JOURNAL OF NEUROCHEMISTRY
| 2014 | 129 | 235–239
doi: 10.1111/jnc.12621
*Department of Neuroscience, University of Wisconsin, School of Medicine and Public Health, 1300
University Avenue, Madison, WI, USA
†Department of Neurobiology and Anatomy, Drexel University College of Medicine, Philadelphia, PA,
USA
Abstract
Microtubules in neurons consist of highly dynamic regions as well
as stable regions, some of which persist after bouts of severing
as short mobile polymers. Concentrated at the plus ends of the
highly dynamic regions are microtubule plus end tracking
proteins called +TIPs that can interact with an array of other
proteins and structures relevant to the plasticity of the neuron. It is
also provocative to ponder that short mobile microtubules might
similarly convey information with them as they transit within the
neuron. Thus, beyond their known conventional functions in
supporting neuronal architecture and organelle transport, microtubules may act as ‘information carriers’ in the neuron.
Keywords: axon, dendrite, microtubule, spine.
J. Neurochem. (2014) 129, 235–239.
Microtubules are major architectural elements without which
the neuron could not achieve or maintain its exaggerated
shape. In addition to serving as structural elements, microtubules are railways along which molecular motor proteins
convey cargo. Microtubule arrays in axons, dendrites, growth
cones, and migratory neurons are tightly organized with
respect to the intrinsic polarity of the microtubule, which is
relevant to both its assembly and transport properties.
Vibrant research is being conducted on the mechanisms by
which microtubules are organized in different compartments
of the neuron, how microtubule dynamics and stability are
regulated, and the orchestration of microtubule-based transport of organelles and proteins. While all of this is surely
enough to cause one to marvel, we cannot avoid pondering –
what other work might microtubules do for neurons?
We are inspired to think about this question by a sizable
body of knowledge about how microtubules and the actin
cytoskeleton influence one another. It has long been known
that when microtubules are pharmacologically disassembled,
the actin cytoskeleton responds, and often dramatically. The
engineers have taught us that this response is because of, at
least in part, physical principles wherein microtubules bear
compressive forces of the contractile actin cytoskeleton, such
that the removal of microtubules causes a notable uptick in
those forces (Heidemann et al. 1995). Cell biologists do not
disagree, but have argued that the force relationship may
have more to do with the balance of forces generated by
microtubule-based and actin-based motor proteins (Baas and
Ahmad 2001). There is an additional factor, however, which
the biochemists might argue is the most important of all.
When microtubules are disassembled, they release factors
that had been bound to the lattice of the microtubule, and
these factors play important roles in signaling pathways that
impact the actin cytoskeleton (Wittmann and WatermanStorer 2001). Such factors may include kinases and small G
proteins. Thus, without minimizing the contribution of
physical principles or the importance of motor-driven forces,
these latter observations suggest that microtubules are loaded
with signaling information. Such a perspective was further
buoyed with the discovery of +TIPs (Akhmanova and
Steinmetz 2008), as these proteins affiliate with the plus
ends of microtubules during bouts of assembly and can
interact with a huge variety of other proteins, many of which
reside in the cell cortex. Here, we ponder whether this theme,
of microtubules as information carriers, might be important
in a variety of ways in neurons, perhaps every bit as
important as the roles microtubules play as architectural
elements and railways for organelle transport (Fig. 1).
As alluded to above, microtubules interact with a vast
array of proteins. In addition to microtubule-based motors of
the kinesin family and cytoplasmic dynein, there are classical
Received October 13, 2013; revised manuscript received October 23,
2013; accepted November 20, 2013.
Address correspondence and reprint requests to Erik W. Dent,
Department of Neuroscience, University of Wisconsin, School of
Medicine and Public Health, 1300 University Avenue, Madison, WI
53706, USA. E-mail: [email protected]
Abbreviation used: EB, end-binding.
© 2013 International Society for Neurochemistry, J. Neurochem. (2014) 129, 235--239
235
236
E. W. Dent and P. W. Baas
Fig. 1 Microtubules as information carriers in the axon and dendrite.
