Studies of the peripheral nervous system
have led to the concept of target-derived
neurotrophic support. Neurotrophic factors
such as nerve growth factor are now known
to act as retrograde trophic factors –
retrophins – that are produced in the target
cells and released to presynaptic neurons.
However, using brain-derived neurotrophic
factor (BDNF) tagged with green-
fluorescent protein to monitor the
subcellular dynamics of BDNF in neurites,
Tsumoto and colleagues have provided
persuasive visual evidence that BDNF can
be released at the synapses of brain
neurons in an activity-dependent manner to
act on postsynaptic neurons. Accordingly,
BDNF serves as an anterophin to regulate
postsynaptic development and plasticity in
the central nervous system.
Remarkable progress in the field of cell
technology has enabled the cloning of
various genes for fluorescent proteins, and
these are becoming commercially
available in the form of plasmids carrying
eukaryotic expression promoters. Tagging
a target protein with such a fluorescent
protein at the gene level makes it possible
to visualize the location of the target
protein and to monitor its subcellular
dynamics using fluorescence microscopy.
Using such a molecular genetic approach,
brain-derived neurotrophic factor (BDNF)
protein has been fused to green
fluorescent protein (GFP) in a plasmid
vector, and gene transfer of the plasmid
construct into cells then expresses this
GFP-tagged BDNF (Fig. 1). The
GFP–BDNF was shown to be released
from neurons and mimic the conventional
activities of BDNF through activation of
TrkB receptors
1
. When Kohara, Tsumoto
and colleagues microinjected the gene
encoding GFP–BDNF and the gene for
another fluorescent protein (DsRed) into
the nuclei of cultured neurons, puncta of
GFP–BDNF were found in axon-like
processes and migrated away from the
soma with a velocity of 0.3 ± 0.1 μm s
-1
(Ref. 2). Thus, the green-fluorescent spots
in the axons presumably represent
GFP–BDNF-containing vesicles that are
moving anterogradely.
Surprisingly, the somatic region of the
neurons on which the GFP–BDNF-
carrying axons terminated and formed
synapses also showed green fluorescence
2
.
Because the postsynaptic neurons did not
exhibit the red fluorescence of the DsRed
that had been microinjected
simultaneously, the green fluorescence in
the soma cannot have been ascribed to
their expression of the GFP–BDNF gene,
and instead must have been supplied from
the presynaptic neurons. The effects of
neuronal activity on the synaptic release
of GFP–BDNF were also evaluated. In
neocortical cultures prepared from rat
embryos, spontaneous synaptic activities
were generated, and were manipulated
with TTX or picrotoxin. Treatment with
TTX for 48 hrs blocked the synaptic
currents completely, and markedly
reduced the fluorescence of GFP–BDNF in
the postsynaptic neurons. Conversely,
treatment with picrotoxin enhanced
the firing rates of postsynaptic neurons
and significantly increased the
fluorescence. The activity-dependent
synaptic transfer of GFP–BDNF indicates
that BDNF acts as an anterograde trophic
factor in the CNS.
Several pieces of indirect evidence show
that BDNF can be released from
presynaptic terminals and act on
postsynaptic neurons (Fig. 2). BDNF has
been found in the dense core vesicles of
nerve terminals or recovered in the
synaptic vesicular fraction
3–5
, and its TrkB
receptors are localized in dendrites and
axons
6
. In addition, axotomy of BDNF-
containing neurons results in depletion of
BDNF in their target area, suggesting that
BDNF must be transported anterogradely
to the nerve terminals
7,8
. The present
results clearly show that this is indeed the
case: BDNF is stored in the presynaptic
terminals and released to postsynaptic
neurons. In spite of this conclusion,
significant amounts of GFP–BDNF
fluorescence have also been found in
dendritic processes
2,9
, raising the question
of how BDNF is released from dendrites.
Non-neuronal cells are known to liberate
BDNF, which is presumably packed in
constitutive vesicles, whose dynamics and
turnover are very rapid
10
. In agreement
with the present data, previous
neurochemical studies have shown that
BDNF is, in part, released from CNS
neurons in an activity-dependent manner
and in constitutive fashion
11,12
. Whether a
proportion of BDNF can be released
toward presynaptic CNS neurons, serving
as a ‘traditional’ retrograde trophic factor,
remains to be clarified.
Postsynaptic influences of
neurotrophins have received less
attention than their presynaptic effects.
Target molecules for BDNF include
NMDA-type and AMPA-type glutamate
receptors, nitric oxide synthase (nNOS),
and calcium binding proteins
13–15
.
Phosphorylation of NMDAR1 subunits
becomes apparent, leading to
enhancement of their channel activity in
the acute phase
16
. Exposure to BDNF for a
period of days elevates the expression of
TRENDS in Neurosciences Vol.24 No.12 December 2001
http://tins.trends.com 0166-2236/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0166-2236(00)01955-X
683 Research Update
BDNF as an anterophin;a novel neurotrophic relationship
between brain neurons
Hiroyuki Nawa and Nobuyuki Takei
TRENDS in Neurosciences
Presynaptic Postsynaptic
Axon
Picrotoxin
TTX
None
Dendrite
(b)
(a)
(c)
Fig. 1 . Axonal transport and synaptic transfer of green
fluorescent protein (GFP)-tagged brain-derived
neurotrophic factor (BDNF) between cultured brain
neurons. (a) GFP–BDNF can be found in dendritic
processes and axonal vesicles of neurons transformed
with its gene. In addition, the somatic region of
postsynaptic neuron also exhibits the fluorescence of
GFP–BDNF, which is presumably derived from the
presynaptic neuron. (b) The fluorescence in the
postsynaptic neuron disappears when the neurons are
treated with tetrodotoxin (TTX) or TrkB-Ig. (c) By
contrast, it is enhanced in the presence of picrotoxin.