1 MRC Centre for Developmental Neurobiology, Kings College London, New Hunts
House, Guy's Hospital, London SE1 1UL, UK
2 University of Utah School of Medicine, Department of Neurobiology and Anatomy,
and Children's Health Research Center, Room 401 MREB, 20 North 1900 East, Salt
Lake City, UT 84132-3401 USA
* Author for correspondence (e-mail: susan.chapman{at}kcl.ac.uk)
Accepted 8 July 2003
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SUMMARY |
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Key words: Blastula, Expression, Forebrain, Gastrula, Head, Induction, Organiser, Markers, Patterning, Specification, Trunk/tail, Visceral endoderm
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Introduction |
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In chick, the process of neural induction begins before the onset of
gastrulation, with competence being conferred by FGF signals emanating from
the posterior of the embryo (Muhr et al.,
1999; Streit et al.,
2000
; Wilson et al.,
2001
; Wilson and Edlund,
2001
; Wilson et al.,
2000
). The cellular interactions leading to the specification of
competent tissue as neural, and the timing over which they occur, remain
unclear. Although transplants of posterior epiblast can induce transient
expression of pre-neural markers such as Sox3 in epiblast, stable
expression of Sox2 in specified neuroectoderm requires both central
and posterior epiblast cells to come together at mid-streak stages (3+ or
3c/d), forming a functional organiser
(Streit et al., 2000
). Further
support for the timing of neural specification at mid-streak stages comes from
explant studies in which competent tissue at stage 3d, but not 3c, cultured in
isolation, was able to self differentiate, developing the columnar
neuroepithelial morphology of specified neuroectoderm, as well as having
stable expression of Sox2 (Darnell
et al., 1999
).
The relative spatiotemporal positions of early embryonic tissues
(Fig. 1) suggest that several
tissues could function potentially in anteroposterior patterning. Candidate
tissues able to produce `organising' signals include a population of central
epiblast (CE) cells (Darnell et al.,
1999; Garcia-Martinez et al.,
1993
; Hatada and Stern,
1994
; Healy et al.,
2001
; Lawson and Schoenwolf,
2001a
; Lawson and Schoenwolf,
2001b
; Schoenwolf et al.,
1989b
; Streit et al.,
2000
), and the underlying lower layer, the hypoblast and
ingressing anterior definitive endoderm (ADE). The CE population is a group of
epiblast cells rostral to the tip of the primitive streak between stages 2 and
4. They are in a position equivalent to that of the mouse early gastrula
organiser (EGO), which has been shown to have a role in head patterning when
combined with epiblast and anterior visceral endoderm (AVE)
(Tam and Steiner, 1999
). As
the primitive streak extends forward, the CE population becomes incorporated
into the streak (Garcia-Martinez et al.,
1993
; Garcia-Martinez and
Schoenwolf, 1993
; Joubin and
Stern, 1999
; Lawson and
Schoenwolf, 2001a
; Lawson and
Schoenwolf, 2001b
; Schoenwolf
and Alvarez, 1989
; Schoenwolf
et al., 1989a
; Schoenwolf et
al., 1989b
; Schoenwolf et al.,
1992
; Smith and Schoenwolf,
1991
). Early fate-mapping studies used quail/chick chimaeras and
fluorescent dye injections to determine the fate of cells in the rostral
streak (Garcia-Martinez et al.,
1993
; Garcia-Martinez and
Schoenwolf, 1993
; Schoenwolf
et al., 1992
; Selleck and
Stern, 1991
). Homotopic and isochronic cell grafts from stage 3a/b
rostral streak contributed extensively to head mesenchyme and foregut
endoderm, whereas a small proportion was also detected in notochord and the
median hinge-point cells (i.e. the future floor plate of the neural tube).
Stages 3c-4 rostral streak cells contributed mainly to notochord and median
hinge-point cells, although a small number were traced to the head mesenchyme
and foregut endoderm.
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Owing to contradictory results and gaps in our understanding regarding the
role of CE, the hypoblast and ADE, we have tested these tissues for a role in
establishing anterior positional identity. Previous chick transplant studies
have failed overall to show a role for lower layer tissues in determining cell
fate (Foley et al., 2000).
