538 VOLUME 14 | NUMBER 5 | MAY 2011 NATURE NEUROSCIENCE
NEWS AND VIEWS
10. Santana, L.F. & Navedo, M.F. J. Gen. Physiol. 136,
143–147 (2010).
11. Jing, L., Lefebvre, J.L., Gordon, L.R. & Granato, M.
Neuron 61, 721–733 (2009).
12. Budnik, V. & Salinas, P.C. Curr. Opin. Neurobiol. 21,
151–159 (2011).
13. Rüegg, M.A. & Glass, D.J. Annu. Rev. Pharmacol.
Toxicol. 51, 373–395 (2011).
14. Williams, A.H. et al. Science 326, 1549–1554
(2009).
15. Selkoe, D.J. Science 298, 789–791 (2002).
4. Wu, H., Xiong, W.C. & Mei, L. Development 137,
1017–1033 (2010).
5. Yang, X. et al. Neuron 30, 399–410 (2001).
6. Kim, N. & Burden, S.J. Nat. Neurosci. 11, 19–27
(2008).
7. Catterall, W.A. Annu. Rev. Cell Dev. Biol. 16, 521–555
(2000).
8. Piétri-Rouxel, F. et al. EMBO J. 29, 643–654
(2010).
9. Wheeler, D.G., Barrett, C.F., Groth, R.D., Safa, P. &
Tsien, R.W. J. Cell Biol. 183, 849–863 (2008).
538 VOLUME 14 | NUMBER 5 | MAY 2011 NATURE NEUROSCIENCE
NEWS AND VIEWS NEWS AND VIEWS
COMPETING FINANCIAL INTERESTS
The author declares competing financial interests:
details accompany the full-text HTML version of the
paper at http://www.nature.com/natureneuroscience/.
1. Taylor, A.B. & Fallon, J.R. J. Neurosci. 26, 1154–1163
(2006).
2. Sanes, J.R. & Yamagata, M. Annu. Rev. Cell Dev. Biol.
25, 161–195 (2009).
3. Chen, F. et al. Nat. Neurosci. 14, 570–577 (2011).
Hanging by the tail: progenitor populations
proliferate
Zoltán Molnár, Navneet A Vasistha & Fernando Garcia-Moreno
A study now identifies a new progenitor subtype in the developing mouse cortex, similar to the outer radial glia
progenitors described previously in human, ferret and other mammals with larger, folded brains.
Zoltán Molnár, Navneet A. Vasistha and Fernando
Garcia-Moreno are in the Department of Physiology,
Anatomy and Genetics, University of Oxford,
Oxford, UK.
e-mail: zoltan.molnar@dpag.ox.ac.uk
Readers in touch with this field might remember
recent studies showing the presence of a new
progenitor subtype in human, ferret and other
mammals with expanded, convoluted (gyren-
cephalic) cortices: the outer subventricular
zone (OSVZ) progenitor
1–3
(called interme-
diate radial glia by Reillo et al.
3
). A new study
based on cellular behavior, morphology and
gene expression pattern shows that similar
progenitors, termed outer radial glia (oRG) or
(by Shitamukai et al.
4
) outer ventricular zone
progenitors, reside in the developing mouse
cortex
5
. These oRG progenitors lack contact
with the ventricular (apical) surface, but they
maintain their tail-like pial (basal) processes
and thus appear to be ‘hanging’ from the pial
surface. They constitute a third population of
cortical progenitors, the others being radial
glia and intermediate progenitor cells (IPCs)
(Fig. 1a). Radial glial cells span the width from
ventricular to pial surface, undergoing interki-
netic nuclear migration during their cell cycle
and finally dividing at the ventricular surface.
IPCs are derived from asymmetric divisions of
radial glia cells; they express the transcription
factor Tbr2 and divide within the subventricu-
lar zone without nuclear translocation
6
.
The general readership might ask why this
topic is so newsworthy. The answer lies in the
widespread implications that understanding of
cortical progenitor populations has for stem
cell biology, cortical neurogenesis, evolution-
ary biology and comparative biology—leading
toward the ‘holy grail’ that is the comprehen-
sion of the expansion of the mammalian
cerebral cortex
7
. The Wang et al. paper
5
together with the Shitamukai et al.
4
publication
are landmarks because they link the previously
identified OSVZ progenitors in the human and
ferret to these oRG progenitors in the mouse,
thereby not only providing a highly accessible
model organism for which detailed quantita-
tive cell biological analyses are available, but
also reinforcing the concept of a uniform devel-
opmental mechanism for all mammals.
This entire line of research started with the
discovery of cytoarchitectonic distinctions
within the germinal zone in macaque and
human cortices. Smart et al.
8
described the
subventricular zone of the macaque cortex
as being subdivided into an inner subven-
tricular zone (ISVZ) and outer subventricular
zone (OSVZ) by a thin layer of fibers, the inner
fiber layer (Fig. 1a). Discovery of three cyto-
architectonically distinct germinal zones—the
ventricular zone, ISVZ and OSVZ—already
emphasized the heterogeneity of the cortical
progenitor populations
8,9
, although the mor-
phological details of the OSVZ progenitors
and their mode of cell division were not fully
understood
10
. Initially, the OSVZ compart-
ment in human and macaque was considered
an expansion of IPCs
11,12
, before gene expres-
sion data suggested some similarities with
radial glia
10
. Previous studies in human and
ferret had revealed the distinct morphology
and somal translocation behavior of OSVZ
progenitors
1,2
. Besides having a pially directed
process and lacking any contact with the ven-
tricular surface, these also express progenitor-
specific markers such as Sox2 and Pax6 and are
negative for the IPC marker Tbr2.
Although previous studies had suggested
that proliferative cell divisions occur within
the upper SVZ in rodent during embryonic
development
13
, the human and ferret studies
prompted the search for similar cells in the
mouse. The oRGs in mouse are less abundant
than in primates and do not reside in a cyto-
architectonically separate zone
1,5
(Fig. 1a).
The Kriegstein group exploited methods of
real-time recording to study labeled progenitor
neurons in slice cultures and combined these
with additional labeling methods
2,6
. They
injected GFP-expressing adenovirus or retro-
virus into the lateral ventricle or, to label oRGs,
injected GFP-expressing adenovirus at the pial
surface, and they followed labeled progenitors
and their cell divisions for prolonged periods.
This approach revealed all three progenitors—
oRG, radial glia and IPC—with their distinct
patterns of cell division. In addition, the
authors electroporated plasmids expressing
fluorescent proteins to visualize the nucleus
and cell shape. Such studies demonstrated that
radial glia progenitors show periods of interki-
netic nuclear migration (apical-to-basal move-
ment of nuclei in phase with the cell cycle)
punctuated by cell divisions at the ventricular
surface of the germinal zone
6
.
In their latest study, Wang et al.
5
used time-
lapse imaging to show that oRG progenitor
cells arise from asymmetric divisions of radial
glia and undergo self-renewing asymmetric
divisions in a horizontal plane to generate a
neuron (identified by morphology and from
the presence of the neuron-specific mark-
ers NeuN and Tuj1). The other daughter
cell inherits the basal process and maintains
an oRG morphology and Pax6 expression.
The authors also provide rare examples of
© 2011 Nature America, Inc. All rights reserved.