ARTICLES
Activation of neuronal receptors, such as the Gα
q/11
/PLC-linked mus-
carinic receptor and the tyrosine kinase–linked brain-derived neu-
rotrophic factor (BDNF) receptor, increases intracellular Ca
2+
.
Intracellular Ca
2+
and time-dependent changes in [Ca
2+
]
i
are regula-
tors of important neuronal functions such as synapse formation
1–3
. In
neuronal growth cones, Ca
2+
waves are spatiotemporally regulated dur-
ing growth-cone turning, and their elimination prevents normal neu-
ronal differentiation. Ca
2+
waves are therefore a link between external
stimuli and processes such as growth-cone protrusion, axonal
pathfinding and initial formation of synaptic contacts
4–6
. The molecu-
lar identity of the ion channels that mediate these processes in the brain
is largely unknown, but the mammalian TRPCs are prominent candi-
dates because they are Ca
2+
-permeant receptor-operated channels
7
.
TRPCs are a subfamily of the 21 mammalian six-transmembrane
(6TM) domain TRP superfamily
7–9
. TRPC tetramers are weakly
voltage-dependent channels gated by the phosphatidylinositol signal
transduction pathway. The short or classical TRPCs are divided by
homology into two subfamilies: TRPC3/6/7 and TRPC1/4/5. Members
within each subfamily seem to form homo- and hetero-tetramers, as
seen for TRPC1 and TRPC5
10–12
.Gα
q/11
-linked receptors, such as mus-
carinic types 1 and 3 (m1, m3), activate TRPC1, TRPC4 and TRPC5
through phospholipase C β (PLCβ29 , but the specific effector molecules
directly responsible for channel activation are unknown
10,13
.
TRPC5 homomers conduct relatively large Na
+
and Ca
2+
inward cur-
rents and little outward current up to +40 mV. In contrast, the
current–voltage (I–V) relations of TRPC1 and TRPC5 channels are sim-
ilar to that of NMDA receptor channels: at depolarized potentials, the
inward current is gently inwardly rectifying, but steeply outwardly recti-
fying above 0 mV
10
. It has been posited that the TRPC3/6/7 subfamily,
also present in neurons, is gated by diacylglycerol (DAG)
12,14
.
Here we show that TRPC5 is present in growth cones and early
synapses in young rat hippocampal neurons. We found that TRPC5
channels participate in the determination of growth-cone morphol-
ogy and motility by controlling the length of filopodia and the extent
of neurite elongation.
RESULTS
TRPC5 immunolocalization in hippocampal neurons
TRPC5 protein is highly expressed in hippocampal neurons
13
.
Dissociated hippocampal neurons were identified based on accepted
criteria for morphological identification of neurons in low to
medium density cultures
15
. Antibody to green fluorescent protein
(anti-GFP) and antibody to TRPC5 (anti-TRPC5) colocalized in
hippocampal neurons transfected with TRPC5–GFP (3 days in vitro
(3 d.i.v.); Fig. 1b). Antibody binding was specific as evidenced by
experiments using a blocking peptide (Fig. 1a). TRPC5 was non-
uniformly distributed in the neuronal arborization and present in
growth cones. It was also detected in the cell body, in irregular punc-
tae along neuronal processes and in areas consistent with new synapse
formation. TRPC5 was noted in all growth cones observed. No
TRPC5 immunoreactivity was detected in glial cells (data not shown).
To further characterize TRPC5 in neuronal growth cones, hip-
pocampal neurons were co-stained with anti-TRPC5 and the well-
established growth cone marker cortactin
16
. Cortactin is a cortical
actin-binding protein that binds the Arp2/3 complex
17
.
Phosphorylated by kinases downstream of the Rho GTPases Rac and
Cdc42 (ref. 18), it is postulated to play an important role in growth
cone extension and early synaptogenesis
16,19
. TRPC5 was present in
all growth cones of young cultured hippocampal neurons stained
with cortactin (1 d.i.v.; Fig. 2a). As neurons matured and formed
1
Howard Hughes Medical Institute, Children’s Hospital and Harvard Medical School, Enders 1309, 320 Longwood Avenue, Boston, Massachusetts 02115, USA.
2
Harvard Medical School and Harvard-MIT Division of Health Sciences and Technology, Boston, Massachusetts 02115, USA.
3
Howard Hughes Medical Institute,
Massachusetts General Hospital, 55 Fruit Street, Boston, Massachusetts 02114, USA. Present address: Northwestern University Neurosciences Institute, 303 East
Chicago Avenue, Chicago, Illinois 60611, USA. Correspondence should be addressed to D.E.C. (dclapham@enders.tch.harvard.edu).
TRPC5 is a regulator of hippocampal neurite length
and growth cone morphology
Anna Greka
1,2
, Betsy Navarro
1
, Elena Oancea
1
, Anne Duggan
3
& David E Clapham
1
Growth cone motility is regulated by both fast voltage-dependent Ca
2+
channels and by unknown receptor-operated Ca
2+
entry
mechanisms. Transient receptor potential (TRP) homomeric TRPC5 ion channels are receptor-operated, Ca
2+
-permeable
channels predominantly expressed in the brain. Here we show that TRPC5 is expressed in growth cones of young rat hippocampal
neurons. Our results indicate that TRPC5 channel subunits interact with the growth cone–enriched protein stathmin 2, are
packaged into vesicles and are carried to newly forming growth cones and synapses. Once in the growth cone, TRPC5 channels
regulate neurite extension and growth-cone morphology. Dominant-negative TRPC5 expression allowed significantly longer
neurites and filopodia to form. We conclude that TRPC5 channels are important components of the mechanism controlling
neurite extension and growth cone morphology.
NATURE NEUROSCIENCE VOLUME 6 | NUMBER 8 | AUGUST 2003 837
© 2003 Nature Publishing Group http://www.nature.com/natureneuroscience