Removing the lower layer has also met with little previous success, mostly
because of the embryos' ability to recover and replace ablated tissues, such
as the hypoblast at early stages
(Vanroelen et al., 1982
), or
to tissue being removed later than the time in question
(Withington et al., 2001
). We
used the transection assay (Fig.
2) (Darnell et al.,
1999
; Healy et al.,
2001
; Schoenwolf et al.,
1989b
; Yuan et al.,
1995a
) to address what the role for these lower layer tissues is,
and determined that anterior positional identity seems to be separable from
neural specification. Isolating rostral epiblast (prospective anterior neural
plate) from the influences of Hensen's node and ingressing axial mesoderm was
crucial, because ingressing axial mesoderm from stage 4+ has a role in the
induction of Ganf, the earliest specific maker of anterior neural
plate (Knoetgen et al., 1999
).
The expression patterns of Sox2, the most definitive early neural
specification marker identified to date
(Rex et al., 1997
;
Streit et al., 2000
;
Streit et al., 1997
;
Uchikawa et al., 2003
), and
Ganf were re-examined and used to define anterior and neural
identity. We show that anterior positional identity is established and
maintained in the epiblast by the hypoblast at stage 3a/b and ADE at stages 3d
and 4, apparently separately from neural specification, and we propose a
revised model for establishing anteroposterior polarity, neural specification
and head patterning, based on this new evidence.
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Materials and methods |
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In situ hybridisation
In situ hybridisation was performed as described previously
(Chapman et al., 2002). Embryos
were then cleared in 80% glycerol/PBS, embedded in 20% gelatin, fixed with 4%
PFA and sectioned using a Leica vibratome at 40-50 µm. Embryos were imaged
with a SPOT, Coolsnap or Zeiss Axiocam digital camera. The following markers
were used: Sox2, specified neuroectoderm (R. Lovell-Badge):
Wnt8c, ingressing mesodermal cells (J. Dodd): Ganf, earliest
marker of anterior neuroectoderm (A. Zaraisky); Fgf8, primitive
streak (G. Martin); Chordin, primitive streak, Hensen's node and
ingressing axial mesoderm (A. Graham); Crescent, hypoblast and ADE
(P. Pfeffer).
Embryo culture and transection
Transection of embryos was performed as described by Darnell et al.
(Darnell et al., 1999). In
experiment 1, embryos were transected to determine the effect of separating
rostral tissues from the primitive streak, prospective node and ingressing
mesoderm. Embryos were transected at the rostralmost level of the streak (Type
B), or 125 µm rostral to the streak (Type C), at stages 3a-4+ and cultured
on an agar/albumen substrate with no added culture media for 24 hours
(Fig. 2). The blastoderm
isolates were then processed for Ganf and Sox2 transcripts
(Table 1). In experiment 2, the
lower layer of rostral isolates was removed to determine whether this layer
has a role in patterning the rostral epiblast. Isolates were cultured in
collagen: 3.3 mg/ml rat tail collagen (Roche) was prepared in 0.2% acetic
acid. 480 µl collagen, 36 µl DEPC-H2O, 60 µl 10x
DMEM and 20 µl 0.75% bicarbonate solution were added together on ice.
Rostral and caudal isolates of each transected embryo were embedded, and after
30 minutes at 37°C in a 5% CO2 incubator, carbonated Neurobasal
medium supplemented with Glutamax was added. Embryos were transected (Type B)
in saline (123 mM), followed by removal of the lower layer using tungsten
needles (0.125 mm tungsten wire, WPI). No enzymatic treatments were used. RBIs
with an intact lower layer served as controls
(Table 2). To test for mesoderm
in the RBIs, in experiment 3, transected embryos were fixed immediately and
then processed for Wnt8c expression. Experiments 4 and 5 were
designed to test sufficiency of the lower layer to induce Ganf:
either rostral (experiment 4) or caudal (experiment 5) lower layer was
recombined with rostral epiblast in collagen culture for 24 hours and then
processed for Ganf transcripts.
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Results |
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The lower (ventral) layer is formed by polyingression of cells from the
overlying epiblast at stage X/XI, forming islands of cells in the subgerminal
cavity (Fig. 1)
(Harrison et al., 1991;
Lawson and Schoenwolf, 2001a
).
