www.ScienceTranslationalMedicine.org 21 November 2012 Vol 4 Issue 161 161fs40 1
FOCUS
Epilepsy is a devastating disease afecting
1% of the world’s population. 30% of epilep-
sy patients are resistant to available drugs,
a percentage that has not changed since the
1950s. his illustrates how little progress has
been made in understanding the pathogenic
mechanisms of this disease and in devel-
oping new treatments. Given this, and the
fact that epilepsy patients whose seizures
are controlled by anti-epileptic drugs oten
sufer from detrimental side efects, there is
a dire need for new therapeutic approaches
for treating epilepsy (1).
Drug development for epilepsy faces
two main challenges: inding drugs that
abolish seizure activity without deleterious
side efects, and preventing the emergence
of epilepsy whether inherited or acquired.
Inherited epilepsies originate from gene
mutations that usually result in reorgani-
zation of neuronal networks in the brain
during development. Acquired epilepsies
may occur ater insults to the brain such as
trauma or meningitis that lead to a complex
reorganization of brain neuronal networks
in a process called epileptogenesis (Fig. 1).
Eventually this reorganization results in
spontaneous seizures, sometimes ater a sei-
zure-free latent period that may have lasted
for decades. Preventing epileptogenesis and
controlling seizures may involve difer-
ent molecular targets and hence diferent
therapeutic strategies. he ideal therapeutic
strategy would target only the brain regions
responsible for seizure genesis and would
prevent seizures without interfering with
physiological function. None of the current
anti-epileptic drugs fulill these criteria.
Reporting in this issue of Science Trans-
lational Medicine, Wykes et al. (2) take a
diferent tack using gene therapy instead
of drugs. Working in a rat model of focal
neocortical epilepsy, they use gene therapy
to deliver two diferent therapeutic genes to
the rat brain. hey show that expression of
the therapeutic genes by a subpopulation of
excitatory principal (pyramidal) neurons in
the epileptogenic region decreases the excit-
ability of these neurons, abrogating epileptic
activity and preventing epileptogenesis.
he authors created an epileptogenic re-
gion in rat brain by injection of tetanus tox-
in into the rat motor cortex. In this model,
the rats display epileptic activity and motor
seizures similar to epilepsia partialis con-
tinua observed in human patients. he au-
thors used two diferent gene therapy strate-
gies. First, using an optogenetics approach,
they injected a lentiviral vector carrying a
gene encoding the light-activated chloride
ion channel halorhodopsin into the rat
brain along with tetanus toxin to induce fo-
cal epilepsy (Fig. 1). he investigators used
a miniaturized wireless system to record
EEG activity around the clock and a newly
designed algorithm that automatically de-
tects and classiies epileptic activity. A week
later, the researchers shone laser light in 20
s pulses (delivered by an optic iber) into the
epileptogenic region of the rat brain to acti-
vate halorhodopsin expressed by excitatory
principal neurons (Fig. 1). Once activated,
the halorhodopsin channels allowed chlo-
ride ions to low into the neurons resulting
in membrane hyperpolarization, a decrease
in neuronal excitability, and a decrease in
epileptic activity as detected by EEG. Con-
trol rats not exposed to light showed no ab-
rogation of epileptic activity because halor-
hodopsin remained inactive.
his optogenetics strategy has several
advantages: It can target one small brain re-
gion, can be modulated by switching light on
and of, and does not interfere with normal
function because only a few neurons are tar-
geted (the number of neurons is determined
by the volume of tissue accessed by the viral
construct). But there are a number of open
questions including how long halorhodop-
sin delivered by gene therapy will be ex-
pressed by excitatory neurons and whether
long-term expression of this foreign protein
could have deleterious consequences. Ide-
ally, to be able to apply optogenetics to treat
epilepsy, one would need to use a closed
loop system that is able to detect seizure on-
set and then trigger optogenetic silencing of
the excitatory neurons in the epileptic focus.
A proof-of-concept that closed loop sys-
tems could be used to control epilepsy has
been provided recently by Buzsaki and col-
leagues (3) and Huguenard and co-workers
(4). In these studies, electrical stimulation
and light-activated halorhodopsin, respec-
tively, were used to abolish epileptic activ-
ity in rodents with absence-like seizures.
Absence-like seizures are characterized by
short-lasting behavioral arrest and can be
controlled efectively with existing anti-
epileptic drugs. Such closed loop systems
should now be validated in animal models
of non-absence seizures that are refractory
to drug treatment such as the rat model of
focal neocortical epilepsy used by Wykes
and co-workers.
In their second strategy, which did not
involve optogenetics, Wykes et al. injected a
lentiviral vector carrying the gene encoding
a native potassium ion channel, Kv1.1, into
the rat brain (Fig. 1). Expression of Kv1.1 by
neurons led to an outward low of potassium
ions resulting in membrane hyperpolariza-
tion and reduced neuronal excitability. he
principal diference between this approach
and the optogenetics strategy is that over-
expression of the Kv1.1 channel produced
a constitutive decrease in neuronal excit-
ability without the need for activation by
an external light source. When the authors
injected the viral vector carrying the Kv1.1
gene concomitantly with tetatus toxin into
the rat brain, they were able to prevent epi-
leptogenesis as shown by EEG. Even more
exciting, when the researchers injected the
virus carrying the Kv1.1 gene into the epi-
leptogenic region of rats in which epilepsy
had been established one week earlier with
tetanus toxin, there was a steady reduction
in epileptic activity. he reduction in epilep-
tic activity continued over several weeks and
ultimately was abolished, but there were no
motor or behavioral deicits.
he gene therapy approach of Wykes et
al. has several advantages over current anti-
epileptic drugs. Such drugs have major limi-
tations because they act nonspeciically in
the brain resulting in side efects such as cog-
nitive deicits. In contrast, gene therapy acts
speciically delivering the therapeutic gene
to a small number of neurons in a localized
brain region (Fig. 1). A further challenge
with using anti-epileptic drugs for treating
epilepsy is that neurons in epileptogenic
regions oten express multi-drug resistant
EPILEPSY
Treating Epilepsy with a Light Potassium Diet
Christophe Bernard
E-mail: christophe.bernard@univ-amu.fr
Aix Marseille Université, INS, and Inserm, UMRS 1106,
Marseille Cedex 05, France.
Gene therapy in a rat model of focal neocortical epilepsy decreases neuron excitability,
preventing epileptogenesis and abrogating epileptic activity (Wykes et al.).