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First published online 14 February 2007
doi: 10.1242/dev.000265
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Molecular Neurobiology Laboratory, Medical Biotechnology Center, University of Southern Denmark, J. B. Winslowsvej 25, DK-5000 Odense C, Denmark.
* Author for correspondence (e-mail: naajensen{at}health.sdu.dk)
Accepted 5 January 2007
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SUMMARY |
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 TOP SUMMARY INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key words: Zbtb20, HOF, Zfp288, Znf288, BTB, Zinc finger, Cerebral cortex, Hippocampus, Development, Pyramidal neuron, Neurogenesis, Lamination, Migration
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INTRODUCTION |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Morphologically homogenous neurons constitute the compact
granule cell layer of the DG and the CA1 and CA3 pyramidal cell layer (or
stratum pyramidale) of the hippocampus. The subiculum comprises three distinct
subtypes of large pyramidal neurons that form the less-compact pyramidal cell
layer of this area (Ishizuka,
2001), whereas other areas of the hippocampal formation, the
transitional retrosplenial cortex and the neocortex, harbor several subsets of
pyramidal neurons organized in deep and upper layers
(Monuki and Walsh, 2001).
Neurogenesis of projection neurons in the dorsal telencephalon follows a
common path with area fate determination, activity-dependent refinement and an
inside-out developmental sequence, where first-born neurons reside in deep
layers of the cortical plate (CP) and later-born neurons prevail in outer
layers (Sur and Rubenstein,
2005). Cortical pyramidal neurons are generated by asymmetric
divisions of radial glia and progenitors within the ventricular zone (VZ) and
subventricular zone (SVZ) of the dorsal telencephalon, and migrate to the CP
along radially oriented processes of radial glia
(Rakic, 2006). Generation of
projection neurons from cortical progenitors appears to be governed by both
cell-intrinsic and environmental cues
(Fishell, 1995;
McConnell and Kaznowski, 1991;
Mizutani and Gaiano, 2006;
Qian et al., 1997). Cortical
stem cells and progenitors harbor a cell-intrinsic mechanism by which they can
generate preplate-like cells, deep and outer layer-like neurons and macroglia
in a `normal' developmental sequence in vitro
(Shen et al., 2006).
There are two notable developmental specializations to neurogenesis of the
hippocampal stratum pyramidale. First, immature pyramidal neurons in the
hippocampus migrate more slowly to the CP compared with the neocortical
pyramidal neurons (Altman and Bayer,
1990; Nakahira and Yuasa,
2005). Second, whereas lamination of most areas of the cerebral
cortex results from a process we refer to as variant corticoneurogenesis,
lamination of the hippocampus results from invariant corticoneurogenesis. The
former developmental process gives rise to the great diversity of pyramidal
neurons in the neocortical areas. The latter generates the two morphologically
homogenous CA1 and CA3 neuronal populations that constitute the stratum
pyramidale of the hippocampus. Defects in lamination of the hippocampus are
common in human congenital malformations of cortical lamination
(Montenegro et al., 2006;
Tanaka et al., 2006) and in
mice lacking the microtubule-associated proteins Doublecortin and
Doublecortin-like (Corbo et al.,
2002; Tanaka et al.,
2006).
Assuming that progenitors and newborn neurons are exposed to cell-intrinsic
and external changes in cues that trigger fate transitions, how is the
area-specific invariant morphogenesis of pyramidal neurons in Ammon's horn
accomplished? A number of genes have been shown to be important for various
aspects of neurogenesis in the hippocampus including proliferation and
specification of progenitors (Galceran et
al., 2000; Lee et al.,
2000; Machon et al.,
2003; Miyata et al.,
1999; Ohkubo et al.,
2004; Tole et al.,
2000; Zhao et al.,
1999). The mammalian BTB-zinc finger gene Zbtb20 (also
known as HOF, Znf288, Zfp288), hereon referred to as Zbtb20,
is expressed during the critical period of neurogenesis of pyramidal neurons
in areas CA3 and CA1 of the mouse hippocampus
(Mitchelmore et al., 2002).