Together with cells moving rostrally from Koller's sickle and the posterior
marginal zone (PMZ), a complete lower layer is formed, called the primary
hypoblast (Callebaut et al.,
1999
; Stern and Canning,
1990
; Vakaet,
1970
). The endoblast (secondary hypoblast) forms at stage
XIII/XIV, with cells moving rostrally from Koller's sickle and the PMZ.
Primary and secondary hypoblast form a continuous sheet of cells under the
epiblast by stage XIV/2 - the primitive endoderm. The primitive streak forms
at stage 2, as a triangularly shaped structure that elongates rostrally.
Definitive endoderm begins ingression through the rostral end of the primitive
streak from stage 3a to stage 4/4+, by which time the lower layer has fully
displaced the hypoblast sheet rostral to the embryo, forming the germ cell
crescent (Lawson and Schoenwolf,
2003
). At stages 3a/b the rostral streak gives rise to the ADE,
including the midline prechordal plate endoderm (PCPE) that lies beneath the
forebrain. During subsequent development, the prechordal plate endoderm buds
off proliferative mesoderm and together with ingressing mesoderm, forms a
middle layer, the prechordal plate mesoderm, which contributes to the head
mesenchyme (Seifert et al.,
1993
). Axial mesoderm ingresses through the rostral streak from
stage 4+ (the head process), and consists of a mixed cell population of
prechordal plate mesoderm and rostral notochord, which intercalates between
the neuroectoderm and ADE (Foley et al.,
1997
; Vesque et al.,
2000
). The molecular basis for the spatial separation of these two
populations is unclear, although SEM studies of the morphological movements
have been described (England,
1984
; England and Wakely,
1977
; England et al.,
1978
; Wakely and England,
1979
). The laying down of more caudal notochord occurs as Hensen's
node and the definitive streak regress caudally. Intercalation of the
fan-shaped prechordal plate mesoderm results in the prechordal plate mesoderm
coming to partially overlie the PCPE.
Sox2 is a pan-neural marker expressed from the onset of
neural specification
Sox2 is the earliest pan-neural marker stably expressed in the
specified neuroectoderm (Rex et al.,
1997; Streit et al.,
2000
; Streit et al.,
1997
). Embryos were tested for expression of Sox2 from
stage XI/XII (not shown), with expression first detected at stage 3d, as
expected (Fig. 3A). Expression
began just rostral and lateral to Hensen's node and later expanded rostrally
and laterally toward the outer boundary of the neural plate, away from the
streak (stages 4/4+) (Fig. 3B).
This pattern suggests that neural specification occurs in a spatiotemporal
manner across the prospective neuroectoderm. The caudal boundary of expression
remained constant, suggesting that the first cells to express Sox2
are not the anteriormost neuroectoderm, but rather are the more caudal neural
plate. By stage 5, Sox2 was expressed throughout the neural plate,
which is still flat prior to formation of the head fold and neural tube
(Fig. 3C). Concomitant with
node regression, the caudal boundary of Sox2 expression extended
caudally through convergent extension (Fig.
3D). The ventral neural plate was lighter in colour as the neural
tube formed, while the neural plate narrowed as the neural folds rose up and
moved medially, with varying levels of expression within the rostrocaudal
length of the neural plate, with stronger expression of Sox2 in the
rostralmost neural plate. In summary, Sox2 is detected from stage 3d
onwards and is the earliest available stable marker of specified
neuroectoderm.
