduces the main features of the pathological condition: (i) localization of the seizure in the temporal lobe [30]; (ii) a “triggering injury” that often precedes the onset of TLE [ 31 ]; iii) seizure-free latent period [32].
In this study, we administered pilocarpine at doses of 10 mg/kg every 30 min until the rat was weaned (see Methods for details). Rats that did not grow after administration of 40 mg/kg pilocarpine were excluded from the experiment. We terminated seizures with diazepam injection (5 mg/kg) 75 min after the start of training. MTEP (1 mg/kg) was administered 90 min after exercise and then every 24 h for 5 days in the experimental group. We performed RT-qPCR and Western blot analyzes of some target genes/proteins in the rat hippocampus 7 days after status epilepticus (SE) during the latent phase of the model. Behavioral tests, SRS recording, histological analysis, and Western blot analyzes were performed in the chronic phase of the model. The entire experimental design of this study is shown in Figure 1.
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To assess whether administration of MTEP alters the acute and latent phases of the model, we analyzed the survival rate and body weight of rats for one week after induced SE. We observed no differences between the Pilo and MTEP groups (Figures 2a,b).
To verify whether MTEP treatment has an antiepileptogenic effect, we recorded the behavior of rats for 48 h at 1 and 2 months after SE. We analyzed the number and duration of SRS episodes (Figure 2c). Almost all animals in both groups had SRS, indicating
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