Here we show that Zbtb20 induces hippocampus-like corticoneurogenesis in the
mouse brain following ectopic expression of the gene in non-hippocampal
immature pyramidal neurons. We furthermore find that Zbtb20 delays the radial
migration of immature cortical neurons and orchestrates the formation of a
CA-like pyramidal cell layer in the subiculum and posterior retrosplenial
cortex.
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MATERIALS AND METHODS |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) was inserted into Zbtb20S and
Zbtb20L expression plasmids. For microinjection, the
D6/Zbtb20S and D6/Zbtb20L transgenes were excised from
the plasmid vector, gel-purified and microinjected, at a concentration of 6
ng/µL, into the pronucleus of fertilized mouse eggs as previously described
(Jensen et al., 1993). A total
of five transgenic mouse lines (two D6/Zbtb20S and three
D6/Zbtb20L) with ectopic cortical Zbtb20 expression were generated.
All five lines displayed similar structural alterations in cortical lamination
ruling out insertional mutagenesis as a cause of the phenotype. Accordingly,
we selected two representative Zbtb20 transgenic lines (one
D6/Zbtb20S and one D6/Zbtb20L) for the studies described
in this report. Transgenic mice were identified by PCR genotyping of genomic
DNA purified from tail biopsies, using the Wizard genomic DNA purification kit
(Promega). The primers used for the PCR analysis were:
5'-GAGAGAGGACTCGCATTTCGACTTG-3' and
5'-GATGCGAACCGTCACGTCACAGAAG-3', which produce a 354 bp PCR
product using genomic DNA from D6/Zbtb20S mice as template, and a
573 bp product using DNA from D6/Zbtb20L mice as template.
Transfection of cells in vivo by in utero electroporation was performed as
previously described (Nakahira and Yuasa,
2005; Tabata and Nakajima,
2001). Briefly, multiparous mice at 15 days of gestation were
deeply anesthetized, and the uterine horns were exposed. Approximately 1 µL
of pCIG2-EGFP plasmid (Hand et al.,
2005), at a concentration of 4 µg/µL with 0.01% Fast Green
(Sigma), was injected through the uterus into the lateral ventricles of
embryos. Eight 50-millisecond electric pulses of 40 V were delivered in
intervals of 80 milliseconds, directing the DNA towards the medial-dorsal
telencephalon. The voltage pulse was discharged using a pair of
disc-electrodes placed on either side of the head of each embryo through the
uterus. The uterus was placed back in the abdominal cavity to allow embryonic
development to continue to term. Brains from neonatal (P0) and P14 mice were
dissected out and fixed overnight in 4% paraformaldehyde (PFA), embedded in 5%
agar in phosphate-buffered saline (PBS) and subsequently sectioned at 100
µm using a vibratome (Leica VT1000S). The sections were counterstained with
DAPI, and enhanced green fluorescent protein (EGFP) fluorescent
(EGFP+) cells were visualized and photographed. For cell counting,
four subregions in the P0 cerebral cortex [VZ/SVZ, intermediate zone (IZ),
deep and superficial half of the CP] were identified based on cell density, as
visualized with DAPI. The total number of EGFP+ cells in each
region was counted in two adjacent coronal sections at mid-posterior axial
levels from three Zbtb20S transgenic mice (2200 cells in total) and
three control mice (3000 cells in total). All animal protocols were approved
by the Danish Ministry of Justice Animal Care and Use Committee.
Golgi staining
Modified Golgi-Cox impregnation of neurons was performed using
specifications described in the FD Rapid GolgiStain Kit (FD
Neurotechnologies). In brief, 2-month-old mouse brains were immersed in
impregnation solution for 2 weeks, transferred to `Solution C' for 2 days,
embedded in 5% agar in PBS and cut at 100 µm on the microtome. Sections
were mounted on superfrost plus slides (Menzel-Gläser) and dried for 2
weeks prior to staining with silver nitrate solution `Solution D and E'. The
sections were dehydrated and mounted with Depex.
