TRENDS in Neurosciences Vol.24 No.6 June 2001
http://tins.trends.com 0166-2236/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
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because trkB phosphorylation remains
high, BDNF can trigger transcription of
various genes that are involved in
neuronal plasticity. These genes could
encode for neurotransmitters, such as
NPY.
Upregulation of BDNF induced by
seizures in the hippocampus might thus
be part of endogenous processes that limit
epileptogenesis by regulating long-term
changes in plasticity. With respect to
potential BDNF-related treatment of
epilepsy, such long-term regulations
should not be underscored.
Sophie Reibel
INSERM U433, Faculté de Médecine,
Laënnec, Lyon, France.
Antoine Depaulis*
U398 INSERM, Faculté de Médecine,
Strasbourg, France.
*e-mail: Depaulis@Neurochem.u-strasbg.fr
Yves Larmet
IPCB, Université Louis Pasteur,
Strasbourg, France.
References
1 Binder, D.K. et al. (2001) BDNF and epilepsy:
too much of a good thing? Trends Neurosci. 24,
47–53
2 Thoenen, H. (1995) Neurotrophins and neuronal
plasticity. Science 270, 593–598
3 Larmet, Y. et al. (1995) Protective effects of brain-
derived neurotrophic factor on the development of
hippocampal kindling in the rat. NeuroReport 6,
1937–1941
4 Osehobo, P. et al. (1999) Brain-derived
neurotrophic factor infusion delays amygdala and
perforant path kindling without affecting paired-
pulse measures of neuronal inhibition in adult
rats. Neuroscience 92, 1367–1375
5 Reibel, S.et al. (2000) Brain-derived neurotrophic
factor delays hippocampal kindling in the rat.
Neuroscience 100, 777–788
6 Frank, L. et al. (1997) Effects of BDNF infusion on
the regulation of TrkB protein and message in
adult rat brain. Exp. Neurol. 145, 62–70
7 Mamounas, L.A. et al. (2000) BDNF promotes the
regenerative sprouting, but not survival, of
injured serotonergic axons in the adult rat brain.
J. Neurosci. 20, 771–782
8 Reibel, S. et al. (2000) Overexpression of
neuropeptide Y induced by brain-derived
neurotrophic factor in the rat hippocampus is long
lasting. Eur. J. Neurosci. 12, 595–605
9 Vezzani, A. et al. (1999) Neuropeptide Y: emerging
evidence for a functional role in seizure
modulation. Trends Neurosci. 14, 25–30
10 Lothman, E.W. et al. (1993) Rapid kindling with
recurrent hippocampal seizures. Epilepsy Res. 14,
209–220
11 Binder, D.K. et al. (1999) Selective inhibition of
kindling development by intraventricular
administration of TrkB receptor body. J. Neurosci.
19, 1424–1436
Response: BDNF and
epilepsy – the bad
could turn out to be
good
We appreciate the response of Reibel et al. to
our recent review
1
. Their group has made
important contributions to the literature; in
particular, they have shown that chronic
intrahippocampal infusion of brain-derived
neurotrophic factor (BDNF) delays kindling
development in the rat
2
. Because chronic
(and presumably supraphysiologic) infusion
of BDNF downregulates trkB receptor
protein and responsiveness
3,4
, we believe
that their results are consistent with studies
showing that BDNF inhibition using either
trkB receptor bodies
5
or BDNF gene
deletion
6
delays kindling development. It is
not clear to us, therefore, that the ‘chronic
inhibitory effects of BDNF’ to which Reibel
et al. refer are as a result of BDNF-induced
activation of downstream inhibitory genes,
such as neuropeptide Y (NPY) (as suggested
by Reibel et al.) or instead are a result of
downregulation of endogenous trkB
receptor protein and responsiveness.