Schematic showing microtubules in the axon and dendrite of a stylized
neuron. Note the small, stable translocating microtubules (orange) in
the axon (left) and the dynamic microtubules invading dendritic spines
(right). It is not yet known what proteins the small translocating
microtubules in the axon may potentially bind and release (question
mark). However, multiple studies have demonstrated dynamic microtubules are capable of polymerizing directly into dendritic spines,
concentrating +TIP proteins (yellow stars) during polymerization and
releasing them upon depolymerization. See text for details.
structural microtubule-associated proteins and an ever growing list of +TIP proteins. All of these proteins bind and are
released from microtubules through their continuous bouts of
polymerization and depolymerization. However, studying the
dynamic instability of microtubules in dendrites or axons
cannot be readily accomplished with fluorescently labeled
tubulin. This is because, unlike flattened non-neuronal cells
where microtubules can spread out mainly in two dimensions, neuronal dendrites and axons are cylindrical pipes only
a few microns wide, with microtubules packed tightly in
parallel arrays. Thus, in axons and dendrites labeled with
fluorescent tubulin the distances between microtubules are
much smaller than the diffraction limit of conventional
fluorescence microscopy, making it impossible to resolve
individual polymers. It was only when +TIP proteins were
labeled and imaged that the surprising extent of microtubule
dynamics was appreciated.
proteins that comprise these comets actually associate only
transiently with the plus ends of growing microtubules
(Dragestein et al. 2008). Thus, +TIP proteins are constantly
being concentrated and exchanged at the plus ends of
microtubules. What is attracting +TIP proteins to the tip of
growing microtubules? It appears that the calponin homology
domain of EB proteins bridges microtubule protofilaments
and binds close to the GTP-binding site (Maurer et al. 2012).
In addition, a recent study estimates that the GTP cap on
microtubules in cells is actually quite large (> 700 tubulin
subunits) and binds almost 300 EB1 dimers (Seetapun et al.
2012). These data suggest that growing microtubules are
capable of concentrating +TIP proteins by almost 100-fold
over their concentration in the cytoplasm, which bolsters the
conclusion that growing microtubule plus ends act as
‘magnets’ or ‘diffusional sinks’ (Akhmanova et al. 2009)
that are capable of concentrating microtubule-associated
proteins in time and space.
What effects might the localized concentration and release
of +TIP proteins have on cellular structure and function?
+TIP proteins, such as EB proteins, adenomatous polyposis
coli, cytoplasmic linker proteins (CLIPs) and CLIP-associated
proteins are generally thought to stabilize microtubules
against depolymerization by promoting microtubule growth
and rescue or reducing catastrophe (Akhmanova and Steinmetz 2008). Moreover, EB proteins bind microtubules
directly and are also capable of binding other +TIP proteins
(Akhmanova and Steinmetz 2008). Several studies have
shown that microtubule plus ends target specific regions of
cells, such as cell-cell and cell-matrix adhesions (Akhmanova et al. 2009). Interestingly, a recent study has demonstrated that dynein, acting as a +TIP protein, tethers dynamic
microtubule plus ends to NCAM180, which helps maintain
the density of synapses along the dendritic arbor (Perlson
Microtubules: dynamic scaffolds for concentrating
proteins
The first study to show microtubules dynamically polymerizing in dendrites was conducted with end-binding protein 3
(EB3) in cultured hippocampal and Purkinje neurons
(Stepanova et al. 2003). This work demonstrated that
microtubules polymerize slower than in non-neuronal cells,
but otherwise the association of +TIPs with microtubules is
conserved between neuronal and non-neuronal cells. This
study also suggested that microtubule polymerization, and by
extension microtubule dynamic instability, occurs throughout
the extent of the axonal and dendritic arbors. Another
amazing aspect of imaging +TIPs was the observance of
‘moving comets’ that form at the plus ends of growing
microtubules. Interestingly, further studies showed that +TIP
© 2013 International Society for Neurochemistry, J. Neurochem. (2014) 129, 235--239
Information carriers
et al. 2013). One possibility is that this tethering of
microtubules to NCAM180 at synapses may allow directed
transport of material to specific synapses to further enhance
synapse stability.
Microtubules can also bind cell regulators of the Rho
GTPase pathways. Specifically, RhoGEF2 has been shown to
associate specifically with growing microtubule ends (Rogers
et al. 2004) and can result in polarization of Rho/Rhoassociated kinase, which in turn regulates E-cadherin (Bulgakova et al. 2013). Another RhoGEF, GEF-H1 (Lfc), binds
to microtubules in its inactive state (throughout the microtubule) and is released from microtubules upon microtubule
depolymerization (Birkenfeld et al. 2008). Interestingly, one
study has shown that GEF-H1 (Lfc) release from microtubules in dendrites allows it to enter spines and activate RhoA,
which induces changes in actin polymerization resulting in
decreased spine length and increased spine density (Ryan et al.