Immunohistochemistry
In some cases, mice were given an intraperitoneal injection of 0.1 mg of
bromodeoxyuridine (BrdU)/g body weight (diluted in physiological saline)
before they were sacrificed. The brains were removed and immediately frozen in
liquid nitrogen. Cryostat-cut brain sections (20 µm) were collected on
superfrost plus slides, fixed with methanol for 5 minutes and incubated for 1
hour at 37°C or overnight at 4°C, in the presence of a primary
antibody that was diluted in PBS with 0.1% Triton X-100. The following primary
antibodies were used at 1:100 dilution unless otherwise stated: rabbit Zbtb20
(Mitchelmore et al., 2002);
mouse NeuN (Chemicon); mouse reelin (Abcam); goat Brn-1 and goat Brn-2 (Santa
Cruz); rabbit Oct-6, diluted 1: 500 (Sock
et al., 1996). For staining with sheep BrdU antisera, diluted
1:200 (Research Diagnostics), the fixed sections were first treated for 30
seconds each with 2 M HCl and 0.1 M borate. After rinsing in PBS, sections
were incubated for 1 hour at 37°C in secondary antibody diluted in PBS
with 0.1% Triton X-100, washed in PBS and mounted with Vectashield mounting
medium with DAPI (Vector Laboratories). The following secondary antibodies
were used at 1:100 dilution: TRITC-conjugated swine anti-rabbit;
FITC-conjugated goat anti-mouse; FITC-conjugated rabbit anti-mouse;
FITC-conjugated rabbit anti-goat (DAKO); and FITC-conjugated donkey anti-sheep
(Research Diagnostics Inc.). ER81 immunohistochemistry was carried out on 20
µm PFA-fixed cryosections, which were first incubated for 2 hours in PBS
containing 10% normal goat serum and 0.1% Triton X-100. Sections were then
incubated for 48 hours at 4°C with the primary rabbit ER81 antibody
(Arber et al., 2000), diluted
1:200 in PBS containing 0.1% Triton X-100. After rinsing in PBS, sections were
incubated for 1 hour at 37°C in biotinylated goat anti-rabbit antibody
(DAKO), in PBS containing 0.1% Triton X-100. Sections were then rinsed in PBS
and incubated in Vectastain Elite ABC Reagent using diaminobenzidine
tetrahydrochloride (DAB) as the substrate, according to the manufacturer's
instructions (Vector Laboratories).
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Behavioral tests
A total of 13 Zbtb20S transgenic and 11 wild-type adult female
littermate mice were used in the behavioral test. The two groups of mice were
housed three to five together in standard cages with ad libitum access to food
and water. All animals were maintained on a 12-hour light-dark cycle. The
visual cliff test was performed between 10.00 h and 14.00 h, and the circular
platform maze test was performed between 18.00 h and 23.30 h.
The visual cliff test apparatus was prepared according to specifications
described elsewhere (Fox,
1965). It consists of an elevated horizontal plane (safe side)
connected to a 60 cm vertical drop followed by a second horizontal plane (deep
side). Both horizontal planes were covered with 2 cm2 black and
white checkerboard pattern paper to accentuate the vertical drop-off. A sheet
of clear Plexiglas was placed across the top horizontal plane, extending
across the cliff so that there was no actual drop-off, just the visual
appearance of a cliff. The edge of the cliff harbors a ridge of aluminium, 40
mm high and 25 mm wide. Each mouse was placed on the aluminium block at the
start of ten consecutive trials, and allowed to step down to one of the sides
(safe or deep). The choice of side was recorded.
The circular platform maze was carried out as previously described
(Pompl et al., 1999) with some
modifications. Briefly, the behavioral testing consisted of 17 trials, with
one trial per day. During the first 10 days of the trial (the learning period)
the location of the escape box was maintained in the same position. In the
reverse learning period, which lasted for a total of 7 days, the escape box
was moved to a new position 180° from its previous location. Mice were
introduced into the maze at three different orientations relative to the
escape hole (90°, 180° or 270°). Each mouse was allowed a maximum
of 300 seconds per trial. The total numbers of errors (nose pokes into
non-escape holes) and latency to enter the escape hole were recorded. During
the reverse learning period, the mice were introduced into the maze at
orientations of 90° or 270° to the escape hole. The number of nose
pokes into the learning period escape hole was recorded as `probes'.
