TIGEM (Telethon Institute of Genetics and Medicine), Via P. Castellino 111, 80131 Napoli, Italy
Author for correspondence (e-mail:
studer{at}tigem.it)
Accepted 13 October 2004
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SUMMARY |
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Key words: COUP-TFs, Cell migration, Forebrain, Mouse
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Introduction |
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As suggested by various studies, directional migration can be achieved by
short-range guidance cues and by long-range diffusible gradients
(Tessier-Lavigne and Goodman,
1996). Contact guidance relies on a permissive environment, on
which gradients of diffusible guidance molecules can be superimposed, to
achieve directional migration. However, the distribution and molecular nature
of short- and long-range molecules, and the substratum that interneurons use
in their migration towards the cortex, are poorly understood. Motogenic
factors, such as hepatocyte growth factor and the neurotrophin molecules BDNF
and NT4, have been shown to influence the numbers of cells migrating away from
the subpallium (Polleux et al.,
2002
; Powell et al.,
2001
). Guidance molecules with repulsive and attractive activities
are likely to be involved in guiding migrating cells from the subpallium to
the pallium, and within the subpallium
(Marin et al., 2003
;
Wichterle et al., 2003
). For
the substratum, one report has shown that blocking the function of the TAG1
adhesion molecule results in a marked reduction in GABAergic neurons in the
cortex (Denaxa et al., 2001
).
However, in Tag1 mutant mice, there is no major alteration in the
tangential migration of interneurons
(Marin and Rubenstein, 2003
),
and treatment of cortical slices with phosphoinositide-specific phospholipase
C (PI-PLC), an enzyme that cleaves GPI-anchored proteins, such as TAG1, does
not alter interneuron migration (Tanaka et
al., 2003
). Therefore, nothing is known about the nature of
short-range guidance contact cues involved in tangential migration.
The nuclear orphan receptor COUP-TFI favours migration of neurons through
an integrin-dependent mechanism in cell cultures
(Adam et al., 2000).
Overexpression of COUP-TFI in retinoic-acid-treated neuronal aggregates coated
with different cell substrata, such as polylysine, laminin or fibronectin,
results in a higher rate of migration compared with controls, whereas
overexpression of a mutated form of COUP-TFI has no effects on cell migration.
Moreover, increased levels of vitronectin, an extracellular matrix (ECM)
molecule involved in neurite extension, motor neuron differentiation and
possibly neuronal migration, are detected both in aggregate and monolayer cell
cultures after overexpression of COUP-TFI. This, and the data that show that
COUP-TFI stimulates transcription from the vitronectin promoter in vitro,
strongly suggests a role of COUP-TFI in the regulation of ECM synthesis during
the process of neuronal migration. Although COUP-TFI has been shown to be
involved in cortical regionalization and axon pathfinding in the developing
telencephalon (Zhou et al.,
1999
; Zhou et al.,
2001
), its role in promoting cell migration in vivo has not been
established so far.
Here, we show that COUP-TFI and COUP-TFII are expressed in migrating cells in specific pathways in the basal telencephalon of mouse embryos at a stage when interneuron migration is robust. Moreover, expression of COUP-TFI in the cortex co-localizes with the GABAergic marker calbindin, suggesting that a subpopulation of COUP-TFI-positive cells in the cortex are GABAergic interneurons. With the help of transplantation and tracing techniques in organotypic slice cultures, we first show the presence of a dorsal-to-ventral migratory pathway that originates in the region of the interganglionic sulcus. We then demonstrate that COUP-TFI is expressed in the basal telencephalon in neurons not only migrating dorsally towards the cortex, but also ventrally towards the pre-optic area (POa) and the hypothalamus. Finally, by ectopic expression of COUP-TFI and COUP-TFII in the GEs, we show an increased rate of migrating cells. While COUP-TFI appears to control dorsal and ventral migration in the basal telencephalon, COUP-TFII is more specific in modulating tangential migration into the intermediate zone of the cortex, suggesting distinct functions of COUP-TFs in regulating cell migration in the developing forebrain.
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Materials and methods |
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Slice culture experiments
Organotypic slice cultures of embryonic mouse telencephalon were prepared
as previously described (Anderson et al.,
1997). Brain slices 250 µm thick were used for the grafting
experiments (see below), for tracing with the fluorescent carbocyanide dye
1,1'-dioctadecyl 3,3,3',3'-tetramethylindocarbocyanine
perchlorate (DiI; Molecular Probes), and for electroporation and lipofectamine
injections (see below).
