GABAergic Mechanisms in Epilepsy
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1 Epilepsia, 42(Suppl. 3):8 12, 2001 Blackwell Science, Inc. International League Against Epilepsy GABAergic Mechanisms in Epilepsy David M. Treiman Department of Neurology, University of Medicine and Dentistry of New Jersey, Robert Wood Johnson Medical School, New Brunswick, New Jersey, U.S.A. Summary: -Aminobutyric acid (GABA), the principal inhibitory neurotransmitter in the cerebral cortex, maintains the inhibitory tone that counterbalances neuronal excitation. When this balance is perturbed, seizures may ensue. GABA is formed within GABAergic axon terminals and released into the synapse, where it acts at one of two types of receptor: GABA A, which controls chloride entry into the cell, and GABA B, which increases potassium conductance, decreases calcium entry, and inhibits the presynaptic release of other transmitters. GABA A - receptor binding influences the early portion of the GABAmediated inhibitory postsynaptic potential, whereas GABA B binding influences the late portion. GABA is rapidly removed by uptake into both glia and presynaptic nerve terminals and then catabolized by GABA transaminase. Experimental and clinical study evidence indicates that GABA has an important role in the mechanism and treatment of epilepsy: (a) Abnormalities of GABAergic function have been observed in genetic and acquired animal models of epilepsy; (b) Reductions of GABA-mediated inhibition, activity of glutamate decarboxylase, binding to GABA A and benzodiazepine sites, GABA in cerebrospinal fluid and brain tissue, and GABA detected during microdialysis studies have been reported in studies of human epileptic brain tissue; (c) GABA agonists suppress seizures, and GABA antagonists produce seizures; (d) Drugs that inhibit GABA synthesis cause seizures; and (e) Benzodiazepines and barbiturates work by enhancing GABA-mediated inhibition. Finally, drugs that increase synaptic GABA are potent anticonvulsants. Two recently developed antiepileptic drugs (AEDs), vigabatrin (VGB) and tiagabine (TGB), are examples of such agents. However, their mechanisms of action are quite different (VGB is an irreversible suicide inhibitor of GABA transaminase, whereas TGB blocks GABA reuptake into neurons and glia), which may account for observed differences in drug sideeffect profile. Key Words: Antiepileptic drug GABA Model Neurotransmitters Seizures. Abnormal discharges are due to potentiation of excitatory mechanisms or to a failure of intrinsic cerebral inhibitory systems. Gowers, 1881 Epileptic seizures can be thought of as paroxysmal hypersynchronous transient electrical discharges in the brain that result from too much excitation or too little inhibition in the area in which the abnormal discharge starts. Excitation and inhibition of neurons may be mediated by many different neurotransmitters. -Aminobutyric acid (GABA) is now recognized as the principal inhibitory neurotransmitter in the cerebral cortex (1). The structure of GABA is shown in Fig. 1. GABA is localized primarily in short-axon interneurons that synapse on cell bodies and proximal axons, and serves to maintain Address correspondence and reprint requests to Dr. D.M. Treiman at Department of Neurology, University of Medicine and Dentistry of New Jersey, Robert Wood Johnson Medical School, 97 Paterson Street, New Brunswick, NJ 08901, U.S.A. treiman@umdnj.edu inhibitory tone that counterbalances neuronal excitation. When this balance is perturbed, seizures may ensue. GABA is formed within GABAergic axon terminals by transamination of -ketoglutarate to glutamic acid, which is then decarboxylated by glutamic acid decarboxylase (GAD) to GABA. It is released into the synapse and then acts at one of two types of GABA receptors: GABA A receptors and GABA B receptors. GABA A receptors are ligand-gated ion channels that hyperpolarize the neuron by increasing inward chloride conductance and have a rapid inhibitory effect. The GABA A -receptor complex is a pentameric heterooligomer that contains binding sites for GABA, barbiturates, benzodiazepines, picrotoxin, and neurosteroids. A number of subunits of the GABA A complex have been isolated ( 1 6, 1 4, 1 3,, and ), and multiple GABA A receptor subtypes appear to exist in vivo. GABA A -receptor subtypes in the brain have been reviewed recently by McKernan and Whiting (2). GABA B receptors are G protein linked receptors that hyperpolarize the neuron by increasing potassium conductance. GABA B receptors decrease calcium entry and have a slow inhibitory effect. GABA B receptors are present on both excitatory and inhibitory 8