Statistics
The percentage of EGFP+ cells in each of the four cortical
subregions was compared between control and Zbtb20S transgenic mice
using Student's t test. The preference for stepping down to the safe
or deep side of the visual cliff was analyzed using paired Student's
t test. The number of steps to the safe side was analyzed using
Student's t test. Circular platform maze data including latencies and
errors to find the escape hole during the learning period (days 1 to 10) and
the reverse learning period (days 11-17) were analyzed using repeated measures
(RM) analysis of variance (ANOVA). Paired Student's t test was used
to compare the number of errors and escape latencies between days 10 and 11.
Student's t test was used to analyze differences in latencies (on the
same day) and errors (at day 17) between the two groups of mice. In addition,
Student's t test was used to compare the number of probes to the
learning period escape hole at day 11 with the number of probes to each of the
remaining 15 holes. Whenever the data were not normally distributed, the
median values were compared using the Mann-Whitney rank sum test. A
P-value of less than or equal to 0.05 was considered to be
significant. All data are depicted as means±s.e.m. All statistics were
done using SigmaStat (SPSS).
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RESULTS |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Similar malformations of cortical development, which generally appear to be most pronounced at medial-posterior levels along the anterior-posterior axis, are observed in adult Zbtb20S, Zbtb20L and Zbtb20S/L transgenic mice (Fig. 3A-M and data not shown). Although present at anterior axial positions (Fig. 3A,D,G), the corpus callosum is lacking at more posterior levels (Fig. 3B,E,H). At medial-posterior positions, the subicular and retrosplenial areas are transformed into a three-layered archicortex composed of a compact hippocampus-like pyramidal cell layer and a markedly expanded apical dendrite layer (Fig. 3C,F,I,J,K). The compact CA-like laminar transformation of the subiculum was confirmed in horizontal brain sections (Fig. 3L,M). The transformed retrosplenial area of Zbtb20 transgenic mice comprises a single stratum pyramidal-like cell layer composed of large homogeneous-appearing neurons with a marginal zone projecting apical dendrites (Fig. 4). The transformed neurons are typical pyramidal-like with basal and apical dendrites covered with spines, and they show a morphologic resemblance to CA1 pyramidal cells (Fig. 4F,G).
As developmental transformations of the Zbtb20 transgenic cortex are most
pronounced at posterior axial levels, we performed molecular marker analyses
on subicular, posterior retrosplenial and visual areas. The transcription
factor Oct-6 (Pou3f1; also known as Scip and Tst1) is a marker of CA1 and
layer V pyramidal neurons in adult rodent brains
(Fig. 5A,B)
(Frantz et al., 1994). In
Zbtb20 transgenic brains, there is a robust Oct-6 immunostaining of cells in
subicular and medial retrosplenial areas, which is similar in intensity to
that of cells in the CA1 area of the hippocampus
(Fig. 5G,H), but different from
the scattered staining of cells in wild-type subicular and medial
retrosplenial areas (Fig.
5A,B). The ETS family transcription factor ER81 (Etv1 - Mouse
Genome Informatics) is expressed in subsets of subicular and layer V pyramidal
neurons in various cortical areas including the retrosplenial cortex
(Fig. 5C)
(Yoneshima et al., 2006). In
contrast to wild-type brains, ER81-positive cells were not revealed in
subicular and retrosplenial areas of Zbtb20 transgenic brains
(Fig. 5I), further supporting
the notion of a CA-like transformation of these regions. Expression of Brn-1
and Brn-2 (Pou3f3 and Pou3f2, respectively - Mouse Genome Informatics),
markers of superficial cortical layers and SVZ of the neocortex at P0
(McEvilly et al., 2002), was
detected in upper CP and SVZ by immunohistochemistry of wild-type brains
(Fig. 5D,E), but was not
revealed in visual (dorsal) and posterior retrosplenial (medial) areas of
Zbtb20 transgenic brains (Fig.