Grafting experiments
For the grafting experiments, the MGE, the LGE, or the region at the
MGE/LGE border (MLGE) were removed from the donor brain slices derived from a
green fluorescent protein (GFP)-expressing transgenic embryo
(Hadjantonakis et al., 1998)
and transferred to the same position in a host wild-type brain slice. The
chimaeric slices were examined 1 hour after the transplant under a stereoscope
with a GFP filter, to confirm that the transplants were successfully and
correctly integrated into the host; slices where the grafts did not integrate,
or integrated in an incorrect location, were not used for this study. The
medium was changed every day, and after about 60 hours the slices were fixed
in 4% paraformaldehyde.
Electroporation and lipofectamine-mediated injection
For the fate map, a GFP-expressing vector was electroporated into the GEs
of embryonic day (E) 13.5 brain slices using the same method and conditions as
described previously (Stuhmer et al.,
2002). For the gain-of-function approach, we used the PolyFect
Transfection Kit (Qiagen, Hilden, Germany), containing 250 ng/µl of the
expression vectors (CMV-GFP or CMV-COUP-TFs-IRES-GFP). Full-length mouse
COUP-TFI and COUP-TFII (kindly donated by M. Tsai, Baylor College, USA) were
cloned into the BamHI-XhoI sites of the pIRES-hrGFP-2a
expression vector (Stratagene, California, USA). We injected the constructs
into the desired region of the brain slices, under microscopic guidance with a
micro-syringe (Hamilton, Reno, Nevada, USA) held by a micromanipulator system
using a 33-gauge blunt-ended needle (Hamilton). The slices were then cultured
for 60 hours, fixed in 4% paraformaldehyde, and either observed by confocal
microscopy (Leica DMIRE2) or embedded in OCT for further sectioning in a
cryostat.
Immunohistochemistry and immunofluorescence
The brains were sectioned and treated for immunostaining according to
standard procedures. Combined immunohistochemistry and in-situ hybridization
on cryosections were carried out as described previously
(Hirsch et al., 1998). The
times of incubation with the primary antibodies ranged from 90 minutes
(anti-COUP-TFs, anti-reelin) to overnight. The following antibodies were used:
rabbit
-COUP-TFI (1:500), rabbit
-COUP-TFII (1:1000), mouse
-reelin (clone G10, 1:500; kind gift of A. Goffinet), mouse
-calbindin (clone CB-955, Sigma, 1:500), mouse
-GABA (clone
GB-69, Sigma, 1:1000) and mouse
-ß-tubulin type III (clone
SDL.3D10, Sigma, 1:400). Sections were alternatively incubated in a
biotinylated secondary antibody (Vector, 1:200) and processed by the ABC
histochemical method (Vector) or with a fluorescent secondary antibody
(Molecular probes 1:400; Alexafluor 488
-rabbit, Alexafluor 594
-rabbit, Alexafluor 594
-mouse) for 1 hour at room temperature.
The immunohistochemistry-treated sections were dried, dehydrated and mounted
on a coverslip with Permount (Fisher); the immunofluorescence-treated sections
were mounted with Vectashield (Vector). The GFP was detected by its endogenous
fluorescence.
Cell counting
In the grafting experiments, the cells were counted on images obtained from
6 µm sections of the slices that were acquired with a CCD camera attached
to a conventional microscope. To count the cells, a standardized box (a
40x enlargement of the slice) was used; for each transplant, three
sections were evaluated, and for each section, the cells in two different
regions were counted. In the gain-of-function experiments, an image of the
whole slice was obtained by confocal microscopy, after reconstruction of all
of the confocal planes. The GFP-positive cells that migrated towards the
cortex or towards the POa were counted on this reconstructed image, and
normalized for the total number of GFP-positive cells [e.g. cortex/(cortex +
basal ganglia), or POa/(POa + basal ganglia)]. The data from control and
overexpressing cells within the same slice were compared, and paired Student's
t-tests were used for the analysis.
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Results |
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To study the expression profile of both COUP-TFs during the period of neural migration, we performed immunohistochemistry on E13.5 mouse forebrains, when tangential migration is well pronounced. At this stage, COUP-TFI expression was localized to all layers of the neocortex, to the piriform cortex, to the ventricular and subventricular zones of the LGE, to the ventricular zone of the MGE, to the POa, and in scattered cells in various regions of the basal telencephalon (Fig. 1A). By contrast, COUP-TFII expression was mainly restricted to the marginal zone of the neocortex and to the piriform cortex and POa of the basal telencephalon. Scattered COUP-TFII-positive cells were also identified in the LGE, at the cortico-striatal boundary, and in the intermediate zone of the neocortex (arrowheads in Fig. 1A'). Expression of COUP-TFI and COUP-TFII was also seen in the interganglionic region where the MGE and LGE are fused, but before the appearance of the CGE (asterisk in Fig. 1A,A'). For convenience, we will define this area as the `MLGE border' henceforth. Double labelling for COUP-TFI and COUP-TFII and COUP-TFI and COUP-TFII highlighted an increased expression of COUP-TFs in this region (insets in Fig. 1A,A').
