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First published online 3 July 2006
doi: 10.1242/dev.02464
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Institute of Anatomy and Cell Biology, Department of Molecular Embryology, University of Freiburg, Albertstrasse 17, D-79104 Freiburg, Germany.
* Author for correspondence (e-mail: bodo.christ{at}anat.uni-freiburg.de)
Accepted 30 May 2006
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SUMMARY |
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 TOP SUMMARY INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key words: Chick embryo, Somite, Neural tube, Dermomyotome, Wnt6, Wnt11
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INTRODUCTION |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). The dorsal part of the somite remains epithelial and
becomes the dermomyotome, which gives rise to dermis and muscle. In the course
of dermomyotomal differentiation, the dorsomedial and ventrolateral lips of
the dermomyotome (DML and VLL, respectively) remain epithelial growth zones
(Ordahl et al., 2001), whereas
the central dermomyotome (CD) de-epithelializes to give rise to the dorsal
dermis and subcutis as well as muscle
(Gros et al., 2005;
Relaix et al., 2005;
Ben-Yair and Kalcheim, 2005)
(reviewed by Scaal and Christ,
2004).
Signals from adjacent tissues play important roles in the patterning of
somites along the dorsoventral and mediolateral axes. Commitment of cells in
somites occurs after somite formation in response to external cues
(Aoyama and Asamoto, 1988;
Ordahl and Le Douarin, 1992;
Christ et al., 1992). Several
lines of evidence indicate that Shh secreted from the notochord and floor
plate acts as a ventralizing and medializing signal
(Fan and Tessier-Lavigne,
1994; Johnson et al.,
1994; Chiang et al.,
1996; Kos et al.,
1998). By contrast, signals from the surface ectoderm and the
dorsal neural tube induce the formation and/or maintenance of the dermomyotome
(Brand-Saberi et al., 1993;
Pourquié et al., 1993;
Kuratani et al., 1994;
Fan and Tessier-Lavigne, 1994;
Spence et al., 1996) (reviewed
by Scaal and Christ,
2004).
The Wnt family of secreted proteins play many roles during vertebrate
development, including cell fate choice, proliferation and survival
(Dickinson and McMahon, 1992;
Parr and McMahon, 1994;
Cadigan and Nusse, 1997;
Huelsken and Birchmeier,
2001). In somite development, Wnt1 and Wnt3a have been shown to be
required for the development of the medial and dorsal regions of the somites,
as well as to induce myogenesis (Marcelle
et al., 1997; Ikeya and
Takada, 1998; Wagner et al.,
2000). Moreover, the epithelial structure of the newly formed
somite, as well as that of the dermomyotome, are influenced by Wnts, which
have been suggested to induce an epithelial morphology via ß-catenin
(Hinck et al., 1994;
Gumbiner, 1996;
Linker et al., 2005).
A member of this family, Wnt6, has been cloned in different
species, including human, mouse, Drosophila, Xenopus, Amphioxus and
chick, and its expression pattern has been described
(Cauthen et al., 2001;
Janson et al., 2001;
Schubert et al., 2001;
Itaranta et al., 2002;
Schubert et al., 2002;
Rodriguez-Niedenführ et al.,
2003; Loganathan et al.,
2005). In avian embryos, at the level of the segmental plate and
the epithelial somite, Wnt6 is expressed in the entire ectoderm
overlying the neural tube, the paraxial mesoderm and the LPM. Following somite
compartmentalization, which leads to the formation of the dermomyotome and the
sclerotome, Wnt6 expression ceases in the medial aspect and becomes
restricted to the lateral ectoderm overlying the LPM.
Wnt11 is a member of the non-canonical type of Wnt signaling. Recently, it
has been shown to also participate in the canonical Wnt pathway
(Tao et al., 2005). In chick,
it is expressed in the dorsomedial lip (DML) of matured somites
(Marcelle et al., 1997),
whereas in zebrafish, Wnt11 is known to be involved in
convergence-extension-movements during gastrulation
(Heisenberg et al., 2000). The
function of Wnt11 in the avian dermomyotome remains unknown.