2005). Thus, activators of Rho GTPases may be locally
delivered to specific regions of the neuronal cell membrane by
microtubules.
Putative role of microtubule signaling in dendritic
spines
Local delivery of materials to specific regions of neuronal
cell membranes has important implications for the function
of neurons, specifically at dendritic spines. A recent study
showed that microtubules in dendrites can be quite dynamic
as compared to those in the axon (Kollins et al. 2009),
indicating that dynamic microtubules may underlie plasticity
within the dendritic arbor, even in mature neurons. Surprisingly, a number of studies have now documented that
microtubules labeled with enhanced green fluorescent protein
(EGFP)-tubulin or the end-binding protein 3 (EB3-EGFP)
are capable of polymerizing within the dendritic shaft and
into dendritic spines (Gu et al. 2008; Hu et al. 2008;
Jaworski et al. 2009). Subsequent studies have shown that
these microtubule invasions of spines are regulated by both
activity and neurotrophins. Recent work has documented that
microtubule invasion frequency increases after synaptic
NMDA receptor activation through a paradigm that has been
shown to induce chemical long-term potentiation (Merriam
et al. 2011). Importantly, these microtubule invasions also
result in a long-lasting increase in spine head size that is
significantly greater than in non-invaded spines. In contrast,
stimulation of both synaptic and extrasynaptic NMDARs by
bath application of NMDA, a paradigm for inducing longterm depression, results in a loss of microtubule dynamics in
dendrites and spines (Kapitein et al. 2011).
Microtubule entry of spines is also associated with
increased spine post-synaptic density protein of 95kDa
(PSD-95) content in response to application of brain-derived
neurotrophic factor (Hu et al. 2011). Since PSD-95 content
in spines is directly associated with synaptic maturation
237
(El-Husseini et al. 2000) and knockdown of PSD-95
decreases synaptic strength and spine density (Ehrlich et al.
2007), these data suggest that microtubule entry of spines
contributes directly to post-synaptic structural changes in
spines. Moreover, directly inhibiting microtubule dynamic
instability with nanomolar concentrations of nocodazole,
which abolishes microtubule entry into spines (Merriam
et al. 2011), causes spine loss with a commensurate increase
in the number of filopodia along the dendritic shaft (Jaworski
et al. 2009). However, bath application of pharmacological
agents will also affect presynaptic microtubule dynamics.
Thus, changes in spines may result from a combination of
presynaptic changes and the lack of microtubule invasion of
spines post-synaptically. Together, these studies implicate
microtubule invasion of dendritic spines may be involved in
trafficking of molecular components to and from the synapse
along microtubules (Schapitz et al. 2010; Dent et al. 2011),
although direct imaging of microtubule cargo along labeled
microtubules entering spines has yet to be documented.
Nevertheless, what role do +TIP proteins play in this
mechanism underlying activity-dependent microtubule polymerization into spines? As it turns out, +TIP proteins play a
central role. EB3 has been shown to interact with the Src
binding protein p140Cap in spines and over-expression of either
of these proteins results in spine enlargement, whereas knockdown of these proteins results in reversion of spines to a thin,
filopodial morphology (Jaworski et al. 2009). These authors
proposed that as it enters spines, EB3 stabilizes p140Cap in the
post-synaptic density, which results in inhibition of Src kinase
activity and subsequent stabilization of cortactin, an important
protein involved in activation of actin assembly. These results
suggest that concentrating a microtubule +TIP protein in
dendritic spines via dynamic microtubule polymerization can
have important effects on the spine cytoskeleton, and subsequently neuronal function. However, this study did not directly
address how microtubules enter spines.
Work from the Dent laboratory addresses this question and
shows that the microtubule +TIP protein EB3 also appears to
play an important role in microtubule invasion of spines
(Merriam et al. 2013). Again, it is through the interaction of
microtubule +TIPs and actin-associated proteins. Drebrin, an
actin-associated protein that directly interacts with EB3
during neuritogenesis (Geraldo et al. 2008), also functions to
elicit microtubule entry into spines via EB3. Actin polymerization, downstream of calcium entry into spines, concentrates drebrin in spines. Over-expression of drebrin increases
microtubule invasion frequency and the number of spines
invaded by microtubules, and knockdown of drebrin
decreases the frequency and number of microtubule invasions markedly (Merriam et al. 2013). Interestingly, this
interaction of EB3 and drebrin may be regulated through
phosphorylation of drebrin at serine 142 (Worth et al. 2013).