|
In summary, COUP-TFI and COUP-TFII showed distinct and mostly non-overlapping expression profiles in the developing telencephalon at E13.5. Furthermore, COUP-TFs appeared to be expressed in migrating cells at the stages in which several tangential migratory pathways within the developing telencephalon are well pronounced.
COUP-TFs are detected in specific and non-overlapping cellular populations in the developing cortex
To characterize the types of cells in which COUP-TFs are expressed, we
performed a series of double immunofluorescence studies for both COUP-TFs and
cell-type-specific markers (Fig.
2).
|
Taken together, these data strongly suggest that in the cortex COUP-TFI is expressed in GABAergic interneurons, whereas COUP-TFII is expressed in Cajal-Retzius cells.
COUP-TFI, and not COUP-TFII, is expressed in neurons migrating tangentially from the basal telencephalon to the cortex
We have previously shown that some COUP-TFI-positive cells in the cortex
are GABAergic interneurons. It is now well established that the GEs are the
major source of most neocortical interneurons (reviewed by
Corbin et al., 2001;
Marin and Rubenstein, 2001
).
Therefore, to assess whether COUP-TFI-positive cells located in the basal
telencephalon are interneurons migrating to the cortex, a series of grafts
from the GEs of E13.5 GFP-expressing transgenic brain slices were
homotopically transplanted into wild-type E13.5 brains (n=27)
(Fig. 3A); expression of
COUP-TFI and COUP-TFII was subsequently monitored in adjacent sections of the
same slices. An example of an MLGE graft is shown in
Fig. 3B, which demonstrates the
fate of fluorescent cells after 60 hours of incubation, at which point
GFP-positive cells were distributed in the mantle layer of the basal
telencephalon and in various layers of the cortex. High magnification of the
lateral and medial cortex showed that GFP-positive cells were present in the
marginal and intermediate zones (Fig.
3C,F). Interestingly, some GFP-positive cells were also present in
deeper layers, with a radial orientation towards the surface of the cortex
(arrows in Fig. 3C-E). These
cells were previously reported to migrate from the marginal zone to the
ventricular zone before moving radially, to take up their positions in the
cortical anlage (Nadarajah et al.,
2002
). After double labelling with anti-COUP-TFI, 75% of the
GFP-positive cells (n=250) were also positive for COUP-TFI, including
the ventricle-directed cells (Fig.
3E). Adjacent sections of the same grafted brain slices showed no
co-localization of COUP-TFII and GFP (Fig.
3H). This is in agreement with the observation that
COUP-TFII-positive cells in the cortex are non-GABAergic, and therefore do not
originate from the basal telencephalon. Thus, our data confirm that COUP-TFI
in the cortex is expressed in GABAergic interneurons originating from the
subpallium, whereas COUP-TFII expression has a pallial origin.
|
|
Finally, to assess whether ventrally directed migration also originates from more caudal levels, we grafted the CGE of a GFP E13.5 mouse brain to a wild-type brain of the same stage (n=5) (Fig. 5A). After 60 hours of incubation, GFP-positive cells migrated out of the graft into two main streams: a medial stream directed towards the third ventricle, and a lateral stream directed laterally and ventrally into the hypothalamic region (Fig. 5B). Both streams contained single neurons with short and polarized leading processes indicative of migrating cells (Fig. 5C-F). Adjacent sections of the same brain slices showed co-labelling of GFP with COUP-TFI (Fig. 5C,D), whereas no COUP-TFII-positive cells were co-localized with GFP-positive cells (Fig. 5E,F).
|
Ectopic expression of COUP-TFI in the basal telencephalon promotes cells to migrate in both dorsal and ventral directions
At this stage, we have demonstrated that a subpopulation of
COUP-TFI-positive cells in the basal telencephalon are cells that are in the
process of migrating; however, this does not demonstrate that COUP-TFI is
directly involved in migration. To address this issue, we set up a functional
assay in E13.5 brain slice cultures, in which we ectopically expressed
COUP-TFI in the GEs at different dorso-ventral and antero-posterior locations.