In this study we examined the regulation of the dynamic pattern of Wnt6 expression in the avian embryonic ectoderm. We show that Wnt6 expression in the surface ectoderm becomes downregulated by Wnt1 and Wnt3a signaling from the neural tube. We present evidence that this inhibiting action of the neural tube is mediated by Wnt11 in the DML, thus providing evidence of a patterning influence of neural tube and paraxial mesoderm on the surface ectoderm. Our results suggest that after the lateralization of Wnt6, Wnt11 takes over the function of Wnt6 to maintain the epithelial state of the medial region of the dermomyotome. We present a model suggesting that Wnt11 in the DML, and Wnt6 in the VLL, maintain the epithelial character of the dermomyotomal margins to enable ongoing growth of the dermomyotomal sheet during epaxial and hypaxial myogenesis.
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MATERIALS AND METHODS |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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).
Separation of somites from axial organs
A longitudinal slit was made between neural tube and adjacent somites
[between somites 12-17 (somite stages V-XI), i.e. corresponding to a length of
4-6 somites] on one side of HH stage 14 chick embryos. An aluminium foil
barrier was inserted into the slit and the embryo reincubated from 12 to 18
hours and then processed for in situ hybridization.
Removal of neural tube
Portions of unilateral halves or the whole neural tube of HH stage 12-14
chick embryos were removed at the level of epithelial somites (I-IV) just
prior to their maturation as previously described
(Christ et al., 1992). Embryos
were reincubated from 12 to 18 hours, and then processed for in situ
hybridization.
Removal of dermomyotome
Whole dermomyotomes or medial dermomyotomes (of somites 10-12, at somite
stages V-X) of HH stage 12-13 chick embryos were removed at the level of
matured somites. Embryos were reincubated from 12 to 18 hours and then
processed for in situ hybridization.
Grafting of medial dermomyotomal lip
Medial lips of dermomyotomes from HH stage 13-14 chick or quail embryos
were grafted to the segmental plate of chick embryos of HH stage 11-12.
Embryos were reincubated for 8-10 hours, fixed and processed for in situ
hybridization and immunohistochemistry.
Cell injection
Wnt3a- and Wnt1-expressing cells were a gift from Andreas Kispert
(Medizinische Hochschule Hannover, Germany). CHO B3 cells expressing Noggin
protein and DHFR control CHO cells were kindly provided by Richard Harland
(University of California at Berkeley). Cell lines were cultured as described
elsewhere (Lamb et al., 1993).
Confluent cultures were harvested, cells were washed in phosphate-buffered
saline (PBS), pelleted and resuspended in a minimal volume of medium. For cell
injection, the ectoderm (at the level of somite I-V of HH stage 13-14 embryos)
was punctured with a tungsten needle. With the help of a blunt glass needle, a
tunnel was made below the ectoderm and concentrated cell suspensions were
locally applied with a micropipette along the length of the tunnel. For some
embryos, noggin-expressing cells were injected into the neural tube at the
level of the epithelial somites. Embryos were reincubated from 12 to 18 hours,
processed for whole-mount in situ hybridization. Control cells showed no
effect on target genes expression (not shown).
Electroporation of Wnt11 and dnWnt11 RCAS
Wnt11 and dnWnt11 RCAS constructs were kindly provided by Philippa
Francis-West (Kings College, London)
(Anakwe et al., 2003). The
electroporation procedures and equipment were used as described by Scaal et
al. (Scaal et al., 2004).
Electroporation was performed at the level of epithelial somites (I-IV) of HH
stage 12-15 chick embryos. Constructs were co-electroporated with GFP
plasmids, the latter electroporated alone were used as a control. Embryos were
reincubated from 12 to 16 hours, photographed using a fluorescence microscope
to visualize the localization of the plasmid, and then processed for
whole-mount in situ hybridization.
In situ hybridization
Embryos were fixed overnight at 4°C in 4% PFA. The embryos were washed
in PBT, dehydrated in methanol and stored at 4°C. Whole-mount in situ
hybridization was performed as described by Nieto et al.