Indeed, their own observations regarding
the effects of BDNF in the rapid kindling
model (described in their letter) fit quite well
with the idea that BDNF infusion has an
initial pro-excitatory effect followed by
longer-term downregulation of BDNF
signaling observed as suppression of
kindling. To resolve this question, it would
be useful to know the level of trk receptor
activation at various time points in their
model, because seizures are known to
increase trk receptor activation in an
anatomically and temporally specific
manner
7
. Among other evidence, the fact
that transgenic mice chronically
overexpressing BDNF demonstrate
increased excitability in hippocampus and
entorhinal cortex
8
and spontaneous seizures
(S.D. Croll et al., unpublished) lends further
support to the idea that the net effect of
BDNF in vivo is pro-excitatory. As
mentioned in our review, we agree with
their contention that BDNF might activate
downstream pro-inhibitory genes, such as
neuropeptide Y (NPY), to limit excitability.
Indeed, the striking similarity in anatomy
and time course of BDNF
immunoreactivity
9
, trk receptor activation
7
and NPY immunoreactivity
10
following
seizures lends support to such a mechanism.
The question mark at the end of our
title
1
was meant to underscore the fact
that we do not fully understand the role of
BDNF in epileptogenesis. Our primary
goal was to generate interest in the clearly
dramatic effects of BDNF on excitability
and plasticity in a number of in vitro and
in vivo epilepsy models.
Devin K. Binder*
Dept of Neurological Surgery, University of
California, San Francisco, CA 94110, USA.
*e-mail: dbinder@itsa.ucsf.edu
Susan D. Croll
Regeneron Pharmaceuticals, 777 Old Saw
Mill River Road, Tarrytown, NY 10591, USA.
Christine M. Gall
Dept of Anatomy and Neurobiology, University
of California, Irvine, CA 93697-4292, USA.
Helen E. Scharfman
CNRRR, Helen Hayes Hospital, West
Haverstraw, NY 10993-1195, Depts of
Pharmacology and Neurology, Columbia
University College of Physicians and
Surgeons, New York, NY 10032, USA.
References
1 Binder, D.K. et al. (2001) BDNF and epilepsy: too
much of a good thing? Trends Neurosci. 24, 47–53
2 Larmet, Y. et al. (1995) Protective effects of brain-
derived neurotrophic factor on the development of
hippocampal kindling in the rat. NeuroReport 6,
1937–1941
3 Frank, L. et al. (1996) BDNF downregulates
neurotrophin responsiveness, trkB protein and
trkB mRNA levels in cultured rat hippocampal
neurons. Eur. J. Neurosci. 8, 1220–1230
4 Knusel, B. et al. (1997) Ligand-induced
downregulation of trk messenger RNA, protein
and tyrosine phosphorylation in rat cortical
neurons. Neuroscience 78, 851–862
5 Binder, D.K. et al. (1999) Selective inhibition of
kindling development by intraventricular
administration of trkB receptor body. J. Neurosci.
19, 1424–1436
6 Kokaia, M. et al. (1995) Suppressed epileptogenesis
in BDNF mutant mice. Exp. Neurol. 133, 215–224
7 Binder, D.K. et al. (1999) Immunohistochemical
evidence of seizure-induced activation of trk
receptors in the mossy fiber pathway of adult rat
hippocampus. J. Neurosci. 19, 4616–4626
8 Croll, S.D. et al. (1999) Brain-derived neurotrophic
factor transgenic mice exhibit passive avoidance
deficits, increased seizure severity and in vitro
hyperexcitability in the hippocampus and
entorhinal cortex. Neuroscience 93, 1491–1506
9 Gall, C.M. et al. (1996) Cellular localization of
BDNF protein after recurrent seizures in rat:
evidence for axonal transport of the newly
synthesized factor. Epilepsia 37 (Suppl. 5), 47
10 Marksteiner, J. et al. (1990) Neuropeptide Y
biosynthesis is markedly induced in mossy fibers
during temporal lobe epilepsy of the rat. Neurosci.
Lett. 112, 143–148
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