The migrating cells were followed after 60 hours of incubation. On one side,
and as a control, we injected a construct expressing GFP under the control of
a CMV promoter, while on the contralateral side, we injected a construct
expressing COUP-TFI followed by an IRES-GFP sequence. In this way, we could
follow the fate of the injected cells by following GFP fluorescence in the
same slices (Fig. 6A). The
histogram in Fig. 6B shows the
average value of GFP-positive cells in the cortex and POa, expressed as a
percentage of the total number of positive cells (for control 2838 cells, and
for COUP-TFI 2318 cells; n=25; see also Materials and methods for
details). In all the cases examined, the COUP-TFI-injected sides showed a
statistically significant increase in the number of cells in the cortex,
compared with the control side (Fig.
6B-D). Ventral migration was observed only in caudal sections in
which the constructs were focally injected into the subventricular zone of the
MLGE region (Fig. 6A). In
controls, 24% and 17% of GFP-positive cells were scored on average in the
cortex and in the POa, respectively (Fig.
6B), whereas the non-migrating cells were maintained in compact
clusters next to the injection site. The injection of a CMV-COUP-TFI-IRES-GFP
construct into the contralateral side of the same slices resulted in
GFP-positive cells that were more dispersed in the mantle layer (arrowheads in
Fig. 6D), and that were still
in the process of migrating dorsally towards the marginal zone of the cortex
and ventrally towards the POa (arrows in
Fig. 6D). Moreover, a higher
number of GFP-positive cells were scored in the cortex and in the POa (72% and
46%, respectively), compared with the control side. Thus, in the presence of
higher levels of COUP-TFI, injected cells showed significantly increased
spreading and migrating, compared with the normal situation
(Fig. 6B), suggesting that
COUP-TFI modulates cell migration in the basal telencephalon.
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Discussion |
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In this report, we have identified a novel migratory path, which to our
knowledge has never been reported before. Using grafting experiments, DNA
electroporation and tracer injections, we have shown that cells located in the
interganglionic region, where the MGE and LGE fuse together, have the
capability of migrating ventrally towards the pre-optic and hypothalamic
regions of the diencephalon (Figs
3,
4,
5). As this path originates
from the interganglionic region at specific caudal levels, it is very likely
that it has been missed in other studies using similar approaches
(Anderson et al., 2001;
Jimenez et al., 2002
;
Lavdas et al., 1999
;
Wichterle et al., 2001
). The
novelty of this path is twofold: first, cells migrate tangentially from dorsal
to ventral, along the subventricular zone of the MGE, i.e. in opposite
directions with respect to the MGE-derived cortical interneurons; and second,
these cells exit the basal telencephalon and migrate into the basal
diencephalon. These cells are different from the gonadotropin-releasing
hormone neurons, which originate in the olfactory placode and migrate along
the vomeronasal nerve fibres until they reach the POa and hypothalamus
(Wray et al., 1994
;
Yoshida et al., 1995
).
Migration of GABAergic neurons from the GEs to the dorsal thalamus has been
observed in human brains; however, rodent embryos did not reveal a similar
migratory pathway (Letinic and Rakic,
2001
). With the help of retroviral cell tracing, Marin and
collaborators (Marin et al.,
2000
) have shown that cells emanating from the MGE and the
adjacent POa/anterior entopeduncular area express the transcription factor
Nkx2.1 and migrate to the developing striatum, where they
differentiate into local circuit neurons. It would be interesting to find out
whether Nkx2.1 is also involved in the opposite migratory path
described in this report.
Furthermore, we have shown that cells originating from the CGE migrate via
different streams into the basal diencephalon, and in particular into the
hypothalamus (Fig. 5B). As
opposed to the MLGE transplant, in which the stream of ventrally migrating
cells is quite compact, cells migrating out of the CGE take a medial and
latero-ventral route. We do not know the fate of these ventrally migrating
cells. In-vivo ultrasound-guided labelling or transplantation
(Nery et al., 2002;
Wichterle et al., 2001
), in
which total cortices are manipulated in toto and characterized at later
stages, would help us to understand the final destinies of these migrating
cells.
Is the basal telencephalon only chemorepulsive?
Transplantation experiments and co-culture assays have shown that the POa
and hypothalamic regions prevent interneurons from migrating in a ventral
direction by secreting repulsive molecules that are responsible for the dorsal
migration of interneurons towards the cortex
(Marin et al., 2003;
Wichterle et al., 2003
).