(Nieto et al., 1996). Selected
stained embryos were embedded in 4% agar and sectioned with a vibratome at 50
µm.
The following probes were used in this study: chick Wnt11 (1000
bp; Christophe Marcelle, Marseille); Pax1 (1.5 kb insert cloned into
pBlusescript II KS; Cecilia Ebensperger, Freiburg); Pax3 (a 1543 bp
insert cloned in to pGEM 72f; Marianne Bronner-Fraser, Pasadena); full-length
Paraxis clone was a gift from Prof. Eric Olson (Dallas). For chick
Wnt6, we used the cloned Wnt6 1500 bp fragment
(Rodriguez-Niedenführ et al.,
2003), as a template. Sense and antisense riboprobes were labeled
with digoxigenin RNA labeling kit as recommended (Boehringer, Mannheim,
Germany).
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|
RESULTS |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) and indicates that ectodermal Wnt6 is dispensable during the
development of the medial somite.
We examined if the loss of Wnt6 expression in the medial ectoderm
is due to an inhibitory action of the axial organs. Axial organs are known to
be involved in patterning the medial somite, but so far no patterning
influence on the ectoderm has been described
(Christ et al., 1992;
Dietrich et al., 1997;
Marcelle et al., 1997;
Münsterberg and Lassar,
1995; Stern and Hauschka,
1995; Stern et al.,
1997; Pourquié et al.,
1995; Pourquié et al.,
1996). To determine the role of axial organs in the regulation of
Wnt6 expression, we separated four to six matured somites and the
ectoderm overlying the somites from the neural tube by insertion of an
aluminium foil barrier at HH stage 14. After a reincubation period of 12 to 18
hours, we observed an overexpression of Wnt6 at the level of the
barrier, with the expression domain extending into the medial ectoderm
(Fig. 2A,D; n=8). In a
different approach, we microsurgically removed the respective half of neural
tube at the same location. Loss of the neural tube also results in a
lateromedial expansion of Wnt6 expression
(Fig. 2B,E; n=6). This
suggests that the lack of Wnt6 expression in the ectoderm covering
the medial region of the matured somites is due to inhibitory signals from the
neural tube.
In order to identify the signals from the neural tube which inhibit
Wnt6 expression, we examined the influence of Wnt1 and Wnt3a on
Wnt6 expression. Wnt1 and Wnt3a are expressed in the dorsal neural
tube and have been shown to be regulators of medial somite patterning
(Münsterberg et al.,
1995; Marcelle et al.,
1997). After injection of Wnt1- or
Wnt3a-expressing cells into the subectodermal space dorsal to the
somites, Wnt6 expression was totally inhibited at the site of
injection (Fig. 2C,F;
n=12; Wnt1; data not shown). This strongly suggests that the loss of
Wnt6 expression in the medial ectoderm overlying the maturing somites
is due to an inhibitory action of Wnt3a and/or Wnt1 from the dorsal neural
tube.
Wnt11 in the DML is a transducer of Wnt signals from the neural tube to the ectoderm
We have shown that Wnt1 and Wnt3a are able to inhibit Wnt6
expression in the medial surface ectoderm. However, Wnt1 and
Wnt3a both are expressed in the dorsal neural tube already during
early stages of paraxial mesoderm development when Wnt6 is still
expressed in the entire surface ectoderm, including the medial aspect close to
the neural tube (Hirsinger et al.,
1997; Marcelle et al.,
1997; Cauthen et al.,
2001). This paradox could be explained by the hypothesis that Wnt1
and Wnt3a do not have a direct effect on Wnt6 but act via an
intermediate signal that is not active before the epithelial somite has
developed into dermomyotome and sclerotome.
|
). To test if dermomyotomal signals influence
Wnt6 expression, we removed the entire dermoymotome, or medial halves
of the dermomyotome, and checked for Wnt6 expression. In both
experiments, ectodermal Wnt6 expression was upregulated at the site
of surgery, and expression extended to the medial surface ectoderm,
demonstrating that the dermomyotome exerts an inhibitory action on
Wnt6 expression (Fig.