2 GABAergic MECHANISMS 9 FIG. 1. Structure of -aminobutyric acid. axon terminals. Activation is associated with a decrease in neurotransmitter release, and thus GABA B agonist drugs, such as baclofen, under some circumstances may be antiepileptic (3) and, in other experimental paradigms, proepileptic drugs (4). After release from the presynaptic axon terminals, GABA is rapidly removed by uptake into both glia and presynaptic nerve terminals and then is catabolized by GABA transaminase to succinic semialdehyde. Succinic semialdehyde is converted to succinic acid by succinic acid semialdehyde dehydrogenase and then enters the Krebs cycle. Olsen and Avoli (5) recently described the role of GABA A and GABA B receptors in the generation of GABA-mediated inhibitory postsynaptic potentials (IPSPs) with data generated in Avoli s laboratory (see Fig. 2). Bicuculline methiodide, a GABA A inhibitor, inhibits the early portion of the IPSP whereas CGP , a GABA B inhibitor, blocks the slow inhibitory effect seen as the late portion of the IPSP. Both drugs given together block the entire IPSP. In another experiment, CGP prevented the occurrence of pairedpulse inhibition, thus demonstrating a role of GABA B autoreceptors in this GABA-mediated inhibitory phenomenon. ROLE OF GABA IN EPILEPSY Let us now consider each of these lines of evidence in detail. EVIDENCE FROM GENETIC EPILEPSIES AND EPILEPSY MODELS Several lines of evidence from genetic epilepsies and genetic models of epilepsy support a role for GABA in epilepsy. There is impaired GABA synthesis in human pyridoxine deficiency, a disorder characterized by the onset of seizures in infancy. Decreased [ 3 H]-flunitrazepam binding has been demonstrated by Olsen et al. (6) in the substantia nigra pars reticulata and periaqueductal gray matter of seizure-susceptible gerbils studied before the appearance of seizures, suggesting that the decreased BZD binding reflects an etiologic abnormality in the GABA receptor, rather than an effect of the seizures. DBA/2 mice have an increased susceptibility to audiogenic seizures. Horton et al. (7) found a reduction in the number of high-affinity GABA receptors, and Olsen et al. (8) found reduced BZD binding in a number of areas in brains from DBA/2 mice. El (epileptic) mice have been shown to have increased numbers of GABAimmunoreactive neurons (9). Similar findings have been reported in genetically epilepsy prone (GEPR) rats (10) and in seizure-susceptible gerbils (11). These observations suggest that possible synchronizing effects of GABA interneurons may result in paradoxic facilitation of some types of epileptic discharges in some of these models. Conversely, photosensitivity-producing epilepsy in the baboon has been thought to be due to deficiency in What is the role of GABA in epilepsy and in epileptogenesis? We need to consider evidence from a number of experimental and clinical sources that provide strong support for a role of GABA in the mechanism and treatment of epilepsy. 1. Abnormalities of GABAergic function have been observed in genetic and acquired animal models of epilepsy. 2. Reductions of GABA-mediated inhibition, activity of glutamate decarboxylase, binding to GABA A and benzodiazepine sites, GABA in cerebrospinal fluid (CSF) and brain tissue, and GABA detected during microdialysis studies have all been reported in studies of human epileptic brain tissue. 3. GABA agonists suppress seizures, and GABA antagonists produce seizures. 4. Drugs that inhibit GABA synthesis cause seizures. 5. Benzodiazepines (BZDs) and barbiturates, which are effective anticonvulsants, work by enhancing GABA-mediated inhibition. 6. Drugs that increase synaptic GABA by inhibiting GABA catabolism [vigabatrin (VGB)] or reuptake [tiagabine (TGB)] are effective anticonvulsants. FIG. 2. Inhibitory postsynaptic potentials (IPSPs) and presynaptic inhibition. The control tracing shows a typical monosynaptic response recorded with a potassium acetate filled intracellular microelectrode in a human cortical neuron in the presence of ionotropic excitatory amino acid receptor antagonists. The early hyperpolarization (IPSP) (arrow at A in the control tracing) is abolished by the -aminobutyric acid (GABA A )-receptor antagonist bicuculline methiodide (BMI), as shown in the middle tracing, thus indicating this response is GABA A receptor mediated. The late hyperpolarization (arrow at B in the control tracing) is abolished by applying the GABA B receptor antagonist P-3- aminopropyl,p-diethoxymethyl phosphoric acid (CGP 35348), as shown in the bottom tracing, thus indicating the late response is GABA B receptor mediated. (From ref. 5, with permission).