A recent study has also provided evidence that a structural
microtubule-associated protein, MAP1b, regulates microtubule
© 2013 International Society for Neurochemistry, J. Neurochem. (2014) 129, 235--239
238
E. W. Dent and P. W. Baas
dynamics by sequestering EB1/3 to the cytosol (Tortosa
et al. 2013). Interestingly, MAP1b can also regulate the
activity of Rho GTPases by binding the guanine nucleotide
exchange factors, Tiam1 and GEF-H1 (Montenegro-Venegas
et al. 2010) and has recently been shown to regulate
a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic
acid
receptor endocytosis and long-term depression (Benoist
et al. 2013). Thus, there is a complicated and dynamic
interaction between +TIP proteins, structural microtubuleassociated protein and GTPases, both at the surface of
microtubules and in the cytosol.
The idea that microtubule +TIPs and actin-associated
proteins are regulated through phosphorylation in dendritic
spines would be consistent, but would also add a layer of
complexity to the evolving theory that microtubule ends can
act as ‘moving platforms’ that are comprised of a set of +TIP
proteins whose association with EB proteins are regulated
through phosphorylation/dephosphorylation at cellular membranes (Tamura and Draviam 2012). Thus, regulated EB
protein interactions with other +TIP proteins and the actin
cytomatrix is likely to be conserved in all types of cells,
including in dendrites of mature neurons.
Microtubule movements and delivery of signaling
molecules
It is with some caution that we recommend the term ‘moving
platforms’ for the ends of microtubules, as they are actually
not moving but rather assembling. True movement of
microtubules occurs in axons, and presumably in dendrites
as well, in the form of short fragments of microtubules. The
issue of microtubule transport in neurons had been controversial for decades before the laboratory of Anthony Brown
employed a clever photobleach approach to reveal the
movement (Wang and Brown 2002). After allowing fluorescent tubulin to incorporate into microtubules, Brown and
colleagues photobleached a region of the axon of about 30
microns in length, and then observed the movement of
fluorescent microtubules from the flanking regions through
the bleached zone. The movement had a notable bias in the
anterograde direction, but occurred in both directions. The
only microtubules that were observed to move were short, on
the order of 5–10 microns in length, and their movement was
rapid, with rates on the order of known molecular motors.
These observations launched over a decade of subsequent
research, mainly from the Baas laboratory, on the underlying
mechanisms of the transport, both in terms of the severing
proteins that cut the microtubules into pieces sufficiently
short to be transported, and in terms of the motor proteins
that fuel the transport (Baas and Mozgova 2012).
The microtubule transport work was originally undertaken
to address the issue of how tubulin is transported within
axons and how microtubules achieve their characteristic
patterns of polarity orientation in axons and dendrites (Baas
and Lin 2011). Studies undertaken thus far indicate that
cytoplasmic dynein is a key motor underlying the transport of
short microtubules, and that kinesins re-purposed from
mitosis can influence their transport as well (Baas and
Mozgova 2012). One possibility is that the short microtubules moving in the retrograde direction are the manifestation
of a mechanism that sends mis-oriented microtubules back to
the cell body. Now, the issue arises as to whether short
mobile microtubules might be moving platforms, in the truest
sense of the term ‘moving’. The short mobile microtubules
appear to be unusually stable, and hence might be constructed of a specially modified form of tubulin, such as
polyaminated tubulin (Song et al. 2013), or might be
decorated with particular stabilizing proteins. If this is the
case, it is not difficult to fathom that the short mobile
microtubules could also bind to proteins that need to be
conveyed either anterogradely or retrogradely in the axon, to
elicit a functional effect. At present, this speculation is not as
mature as the theory applied to +TIPs, but nonetheless
compelling to ponder. We posit that both stable short mobile
microtubules and the highly dynamic ends of longer
microtubules can act as information carriers in the neuron.
Gathering evidence for such a scenario suggests this as a
third key function for neuronal microtubules, in addition to
architecture and organelle transport.
