Equipe Biologie de la Différenciation Epithéliale, UMR CNRS 5538, LEDAC, Institut Albert Bonniot, Université Joseph Fourier, BP 53-38041 Grenoble Cedex 9, France
Author for correspondence (e-mail:
danielle.dhouailly{at}ujf-grenoble.fr)
Accepted 11 May 2004
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SUMMARY |
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Key words: Amnion, Bmp4, Chick, Dermis, Dorsoventral axis, Feather, Msx1, Noggin, Skin, Shh, Somatopleure
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Introduction |
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Two questions thus arise: what are the origins of and how are the dermal
progenitors of a pteryla specified? Numerous experiments have been conducted
using heterotopic mesoderm transplantations
(Mauger, 1972) and
dermal-epidermal recombinations (Dhouailly,
1977
) that have shown that the information relative to the feather
macropattern and micropattern resides first in the mesoderm and then in the
dermis. In avian embryos, the origin of the dermis from different body regions
has been investigated by the heterospecific chick/quail marking technique. In
the trunk, the ventral dermis is derived from the somatopleure, whereas the
dorsal dermis derives from the somite dermomyotome
(Mauger, 1972
). More
precisely, the dermis of the spinal pteryla derives from the medial part of
the dermomyotome, whereas its lateral part probably gives rise to the dermis
of the lateral semi-apterium, which forms the frontier with the ventral side
(Olivera-Martinez et al.,
2000
; Olivera-Martinez et al.,
2002
). The embryonic somatopleure can be divided by the
rostrocaudal axis into two
150 µm parts that behave differently
(Altabef et al., 1997
;
Michaud et al., 1997
). The
area that is the closest to the somites corresponds to the proximal
somatopleure and the other to the distal somatopleure. The aim of our study
was to understand how these two somatopleural mesoderm areas interact to form
the ventral feather macropattern, and what molecular factors are involved.
Until recently, the specification of pterylae formation has been poorly
documented at the molecular level. With respect to the dorsal pteryla, results
have shown that a dorsal neural tube signal, which can be substituted by Wnt1,
causes the commitment of median dermomyotomal cells into dermal progenitors
(Olivera-Martinez et al.,
2002; Olivera-Martinez et al.,
2001
), whereas nothing was known about the signaling involved in
ventral dermis formation. The juxtaposition of the ventral pteryla and the
midventral apterium provides a unique opportunity to understand the mechanisms
that allow the specification of these two different types of skin.
Interestingly, experimental manipulation of the chick distal somatopleure
at E2 can lead to the induction of a supplementary pteryla in the midventral
apterium (Sengel and Kieny,
1967a; Sengel and Kieny,
1967b
). This has been achieved by implanting either a living piece
of neural tube or agar implants impregnated with brain extract into the
presumptive territory of the midventral apterium. In preliminary experiments,
we were able to reproduce these results by grafting the ventral part of stage
HH 13 anterior neural tube into the same region. By contrast, the graft of the
dorsal half of the same fragment of neural tube did not change the fate of the
apterium. In the past ten years, many different diffusible signaling factors
synthesized by the neural tube have been identified
(Capdevila and Johnson, 1998
;
Echelard et al., 1993
;
Krauss et al., 1993
;
Parr et al., 1993
;
Pourquié et al., 1996
;
Riddle et al., 1993
;
Sela-Donenfeld and Kalcheim,
2000
; Watanabe and Le Douarin,
1996
). The anterior neural tube, between somites 15 and 19,
expresses, in particular, Wnt1 and Wnt3a in its dorsal half and principally
Noggin and Shh in its ventral half. Noggin has been shown to be
dorsally expressed, but only in the posterior part of the neural tube
(Sela-Donenfeld and Kalcheim,
2000
). Among the diffusible signaling factors produced by the
anterior ventral neural tube at stage HH 13 that can inhibit Bmp4 signaling,
two are also produced in the vicinity of the somatopleure: Noggin in the
intermediate mesoderm (Sela-Donenfeld and
Kalcheim, 2000
) and Sonic Hedgehog in the endoderm
(Watanabe et al., 1998
).
Moreover, fusions between the splanchnic and somatic tissues have previously
been shown to be correlated with the formation of ectopic pterylae
(Sengel and Kieny, 1967a
;
Sengel and Kieny, 1967b
;
Dhouailly, 1978
). Noggin and
Shh thus seemed plausible candidates to play a role in pterylae induction from
the somatopleure.