5J,K). In lateral areas of the Zbtb20 transgenic visual cortex,
Brn-1 and Brn-2 immunoreactive cells formed cortical nodules in superficial
layers that are separated from deep layers by a cell-sparse transition zone
(Fig. 5M-P). Reelin is a
glycoprotein secreted from a population of early appearing cortical neurons
termed Cajal-Retzius (CR) cells that settle in the marginal zone
(D'Arcangelo et al., 1997). The
protein appears to guide placement of migrating projection neurons in the CP.
Reelin-positive CR cells were found in the marginal zone of the cerebral
cortex in both normal mice (Fig.
5F) and Zbtb20 transgenic littermates
(Fig. 5L). Thus, there appears
to be a deficiency in subsets of deep and outer layer pyramidal neurons in
Zbtb20 transgenic brains.
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).
Consistent with a deficiency in processing visual cues
(Fig. 6A), Zbtb20 transgenic
mice stepped down to both the safe and deep sides at roughly equal frequencies
(P=0.157), whereas the wild-type littermate mice showed a strong
preference for the safe side (P<0.001). The two groups of mice
were furthermore tested in the circular platform or Barnes maze, which
measures spatial navigation memory (Pompl
et al., 1999). In the 10-day learning period, both wild-type and
Zbtb20 transgenic mice showed a statistically significant improvement in
performance (Fig. 6B and see
Table S1 in the supplementary material) that correlated with a significant
reduction in errors prior to locating the escape box
(Fig. 6C). However, wild-type
mice appeared to use spatial cues to move directly to the escape hole, whereas
Zbtb20 transgenic mice explored the periphery of the platform to locate the
same hole. In the reverse learning period (starting at day 11), the escape box
was moved to a new location 180° relative to the old position. At the
first trial day of this phase, the wild-type mice, but not the transgenic
mice, showed a statistically significant increase in latency and number of
errors (P=0.007 and P=0.002, respectively) compared with the
last trial day of the learning period (Fig.
6B,C). To reveal whether or not the two groups of mice have
recollection of the location of the learning period escape hole, the number of
visits to this hole (probes) was compared with the number of visits to each of
the remaining 15 holes on the first day of the reverse learning period. The
wild-type mice showed a preference for the old escape hole that was not
observed in the transgenic group (Fig.
6D and see Table S2 in the supplementary material). Thus, whereas
wild-type mice appear to remember the location of the escape hole from the
learning phase, Zbtb20 transgenic mice apparently have no recollection of this
hole. Moreover, there was an apparent improvement in the wild-type group to
locate the escape hole that correlated with a statistically significant
decline in both escape latency (P<0.001) and number of errors
(P<0.001). A similar statistically significant effect was not
revealed in the Zbtb20 transgenic group
(Fig. 6B,C). For example at
trial day 17, the wild-type mice were significantly faster at locating the
escape hole (P=0.003), and made significantly fewer errors than the
Zbtb20 transgenic mice (P<0.001). |
DISCUSSION |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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).
The gene is turned on in newborn immature pyramidal neurons in upper layers of
the SVZ in the presumptive hippocampus and is downregulated in these cells
during the second postnatal week. Ectopic Zbtb20 expression in newborn neurons
was shown to occur in medial areas of the dorsal telencephalon of Zbtb20
transgenic mice. The extent of lamination of the neocortex was more variable
compared with the transitional posterior retrosplenial cortex, with some areas
harboring only a thin sheath of cells and a markedly expanded layer I (e.g.
Fig. 3G,H,K). Our preliminary
analyses of ectopic Zbtb20 expression in transgenic brains revealed a more
consistent expression in posterior medial-dorsal areas of the dorsal
telencephalon compared with lateral and anterior areas (e.g.
Fig. 1F,G and not shown). In
line with this, the visual cortex generally appeared to be the most severely
affected neocortical area (e.g. Fig.