Acknowledgements and conflicts of interest
disclosure
The studies in the Dent and Baas laboratories relevant to the ideas
discussed here are funded by grants from the National Institutes of
Health. The authors have no conflict of interest to declare.
References
Akhmanova A. and Steinmetz M. O. (2008) Tracking the ends: a
dynamic protein network controls the fate of microtubule tips. Nat.
Rev. Mol. Cell Biol. 9, 309–322.
Akhmanova A., Stehbens S. J. and Yap A. S. (2009) Touch, grasp,
deliver and control: functional cross-talk between microtubules and
cell adhesions. Traffic (Copenhagen, Denmark), 10, 268–274.
Baas P. W. and Ahmad F. J. (2001) Force generation by cytoskeletal
motor proteins as a regulator of axonal elongation and retraction.
Trends Cell Biol. 11, 244–249.
Baas P. W. and Lin S. (2011) Hooks and comets: the story of
microtubule polarity orientation in the neuron. Dev Neurobiol 71,
403–418.
Baas P. W. and Mozgova O. I. (2012) A novel role for retrograde
transport of microtubules in the axon. Cytoskeleton (Hoboken) 69,
416–425.
Benoist M., Palenzuela R., Rozas C., Rojas P., Tortosa E., Morales B.,
Gonzalez-Billault C., Avila J. and Esteban J. A. (2013) MAP1Bdependent Rac activation is required for AMPA receptor endocytosis
during long-term depression. EMBO J. 32, 2287–2299.
Birkenfeld J., Nalbant P., Yoon S. H. and Bokoch G. M. (2008) Cellular
functions of GEF-H1, a microtubule-regulated Rho-GEF: is altered
GEF-H1 activity a crucial determinant of disease pathogenesis?
Trends Cell Biol. 18, 210–219.
© 2013 International Society for Neurochemistry, J. Neurochem. (2014) 129, 235--239
Information carriers
Bulgakova N. A., Grigoriev I., Yap A. S., Akhmanova A. and Brown N.
H. (2013) Dynamic microtubules produce an asymmetric
E-cadherin-Bazooka complex to maintain segment boundaries. J.
Cell Biol. 201, 887–901.
Dent E. W., Merriam E. B. and Hu X. (2011) The dynamic cytoskeleton:
backbone of dendritic spine plasticity. Curr. Opin. Neurobiol. 21,
175–181.
Dragestein K. A., van Cappellen W. A., van Haren J., Tsibidis G. D.,
Akhmanova A., Knoch T. A., Grosveld F. and Galjart N. (2008)
Dynamic behavior of GFP-CLIP-170 reveals fast protein turnover
on microtubule plus ends. J. Cell Biol. 180, 729–737.
Ehrlich I., Klein M., Rumpel S. and Malinow R. (2007) PSD-95 is
required for activity-driven synapse stabilization. Proc. Natl Acad.
Sci. USA 104, 4176–4181.
El-Husseini A. E., Schnell E., Chetkovich D. M., Nicoll R. A. and Bredt
D. S. (2000) PSD-95 involvement in maturation of excitatory
synapses. Science New York, N.Y, 290, 1364–1368.
Geraldo S., Khanzada U. K., Parsons M., Chilton J. K. and GordonWeeks P. R. (2008) Targeting of the F-actin-binding protein
drebrin by the microtubule plus-tip protein EB3 is required for
neuritogenesis. Nat. Cell Biol. 10, 1181–1189.
Gu J., Firestein B. L. and Zheng J. Q. (2008) Microtubules in dendritic
spine development. J. Neurosci. 28, 12120–12124.
Heidemann S. R., Lamoureux P. and Buxbaum R. E. (1995)
Cytomechanics of axonal development. Cell Biochem. Biophys.
27, 135–155.
Hu X., Viesselmann C., Nam S., Merriam E. and Dent E. W. (2008)
Activity-dependent dynamic microtubule invasion of dendritic
spines. J. Neurosci. 28, 13094–13105.
Hu X., Ballo L., Pietila L., Viesselmann C., Ballweg J., Lumbard D.,
Stevenson M., Merriam E. and Dent E. W. (2011) BDNF-induced
increase of PSD-95 in dendritic spines requires dynamic
microtubule invasions. J. Neurosci. 31, 15597–15603.
Jaworski J., Kapitein L. C., Gouveia S. M. et al. (2009) Dynamic
microtubules regulate dendritic spine morphology and synaptic
plasticity. Neuron 61, 85–100.