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At stage 3c, the number of RBIs with Ganf transcripts is similar
to that of intact embryos, 5/19, compared with 4/15 isolates lacking the lower
layer. The lack of neural specification in these RBIs is due to the exclusion
of CE cells and results in low numbers of RBIs expressing Ganf. Lower
layer removal, now composed of hypoblast and ADE, has no effect on the numbers
of RBIs expressing Ganf, indicating that the inducing activity of the
lower layer may be no longer required. Interestingly, the ADE expresses only
Crescent, Cerberus, Hex and Otx2 at stage 3c, whereas at
stage 3d, Lim1 and Hnf3ß are also induced
(Chapman et al., 2002). This
may indicate that at stage 3c the ADE cannot perform a maintenance role, but
by stage 3d has developed sufficiently to do so. At stage 3d, removal of
hypoblast and ADE again causes a reduction in the numbers of embryos
expressing Ganf, 3/15 (20%) compared with 7/12 intact RBIs. This is
indicative of a maintenance function being lost. At stage 4 this effect is
even more pronounced with 0/8 isolates (7/12 intact RBIs) positive for
Ganf transcripts, suggesting that although the lower layer is
responsible for initial induction and maintenance of anterior identity in
epiblast, factors from other tissues may be required to maintain and even
stabilise the expression. Tissue candidates for this role include Hensen's
node and ingressing axial mesoderm, which have been identified previously as
important in Ganf expression
(Knoetgen et al., 1999
). In
summary, removal of the lower layer in RBIs demonstrates that vertical
signalling by the lower layer is required for the expression of the anterior
neuroectoderm marker Ganf, apparently separately from and before
neural specification, and that following neural specification the lower layer
has a maintenance role, without the involvement of mesoderm.
Mesodermal cells are not detected in RBIs
Patterning of the rostral ectoderm in intact isolates could be due to the
presence of mesodermal cells that are inadvertently included in the RBIs when
transecting (experiment 3). When the lower layer is removed in these isolates,
any mesodermal cells present could conceivably also be stripped away,
resulting in loss of Ganf expression. To test this we, transected
embryos from stages 3a/b through to stage 4 and tested for Wnt8c
expression, which marks ingressing mesoderm
(Fig. 8). Isolates were fixed
immediately after transection, and in no case were Wnt8c transcripts
detected by in situ hybridisation in the RBIs (n=29; stage 3a/b,
n=12; stage 3c, n=7; stage 3d, n=7; stage 4,
n=3). The caudal blastoderm isolates from these transections acted as
controls for the presence of Wnt8c and were positive for mesodermal
cells in all cases.
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Discussion |
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After transection at stage 3a/b, the epiblast still neuralises, as
indicated by the expression of the definitive pan-neural marker Sox2
(Rex et al., 1997). Neural
specification in RBIs depends on the presence of a population of central
epiblast (CE) cells with `organising' ability, acting either as an organiser
or inducer of an organiser (Darnell et al.,
1999
). After removal of Hensen's node in whole embryos and tissue
isolates, the organiser reconstitutes
(Joubin and Stern, 2001
;
Psychoyos and Stern, 1996
;
Yuan et al., 1995a
;
Yuan et al., 1995b
;
Yuan and Schoenwolf, 1998
;
Yuan and Schoenwolf, 1999
). We
have not determined whether the same mechanism operates in the rostral
blastoderm isolates, although markers of notochord (Not1), node
(Shh) and primitive streak (Brachyury/T) were detected in
RBIs, suggesting that the organiser is reconstituted
(Darnell et al., 1999
).
Therefore, tissue identified as able to specify neural identity in RBIs was
present at stage 3a/b and reduced at stage 3c as the primitive streak extended
rostrally, incorporating the CE cells
(Darnell et al., 1999
;
Lawson and Schoenwolf, 2001a
;
Lawson and Schoenwolf, 2001b
),
although long-range neural specification signalling, prior to transection,
cannot be ruled out entirely. When lower layer, composed only of hypoblast,
was included in the RBI, Ganf was expressed at the same frequency as
Sox2. By contrast, removing lower layer from these RBIs resulted in
the loss of Ganf expression, but did not affect neural specification.
Ganf was not transiently induced, suggesting that lower layer signals
are required to establish positional identity in the overlying epiblast before
neural specification at stage 3d.
Hypoblast seems to be required for only a brief period, because in stage 3c
transections, removal of the hypoblast does not abolish Ganf
expression. Only a small proportion of RBIs undergo neural specification at
this stage, as CE cells are excluded from transected RBIs. By contrast,
concomitant with neural specification at stage 3d, transection does not affect
the neural character of RBIs, whereas removal of lower layer still leads to a
reduction in the percentage of RBIs with Ganf expression, similar to
that for stage 3a/b. Hypoblast has been displaced rostrally by the ADE
(including midline prechordal plate endoderm) now underling the region where
Ganf is induced. The ADE may perform a maintenance role from stage 3d
when expression of Lim1 and Hnf3ß is induced, in
addition to Crescent, Cerberus, Hex and Otx2
(Chapman et al., 2002). Further
work will be needed to determine whether the ADE is directly involved in the
induction of Ganf, or whether ADE maintains anterior character
specified earlier by the inductive interaction with the hypoblast.