However, the cues mediating this action have not been identified yet. Here, we
show that cells originating from more dorsal and caudal regions are capable of
migrating ventrally towards the POa/anterior hypothalamus. How do we reconcile
these different results? First, the previous studies showed that the majority
of interneurons that originated from the MGE avoided migrating in ventral
directions. This is what is expected for a circumscribed graft in a section
where the two GEs are well separated
(Marin et al., 2003
) (data not
shown). However, the dorsal-to-ventral cell migration that we describe in this
report originates from a restricted region, the interganglionic sulcus, at
more caudal levels. It is plausible that in order to follow the migration that
originates in the MGE and LGE, this region was not included in other studies.
Therefore, we hypothesize that cells originating from different rostrocaudal
levels can have different responses to the same environment by expressing
position-dependent receptors. Accordingly, COUP-TFs are not expressed in
ventrally migrating cells at more rostral levels, where the two GEs are well
separated (data not shown). Thus, the POa and hypothalamus can have different
roles, repulsion versus attraction, according to the type of cells they
encounter.
A novel role for COUP-TFs in neuronal migration in the developing forebrain
COUP-TFs are orphan nuclear receptors of the steroid/thyroid superfamily
shown to be involved in neurogenesis, axogenesis and neural differentiation
(Park et al., 2003). In the
cortex, COUP-TFI is mainly known for its role in regionalization and in
guidance of thalamocortical projections
(Zhou et al., 1999
;
Zhou et al., 2001
), whereas
COUP-TFII is a fundamental player in angiogenesis and heart development
(Pereira et al., 1999
). In
this report, we have provided the first insights into the functional roles of
COUP-TFI and COUP-TFII in neuronal migration in vivo. In a previous report, it
was shown that COUP-TFI could regulate cell adhesion mechanisms required for
the differentiation of embryonal carcinoma cells
(Adam et al., 2000
). Because of
the substrates on which cells were plated, it was suggested that COUP-TFI
could modify the synthesis of ECM molecules, making cells autonomous for
migration and spreading. Our expression data in vivo and our functional data
in organotypic cultures support these results in a context in which cell
migration assumes a fundamental role in achieving neuronal diversity. By using
these different approaches, we have first shown expression of COUP-TFs in
highly motile neurons, such as GABAergic and reelin-positive cells
(Fig. 2); we have then
confirmed the co-localization of COUP-TFI in migrating neurons in a series of
grafting experiments (Figs 3,
4,
5); and finally, we have
directly demonstrated a role of COUP-TFs in modulating cell migration in a
gain-of-function approach (Figs
6,
7). Our data also demonstrate
that COUP-TFs can control directional migration. Indeed, cells expressing
higher levels of COUP-TFs (and thus GFP) not only tend to spread and lose
their aspect of aggregates, but also follow specific migratory pathways
(dorsal and/or ventral) that are intrinsic to cells expressing COUP-TFs
(Fig. 6,
Fig. 7D).
Therefore, we hypothesize a dual role for COUP-TFs. First, they should regulate short-range cues, such as ECM and/or adhesive molecules, and in this way modulate the neighbouring environment. Changes in a permissive environment would allow random dispersion of migratory cells. Indeed, in the absence of COUP-TFI, GABAergic cells do migrate into the cortex, although in a less organised fashion than in the normal situation (M.S., unpublished). Therefore, we favour the hypothesis that COUP-TFI is involved in modulating cell migration, more than inducing cells to initiate migration.
Second, we propose that COUP-TFs control diffusible guidance molecules,
and/or their receptors, involved in cell migration. Indeed, ectopic expression
of COUP-TFI led to the correct directional migration of the targeted cells,
i.e. dorsal into the cortex and ventral into the POa
(Fig. 6D), suggesting that
cells over- or mis-expressing COUP-TFI were able to respond to
COUP-TFI-dependent guidance cues. More striking is the behaviour of
MGE-migrating cells after mis-expression of COUP-TFII. In this case, neurons
that were committed to migrate into the marginal and intermediate layers of
the neocortex (see control in Fig.
7C) migrated at higher rates solely into the intermediate layer,
avoiding specifically the marginal layer
(Fig. 7D), suggesting that
COUP-TFII regulates guidance cues required for migration into the intermediate
zone of the neocortex. This behaviour is in accordance with the COUP-TFII
expression pattern and the grafting experiments described in this study.
Indeed, COUP-TFII-positive cells in the marginal zone are Cajal-Retzius cells,
as seen by the co-expression with reelin, and it is now well established that
Cajal-Retzius cells originate exclusively from the pallium
(Hevner et al., 2003;
Meyer et al., 1999
;
Takiguchi-Hayashi et al.,
2004
).
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Conclusions |
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ACKNOWLEDGMENTS |
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Footnotes |
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