3F). Although molecular marker analyses indicated a general
deficiency in subsets of outer and deep layer pyramidal neurons in posterior
areas, we did observe clusters of neurons expressing outer layer markers at
lateral axial positions (Fig.
5N,P). This is consistent with a variable expressivity of the
Zbtb20 transgene during neocortical neurogenesis. Alternatively, this
heterogeneity in neocortical projection neuron development could potentially
result from ectopic and heterochronical expression of exogenous Zbtb20 during
early stages of corticoneurogenesis. The malformations of lamination result in
behavioral abnormalities suggestive of impaired processing of visual and
spatial memory traces in the cerebral cortex of adult Zbtb20 transgenic
mice.
BTB-zinc finger factors can regulate key developmental processes in
organisms as diverse as insects and mammals. In the fly nervous system, the
BTB-zinc finger protein Chinmo was recently reported to specify temporal
identity of neuroblast progeny (Doe,
2006; Zhu et al.,
2006). In both mushroom body and projection neuron lineages, loss
of Chinmo causes early-born neurons to adopt the fates of late-born neurons.
In contrast, the temporal identity of mushroom body progeny was transformed
toward an early fate by ectopic expression of Chinmo protein. The BTB-zinc
finger factor Abrupt regulates the morphogenesis of class I dendritic
aborization neurons, and ectopic expression of Abrupt in non-class I neurons
altered the dendritic morphology of these cells
(Li et al., 2004;
Sugimura et al., 2004). Apart
from Zbtb20, little is known about the role of BTB-zinc finger factors in
neurogenesis of the mammalian brain. Outside the brain, the BTB-zinc finger
factor Th-POK/cKrox functions as a molecular switch that turn immature
thymocytes into CD4+ helper T cells
(He et al., 2005;
Sun et al., 2005). Immature
thymocytes develop into CD8+ killer T cells in the absence of this
BTB-zinc finger factor, whereas transgenic overexpression of the gene
redirected major histocompatibility complex class I (CD8+) cells to
class II restricted CD4+ helper T cells. Moreover, the
Zbtb20-related Bcl-6 protein represses several genes that are necessary for
terminal differentiation of B cells (Ahmad
et al., 2003; Kelly and
Daniel, 2006). At the molecular level, BTB-zinc finger proteins
have been proposed to be involved in chromatin remodeling, including
transcriptional repression of downstream genes by recruitment of
co-repressor-histone deacetylase complexes or polycomb group proteins
(Ahmad et al., 2003;
Barna et al., 2002;
Gearhart et al., 2006;
Kelly and Daniel, 2006).
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;
Shen et al., 2006). As
asymmetric divisions of cortical precursors result in cells with distinct
fates, asymmetric distribution of cell-fate determinants is important for
appropriate development of differentiated daughter cells and may also affect
the developmental potential of the progenitor daughter cells. The
telencephalic transcription factor Foxg1 is required to switch off CR neuronal
fate in progenitors, whereas loss of Foxg1 in cortical progenitors results in
untimely CR neurons production (Hanashima
et al., 2004). The hippocampus-like transformation of the
posterior retrosplenial cortex in Zbtb20 transgenic mice is remarkable, as
pluripotent cortical precursors in this area normally generate subsets of
neurons that settle in distinct layers. Our results are consistent with a
model in which Zbtb20 functions as a molecular switch in a pathway that
orchestrates invariant pyramidal neuron morphogenesis and suppresses cell-fate
transitions in newborn neurons (Fig.
7). The endogenous Zbtb20 gene is expressed during the
critical period of development of four homogenous populations of neurons in
the mouse brain including pyramidal neurons in areas CA1 and CA3 and granule
neurons in the dentate gyrus and cerebellum
(Mitchelmore et al., 2002). It
will be important to determine whether or not Zbtb20 is essential for
invariant neurogenesis of these neurons. Moreover, as Zbtb20 is likely to be a
high-level regulator of gene expression, identification of its target genes
will be important to reveal factors that act downstream in the Zbtb20
pathway.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/134/6/1133/DC1
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0.001. Deep, deep half of CP; Superficial, superficial half of
CP.