3 10 D. M. TREIMAN cortical GABAergic inhibition. Lloyd et al. (12) found reduced CSF GABA concentration to be correlated with the degree of epileptic photosensitivity in such baboons. Acquired epilepsy A role of GABA in models of acquired epilepsy has also been proposed and reported in some studies. Reduced GABA-mediated inhibition has been found in several animal models. Esclapez and Trottier (13) reported reduced GABA-immunoreactive cell density in cobaltinduced cortical lesions. The reduction in GABA immunoreactivity was closely correlated with development and regression of seizure activity in this model. Ribak et al. (14) observed reduced GAD-positive axon terminals in alumina gel treated monkeys with epilepsy. However, no consistent changes in GABA function in a number of animal models of limbic epilepsy have been demonstrated. Houser et al. (15) demonstrated a loss of GADpositive terminals in alumina gel foci in the rat. There was a progressive loss of GAD-positive terminals over time, which was correlated with the development of electrocorticogram (EcoG) abnormalities and eventually with behavioral seizures. Human tissue A number of studies have shown changes in GABA concentrations or GABA-receptor densities in human epileptic tissue. GABA A receptors have been found to be reduced in parts of the human hippocampus in which cell loss has been observed (16 18). Reduced BZD binding has been demonstrated in the mesial temporal lobe on positron emission tomographic scanning (19,20). A loss of GAD and GABAergic neurons in human mesial temporal sclerosis also has been demonstrated by some investigators (21 23), but not by others (24). During and Spencer (25) studied glutamate and GABA concentrations before and after seizures in six human patients using microdialysis techniques. Glutamate concentrations increased before seizure onset and were higher in the epileptic hippocampus than in the nonepileptic hippocampus, suggesting a role of glutamate in triggering the seizures. However, the GABA increase that occurs during seizures was greater in the nonepileptic hippocampus than in the epileptic hippocampus (see Fig. 3). There are two types of presynaptic GABA release. Vesicular GABA release is calcium dependent, sensitive to tetanus toxin, and triggered by high potassium concentrations. Nonvesicular GABA release is calcium independent and occurs secondary to depolarization of the cell membrane and sodium influx. Nonvesicular GABA release is dependent on reversal of the GABA transporter. During et al. (26) found the number of GABA transporters to be reduced in epileptic hippocampus, that nonvesicular GABA release from epileptic hippocampus during seizures is not so robust as that from normal hippocampus, and that therefore insufficient FIG. 3. Hippocampal -aminobutyric acid (GABA) concentrations during complex partial seizures with secondary generalization (25). Means of percentages of basal concentrations collected during six seizures in six patients are presented. Samples were collected using a microdialysis probe implanted as part of an evaluation procedure for possible surgical treatment of epilepsy refractory to medical treatment. Sample times in relation to the seizures are indicated on the figure. (From ref. 25 with permission.) amounts of GABA are released to suppress seizure activity. GABA AGONIST AND ANTAGONIST DRUGS A number of GABA agonist drugs including muscimol, tetrahydroisooxazolopyridinol (THIP), cetylgaba, and progabide (PGB) are anticonvulsant in experimental animals, whereas GABA antagonists such as bicuculline and picrotoxin are proconvulsant. Inhibition of GABA synthesis is frequently epileptogenic. A number of GABA-synthesis inhibitors can cause seizures, including 4-deoxypyridoxine, isoniazid, thiosemicarbazide, and L-allyglycine. Drugs that enhance GABA-mediated inhibition also are anticonvulsant. These include the BZDs, which enhance binding of GABA to the GABA receptor, thus increasing the frequency of chloride channel openings (27,28). Barbiturates, which prolong the open time of the chloride channel (29), also are anticonvulsant. Drugs that increase synaptic GABA also have been shown to be potent antiepileptic drugs (AEDs). Two recently developed and marketed AEDs, VGB and TGB, are examples of this class of drugs. Both of these drugs can be considered designer drugs because they were specifically developed with the intent of increasing synaptic GABA concentrations and thus inhibiting seizure activity. Figure 4 shows schematically how each of these drugs works. VGB is an irreversible suicide inhibitor of GABA transaminase and thus inhibits degradation of GABA. This in turn results in an increase in synaptic GABA concentrations. TGB, on the other hand, blocks GABA reuptake into neurons and into glia. This also has the effect of increasing synaptic GABA concentrations. The net effect of the increase in synaptic GABA concentra-
4 GABAergic MECHANISMS 11 FIG. 4. -Aminobutyric acid (GABA)ergic synapse. GABA is synthesized in the presynaptic terminal. After release it causes the GABA A receptor on the postsynaptic neuron to increase inward chloride conductance, as do many other drugs described in the text, including the barbiturates and benzodiazepines. Synaptic GABA is taken back up into the presynaptic terminal and into glial cells. Reuptake inhibitors, such as tiagabine, and drugs that block GABA metabolism, such as vigabatrin, thus increase synaptic GABA levels. SSA, succinic semialdehyde; GAD, glutamic acid decarboxylase; GABA-T, GABA transaminase. (From ref. 38, with permission). tions is reduction of seizure frequency in patients with partial-onset seizures. Both VGB (30 33) and TGB (34 37) have been shown to be potent AEDs in the treatment of partial-onset seizures. Both work by increasing synaptic GABA concentrations. However, the mechanism whereby they produce an increase in GABA concentrations is quite different, and this may account for differences in their side-effect profiles, discussed in other articles in this symposium. REFERENCES 1. Schwartz RD. The GABA A receptor-gated ion channel: biochemical and pharmacological studies of structure and function. Biochem Pharmacol 1988;37: McKernan RM, Whiting PJ. Which GABA A -receptor subtypes really occur in the brain? Trends Neurosci 1996;19: Swartzwelder HS, Bragdon AC, Sutch CP, et al. Baclofen suppresses hippocampal epileptiform activity at low concentrations without suppressing synaptic transmission. J Pharmacol Exp Ther 1986;237: Mott DD, Bragdon AC, Lewis DV, et al. Baclofen has a proepileptic effect in the rat dentate gyrus. J Pharmacol Exp Ther 1989; 249: Olsen RW, Avoli M. GABA and epileptogenesis. Epilepsia 1997; 38: Olsen RW, Wamsley JK, McCabe RT, et al. 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