3A-D; n=18).
Marcelle and co-workers (Marcelle et
al., 1997) have shown that the differentiation of the dorsomedial
lip of the dermomyotome (DML) depends on Wnt1 and Wnt3a signaling from the
neural tube. To test if the hypothesized intermediate signal, which inhibits
Wnt6 expression in response to Wnts from the neural tube, originates
from the DML, we transplanted DMLs from HH13 quail donor embryos to the
segmental plate of HH stage 12 chick host embryos. After 12 hours of
incubation, Wnt6 expression in the ectoderm covering the site of DML
implantation was downregulated. This shows that the DML has an inhibitory
influence on Wnt6 expression (Fig.
3F; n=7).
Wnt11 has been described as a marker gene of the DML, and is
expressed in the DML in response to Wnt1 and Wnt3a signaling from the neural
tube (Marcelle et al., 1997)
(this study see Fig. 3H,I),
making it an excellent candidate for the hypothesized intermediate
Wnt6-inhibitory signal. Indeed, we found that the DML grafts leading
to inhibition of Wnt6 in the ectoderm show robust Wnt11 expression
(Fig. 3E; n=3). We
compared the expression pattern of Wnt11 and Wnt6 during
normal development and found that the onset of dermomyotomal Wnt11
expression correlates with the downregulation of Wnt6 in the medial
ectoderm (Fig. 1). Together,
these data are suggestive of an inhibitory action of Wnt11 on Wnt6
expression.
To directly test the effect of Wnt11 on Wnt6 expression, we
electroporated Wnt11 RCAS into prospective dermomyotomal cells of the
epithelial somite as described by Scaal et
al. (Scaal et al., 2004). To facilitate localization of the
construct, we coelectroporated GFP-pCLGFPA, which has no impact on target gene
expression (Scaal et al.,
2004) (own results not shown). After a reincubation period of
12-16 hours, we observed a robust upregulation of Wnt11 expression at
the site of electroporation (Fig.
4A,B; n=5). We analyzed the electroporated embryos for
Wnt6 expression and found that dermomyotomal overexpression of
Wnt11 leads to a total loss of Wnt6 expression even in the
lateral ectoderm (Fig. 4C-E;
n=7). Conversely, we electroporated a dominantnegative Wnt11
RCAS-construct, which inhibits endogenous Wnt11 signaling, into the same
location. As expected from our previous results, inhibition of Wnt11 signaling
lead to a strong upregulation and medial extension of Wnt6 expression
in the ectoderm overlying the electroporated dermomyotome
(Fig. 4F-H; n=5).
Thus, we have shown that Wnt11 is indeed a negative regulator of Wnt6
expression, and we provide evidence that dermomyotomal Wnt11 transduces the
Wnt6-inhibitory signals from the neural tube to the ectoderm.
Wnt11 acts as a somite epithelialization factor
Having found that Wnt6 expression is restricted to the lateral
ectoderm by the inhibitory action of Wnt11 in the medial dermomyotome, we
sought to determine the functional significance of this regulatory
process.
|
; Linker et al.,
2005). However, in the matured somites, it is expressed only in
the ectoderm overlying the lateralmost margin of the epithelial dermomyotome:
the ventrolateral lip (VLL). The epithelialization factor of the medial
dermomyotome is unknown. We hypothesized that after the loss of Wnt6
expression in the medial ectoderm, Wnt11 in the DML could act as a local
epithelialization factor. To investigate this, we tested the expression of
markers of the epithelial dermomyotome, Pax3 and Paraxis,
after overexpression of Wnt11 in the somites by electroporation of a
Wnt11 RCAS construct. We found an upregulation of Pax3 and
Paraxis in the electroporated somites, which showed an abnormal
morphology, indicating an excessive epithelialization of the tissue
(Fig. 5A-F; n=11).
Conversely, Pax1 expression, which is a marker of the mesenchymal
sclerotome, was totally absent (Fig.