Kapitein L. C., Yau K. W., Gouveia S. M. et al. (2011) NMDA receptor
activation suppresses microtubule growth and spine entry. J.
Neurosci. 31, 8194–8209.
Kollins K. M., Bell R. L., Butts M. and Withers G. S. (2009) Dendrites
differ from axons in patterns of microtubule stability and
polymerization during development. Neural Dev. 4, 26.
Maurer S. P., Fourniol F. J., Bohner G., Moores C. A. and Surrey T.
(2012) EBs recognize a nucleotide-dependent structural cap at
growing microtubule ends. Cell 149, 371–382.
Merriam E. B., Lumbard D. C., Viesselmann C., Ballweg J., Stevenson
M., Pietila L., Hu X. and Dent E. W. (2011) Dynamic microtubules
promote synaptic NMDA receptor-dependent spine enlargement.
PLoS ONE 6, e27688.
239
Merriam E. B., Millette M., Lumbard D. C., Saengsawang W., Fothergill
T., Hu X., Ferhat L. and Dent E. W. (2013) Synaptic regulation of
microtubule dynamics in dendritic spines by calcium, f-actin, and
drebrin. J. Neurosci. 33, 16471–16482.
Montenegro-Venegas C., Tortosa E., Rosso S. et al. (2010) MAP1B
regulates axonal development by modulating Rho-GTPase Rac1
activity. Mol. Biol. Cell 21, 3518–3528.
Perlson E., Hendricks A. G., Lazarus J. E., Ben-Yaakov K., Gradus T.,
Tokito M. and Holzbaur E. L. (2013) Dynein interacts with the
neural cell adhesion molecule (NCAM180) to tether dynamic
microtubules and maintain synaptic density in cortical neurons. J.
Biol. Chem. 288, 27812–27824.
Rogers S. L., Wiedemann U., Hacker U., Turck C. and Vale R. D. (2004)
Drosophila RhoGEF2 associates with microtubule plus ends in an
EB1-dependent manner. Curr. Biol. 14, 1827–1833.
Ryan X. P., Alldritt J., Svenningsson P., Allen P. B., Wu G. Y., Nairn A.
C. and Greengard P. (2005) The Rho-specific GEF Lfc interacts
with neurabin and spinophilin to regulate dendritic spine
morphology. Neuron 47, 85–100.
Schapitz I. U., Behrend B., Pechmann Y. et al. (2010) Neuroligin 1 is
dynamically exchanged at postsynaptic sites. J. Neurosci. 30,
12733–12744.
Seetapun D., Castle B. T., McIntyre A. J., Tran P. T. and Odde D. J.
(2012) Estimating the microtubule GTP cap size in vivo. Curr.
Biol. 22, 1681–1687.
Song Y., Kirkpatrick L. L., Schilling A. B., Helseth D. L., Chabot N.,
Keillor J. W., Johnson G. V. and Brady S. T. (2013) Transglutaminase
and polyamination of tubulin: posttranslational modification for
stabilizing axonal microtubules. Neuron 78, 109–123.
Stepanova T., Slemmer J., Hoogenraad C. C. et al. (2003) Visualization
of microtubule growth in cultured neurons via the use of EB3-GFP
(end-binding protein 3-green fluorescent protein). J. Neurosci. 23,
2655–2664.
Tamura N. and Draviam V. M. (2012) Microtubule plus-ends within a
mitotic cell are ‘moving platforms’ with anchoring, signalling and
force-coupling roles. Open Biol. 2, 120132.
Tortosa E., Galjart N., Avila J. and Sayas C. L. (2013) MAP1B regulates
microtubule dynamics by sequestering EB1/3 in the cytosol of
developing neuronal cells. EMBO J. 32, 1293–1306.
Wang L. and Brown A. (2002) Rapid movement of microtubules in
axons. Curr. Biol. 12, 1496–1501.
Wittmann T. and Waterman-Storer C. M. (2001) Cell motility: can Rho
GTPases and microtubules point the way? J. Cell Sci. 114, 3795–
3803.
Worth D. C., Daly C. N., Geraldo S., Oozeer F. and Gordon-Weeks P. R.
(2013) Drebrin contains a cryptic F-actin-bundling activity
regulated by Cdk5 phosphorylation. J. Cell Biol. 202, 793–806.
© 2013 International Society for Neurochemistry, J. Neurochem. (2014) 129, 235--239