Reassessing current models of early chick development
There is an ongoing debate as to which lower layer tissue in the chick is
equivalent to the mammalian AVE, and whether the hypoblast and ADE have any
patterning role. In mouse, adjoining the rostral boundary of the primitive
streak the early gastrula organiser (EGO), together with epiblast and AVE, is
required for head formation
(Martinez-Barbera and Beddington,
2001). Chick CE cells are in a position equivalent to the EGO and
have `head organiser' properties (i.e. the ability to induce neural identity)
(Darnell et al., 1999
;
Garcia-Martinez et al., 1993
;
Healy et al., 2001
;
Schoenwolf et al., 1989b
).
Determining whether CE cells can be considered a true head organiser still
requires that roles in neuralising naïve epiblast and re-patterning more
caudal areas of the neural plate be demonstrated. At stage 2 and 3a/b, the CE
population is rostral to the extending streak, but by stage 3c it becomes
incorporated into the rostrally extending streak forming Hensen's node
(Schoenwolf et al., 1989b
).
The node acts like a head organiser, establishing and refining neural
identity, and maintaining and embellishing patterning in overlying
neuroectoderm. The properties of axial mesoderm as it ingresses through
Hensen's node at stage 4+ are reported to be the result of its origin in the
node and vertical signals from the definitive endoderm as it intercalates
between the upper and lower germ layers
(Vesque et al., 2000
). An
anteriorising signalling centre in the lower layer could act as the source of
signals that operate to further pattern the extending axial mesoderm,
indicating a relay mechanism operates, where the anterior endoderm patterns,
directly or indirectly, the prechordal plate mesoderm, which in turn patterns
the overlying neuroectoderm (Dale et al.,
1997
; Foley et al.,
1997
; Pera and Kessel,
1997
). Our results suggest that hypoblast and ADE also have an
earlier role in directly patterning the overlying epiblast.
With ingression of axial mesoderm through Hensen's node, head organiser ability is lost, perhaps allowing remaining cells to perform the role of trunk/tail organiser, refining the patterning of more caudal parts of the neural plate. An important related issue is whether neural identity is a neutral fate, with lower layer providing positional identity. In our experiments, removal of the lower layer does not affect neural specification, because RBIs still express the definitive pan-neural marker Sox2. The significance of the Sox2 expression pattern, which expands progressively from medial tissue adjacent to Hensen's node and then laterally across the neuroectoderm, suggests that neural specification does not occur first in the most anteriorly positioned cells of the prospective neural plate. However, Ganf expression is lost when the lower layer is removed. Therefore, these data together support a model in which loss of anterior identity does not affect the neural character of tissue, suggesting that neural identity itself is neutral with respect to position.
The lower layer signals vertically to the overlying epiblast
Transplanted chick lower layer was unable to induce anterior
neuroectodermal (ANE) markers in epiblast, whereas rabbit AVE and chick axial
mesoderm induced Ganf (Knoetgen
et al., 1999). A heterochronic shift in patterning of the ANE was
proposed, with chick prechordal mesoderm taking over the role played by mouse
AVE. Why did the transplanted chick tissue not induce expression of
Ganf? The signals needed to induce positional identity were either no
longer present (transplanted hypoblast was older than stage 3a/b), i.e.
necessary signals could have been reduced by enzymatic treatments used to
facilitate isolation of the lower layer, or the responding tissue was not
neuralised and, therefore, not competent to express Ganf. Our data
demonstrate that intact hypoblast at stage 3a/b is required for the
neuroectoderm to express Ganf. Extirpation of hypoblast at stage 3
did not lead to loss of Ganf expression at later stages; however,
stage 3 is highly dynamic and prospective ANE was not separated from the
influence of the node or ingressing axial mesoderm, both of which are
sufficient to induce the expression of Ganf
(Knoetgen et al., 1999
).