5G-I; n=8). These results suggest that Wnt11, like Wnt6,
is an epithelialization factor acting on the dermomyotome. By restricting
Wnt6 expression to the ectoderm overlying the VLL, and by
Wnt11 expression restricted to the DML, the persistent epithelial
character of the dermomyotome is limited to the marginal lips, which promote
ongoing dermomyotomal growth, whereas the central dermomyotomal domains
deepithelialize to form the dorsal dermis
(Scaal and Christ, 2004). We,
thus, propose an experimental model to explain the maintenance of the
dermomyotomal lips in contrast to the early dissociation of the central
dermomyotome in the mature somite (Fig.
6). |
DISCUSSION |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Upon
signaling from the ectoderm, the bHLH transcription factor Paraxis is
expressed in these epithelializing cells, together with the tyrosine kinase
receptor EphA4 (Burgess et al.,
1996; Sosic et al.,
1997; Schmidt et al.,
2001). During somite formation, the epithelial cells arrange as
spheres to enclose the still mesenchymal somitocoele
(Kulesa and Fraser, 2002).
Studies of segmental plate explants in culture suggest that the
epithelialization step is necessary to synchronize expression of segmentation
genes (Maroto et al., 2005).
Such a community effect might be a general requirement for coordinated gene
expression also in later stages of somite development. Following somite
formation, the ventral somite halves de-epithelialize under the influence of
signals from the notochord and ventral neural tube (reviewed by
Christ et al., 2004). In the
dorsal compartment, the somitic epithelium remains intact under the influence
of the neural tube and the surface ectoderm, thus forming the dermomyotome
(Kenny-Mobbs and Thorogood,
1987; Christ et al.,
1992; Spence et al.,
1996). Molecular studies have revealed that the formation of the
medial dermomyotome depends on Wnt1 and Wnt3a signaling from the dorsal neural
tube (Dietrich et al., 1997;
Fan et al., 1997;
Marcelle et al., 1997;
Wagner et al., 2000).
Accordingly, in mouse, Wnt1/3a knockout mice lose the medial aspect
of the dermomyotome (Ikeya and Takada,
1998). The lateral dermomyotome is known to depend on signals from
the surface ectoderm (Dietrich et al.,
1997; Fan and Tessier-Lavigne,
1994; Fan et al.,
1997). In recent studies, Wnt6 has been identified as an
epithelialization factor from the surface ectoderm which is required for
dermomyotome formation and maintenance
(Schmidt et al., 2004;
Linker et al., 2005). Wnt6
maintains the epithelial morphology of dermomyotomal cells by promoting
Paraxis expression via Frizzled7 and ß-catenin intracellular
signaling (Linker et al.,
2005). Until embryonic day 3 the dermomyotome is a continuous
epithelial sheet of approximately rectangular shape. At either margin, the
epithelial cells form lip-like structures in which cells de-epithelialize and
emigrate to form muscle (Gros et al.,
2004) and endothelium (Wilting
et al., 1995). Later on, the central region of the dermomyotome
(CD) deepithelializes completely to give rise to dorsally emigrating dermal
and subcutaneous precursor cells, and ventrally emigrating proliferative
muscle progenitor cells and satellite cells
(Gros et al., 2005;
Relaix et al., 2005;
Ben-Yair and Kalcheim, 2005).
By contrast, the DML and VLL persist as two separate epithelial proliferation
zones which are required for ongoing mediolateral growth of the dermomyotome
and its derivatives. At embryonic day 7, when the entire dermomyotome has
developed into definite tissues, the DML and VLL disintegrate
(Ordahl et al., 2001;
Venters and Ordahl, 2002). The
molecular basis for the differential timing of dermomyotomal
de-epithelialization in the margins and the CD has remained elusive.
|
; Linker et al.,
2005), is downregulated in the medial and central paraxial
ectoderm by signals from the neural tube. To extend earlier findings that Wnt1
and Wnt3a from the dorsal neural tube pattern the medial dermomyotome
(Dietrich et al., 1997;
Fan et al., 1997;
Marcelle et al., 1997;
Wagner et al., 2000), we show
here that these signals also pattern ectodermal gene expression and inhibit
Wnt6 expression in the ectoderm overlying the medial and central
dermomyotome. Further upstream in this signaling cascade, Wnt1/3a signaling
depends on BMP4 activity in the neural tube
(Marcelle et al., 1997). In
confirmation of our results, we observed that inhibition of BMP4 by
overexpression of Noggin in the neural tube also leads to an extension of
Wnt6 expression to the medial paraxial ectoderm (data not shown).