Transections demonstrate that in RBIs the lack of a node does not affect
induction of Ganf, whilst axial mesoderm begins ingressing only after
Ganf expression has begun and, therefore, is unlikely to be the
initial endogenous inducer. Thus, chick axial mesoderm is probably not the
homologue of the mouse AVE and a heterochronic shift is unlikely. The later
patterning role of axial mesoderm is important in refining regional
neuroectoderm identity (Dale et al.,
1997
; Foley et al.,
1997
; Pera and Kessel,
1997
), but initial anterior positional identity must be assigned
to earlier endodermal tissues.
The modified Nieuwkoop model
An alternative hypothesis, a modified Nieuwkoop model, proposes that AVE
and hypoblast at stage XII/XIII are equivalent tissues. However, the lower
layer in this model is responsible for cell movements, rather than cell fate,
directing cells away from the caudalising influence of Hensen's node
(Foley et al., 2000).
Transplanted hypoblast induced transient expression of Sox3 and
Otx2 in epiblast, indicating signalling capability, but as expression
was not maintained the authors suggested that anteriorising the epiblast is
not the hypoblast's main role. Our data do not support the interpretation of
the proposed early pre-forebrain state, defined by the expression of the
pre-neural markers Sox3 and chick ERNI
(Streit et al., 2000
). ERNI
has been shown to be a retrotransposon only present in the Galliform genome,
requiring clarification of its biological significance
(Acloque et al., 2001
), and
Sox3 is expressed in a mosaic of epiblast cells from prestreak stages
across the entire area pellucida, only becoming restricted to the
neuroectoderm after stage 3d (Rex et al.,
1997
). Rather, in our model successive inductive interactions
anteriorises epiblast, with molecular signals establishing and maintaining
anterior identity separately from neural specification. An explanation for the
failure to maintain the initial Sox3 and Otx2 expression is
that hypoblast is unable to either stabilise or maintain this expression,
requiring later ADE to provide the necessary signals. More importantly, this
early induction suggests that, as in the mouse, the ability to pattern the
early embryo is not confined to Hensen's node and its derivatives.
A revised hypothesis for rostral patterning and head induction
We suggest a revised hypothesis, where successive inductive interactions
between hypoblast/ADE and epiblast act to promote anterior character
(Fig. 10). As hypoblast is
displaced rostrally by the ADE, signals from ADE stabilise/maintain this
rostral identity in the overlying epiblast/neuroectoderm. Rostrally located
hypoblast (stages XII-XIV) is remarkably similar to the mouse AVE, expressing
Lim1, Hnf3b, Otx2, Gsc, Cerberus, Hex and Crescent
(Chapman et al., 2002). Genes
expressed in ADE include Crescent, Cerberus, Hex and Otx2,
whereas Lim1 and Hnf3b are detected only after stage 3d
(Chapman et al., 2002
).
Ganf is the earliest marker detected in the rostral epiblast in
response to anteriorising signals from the lower layer and neural
specification by the head organiser. Head organiser cells leave Hensen's node,
as ingressing axial mesoderm, permitting the remaining population to perform
the role of trunk/tail organiser. Changing gene expression reflecting this
include Otx2, Nodal and Dkk1, which are lost from the streak
at stages 5+/6, while Bmp7 is now expressed in rostral streak from
which it was previously excluded (Chapman
et al., 2002
). This novel hypothesis allows for separate
signalling pathways to pattern anterior and neural identity, and for the
hypoblast to direct cells with a rostral fate away from the caudalising
influence of the trunk/tail organiser
(Foley et al., 2000
). It
further takes into account results suggesting that definitive endoderm is
required for patterning neural plate, as stage 4+ removal results in loss of
the forebrain because of lack of vertical signals to ingressing head process,
and also direct maintenance signals to the overlying neuroectoderm
(Withington et al., 2001
).
Loss of these stabilising and maintenance signals results in the loss of
forebrain identity. This hypothesis is further supported by the Foxa2
conditional mouse mutant, where loss of Foxa2 results in axial
mesoderm losing its identity; anterior neuroectoderm in turn is not
stabilised, resulting in forebrain truncation
(Hallonet et al., 2002
).
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ACKNOWLEDGMENTS |
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