However, as Wnt1/3a are already expressed in early stages of paraxial
mesoderm development, while Wnt6 is still expressed throughout the
surface ectoderm, we searched for an intermediate regulator restricting
Wnt1/3a action on the somite stages following dermomyotome formation. We found
that the inhibition of medial Wnt6 expression depends on the presence
of the DML, thus identifying a patterning influence of the paraxial mesoderm
on the overlying ectoderm. Marcelle and co-workers
(Marcelle et al., 1997) have
shown that the DML is demarcated by Wnt11 expression, and that Wnt11
expression depends on Wnt1/3a signaling from the neural tube. We therefore
tested if Wnt11 is able to inhibit ectodermal Wnt6 expression, and
performed localized overexpression of Wnt11 in the dorsal somites. We found
that indeed dermomyotomal Wnt11 inhibits Wnt6 expression in the
overlying ectoderm, making it an excellent candidate for the intermediate
factor restricting the Wnt6 inhibitory action of Wnt1/3a to later
stages of somite development.
|
;
Ben-Yair and Kalcheim, 2005).
In addition, the cranial and caudal dermomyotomal lips, which give rise to
myotomal cells and persist longer than the CD
(Ordahl et al., 2001;
Gros et al., 2004), are also
exposed to prolonged Wnt6 activity as Wnt6 expression is maintained
in the ectodermal ridges extending into the intersegmental clefts between the
adjacent somites until embryonic day 4
(Rodriguez-Niedenführ et al.,
2003) (our observation). How, then, is the DML kept epithelial? We
found that overexpression of Wnt11 leads to an overexpression of the
epithelial markers Pax3 and Paraxis, whereas the marker of
sclerotomal fate, Pax1, is absent. Moreover, the affected somites
displayed an abnormal morphology and reduced size, indicating an excessive
epithelialization including ventral somitic cells
(Schmidt et al., 2004), thus
preventing sclerotome formation. Thus, we could show that Wnt11 is a
mesoderm-intrinsic epithelialization factor that, upon induction from the
neural tube, maintains the epithelial state of the DML while restricting
Wnt6 expression to the ectoderm overlying the VLL. In the literature,
Wnt11 has been described to be involved in convergence extension movements
during zebrafish gastrulation (Heisenberg
et al., 2000). Here, we present a novel dual role of Wnt11 in
downregulation of ectodermal Wnt6 expression and maintenance of the
epithelial state of the DML. It remains to be elucidated if Wnt11 is
furthermore required for the cell movements during myotomal cell recruitment
in the DML. An important aspect of our results is that Wnt11 represents the
first known mesodermal epithelialization factor acting on its cells of origin
in a paracrine fashion, thus establishing a fundamental difference between the
regulation of epithelialization in the DML and the other dermomyotomal
regions, which are thought to depend entirely on ectodermal signals.
|
; Linker et al.,
2005). Following dermomyotome formation, Wnt1 and Wnt3a, which are
secreted by the dorsal neural tube upon local BMP signaling, induce
Wnt11 expression in the DML
(Marcelle et al., 1997). Wnt11
inhibits Wnt6 expression in the ectoderm overlying the medial and
central dermomyotome, thus restricting Wnt6 expression to the lateral
ectoderm overlying the VLL. As both, Wnt6 and Wnt11, are epithelialization
factors, the DML (via Wnt11) and the VLL (via Wnt6) remain epithelial and
contribute to dermomyotomal growth, whereas cells in the CD de-epithelialize
to differentiate. Importantly, the intermediate activity of Wnt11 as
transducer of neural tube-derived signaling provides a timing mechanism
restricting this process to the fully formed dermomyotome. |
ACKNOWLEDGMENTS |
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