Noggin is known to operate by binding to Bmp2, Bmp4 and Bmp7, and
preventing their interaction with their cognate receptors
(Hirsinger et al., 1997;
Zimmerman et al., 1996
). The
relationship between Shh and Bmps appears to be variable in vertebrate
organogenesis. In the limb bud, expression of Bmp2, but not
Bmp4, can be induced by ectopically expressed Shh and, at
least partially, mediates the polarizing activities of Shh
(Drossopoulou et al., 2000
;
Duprez et al., 1996
;
Laufer et al., 1994
), whereas
ectopic expression of Shh in the dorsal neural tube abolishes
Bmp4 expression (Watanabe et al.,
1998
). In the case of the somatopleure, the expression of
Bmp4 (Hirsinger et al.,
1997
; Sela-Donenfeld and
Kalcheim, 2000
) does not necessarily lead to Bmp4
signaling. Therefore, it was of interest to analyze the pattern of expression
of target genes of Bmp4 signaling, in order to distinguish between the
presence of Bmp4 transcription and a signaling effect. Msx1 is one of
the target genes for Bmp signaling (Alvarez
Martinez et al., 2002
) but we had another reason to be interested
in it: its expression is thought to be involved in delaying differentiation
events (Houzelstein et al.,
1999
; Woloshin et al.,
1995
) and has previously been shown to be implicated in the
delayed formation of the mediodorsal dermis in mouse embryos
(Houzelstein et al., 2000
). As
the formation of ventral pterylae occurs in a wave from the flank to the
medioventral line, we formed the hypothesis that Msx1 might play a similar
role during the establishment of the chick ventral feather macropattern.
In this paper, we report that a wave of Noggin expression occurs in somatopleural mesoderm, and is involved in the formation of the ventral pteryla, whereas the more distal somatopleural mesoderm remains labile and expresses Msx1. However, whereas ectopic expressions of either noggin or Shh in the distal embryonic lateral plate is sufficient to induce the formation of a supplementary pteryla, they are both required in the extra-embryonic area.
Our results allow us to propose a model to explain the formation of the ventral skin feather macropattern, according to which the ventral pteryla is induced at E2 by endogenous Noggin, with a possible synergistic effect of Shh, which progressively downregulates Bmp4 signaling in the proximal somatopleure.
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Materials and methods |
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Microsurgical procedures
Chick and quail embryos were staged, respectively, according the Hamburger
and Hamilton (Hamburger and Hamilton,
1951), and Zacchei table
(Zacchei, 1961
). Ectopic
grafts of the proximal and distal somatic chick mesoderm, rotated 90°,
were performed under the ectoderm as described by Saunders and Reus
(Saunders and Reus, 1974
).
Quail eggs were incubated at 38°C until they reached their chick
counterpart stage. Quail proximal or distal somatopeural mesoderm taken
between the levels of 20th and 25th somites was grafted in chick in an
orthotopic manner. The grafts in the presumptive territory of the midventral
apterium consisted of axial organs as described by Kieny and Sengel
(Kieny and Sengel, 1964
). Cell
aggregates of various transformed cell lines producing diffusible factors were
grafted between the ectoderm and the mesoderm at the limit or at the exterior
of the embryonic area, posteriorly to the level of the 20th somite.
Cyclopamine treatment
Cyclopamine (BIOMOL) was resuspended in 95% ethanol as previously described
(Sukegawa et al., 2000) at a
concentration of 10 mM. Embryos were treated at E2 with 1 µl of cyclopamine
suspension. Control embryos were treated with an equivalent volume of 95%
ethanol.
Cell lines and obtention of cell aggregates
The Noggin-producing CHO cell line (CHO.B3A4) and the parent cell line (CHO
DHFR-) were supplied by Dr R. Harland and Dr J. M. de Jesus
(Lamb et al., 1993). The QT6
cell line, which expresses chick Shh under the influence of the CMV
promoter in the pBK plasmid, and the corresponding control-QT6 cells, as well
as the Bmp2/QT6 cell line were provided by Dr Duprez
(Duprez et al., 1996
). A
Wnt1-producing fibroblast Rat-B1 cell line and the control cells were a gift
from Dr Nusse. A Wnt3a-producing Rat-B1 cell-line was provided by Dr
Kitajewski. The cells were plated on uncoated bacteriological Petri dishes to
form aggregates.
In situ hybridization, immunohistochemistry and histology
Whole-mount in situ hybridization was carried out as described by Wilkinson
(Wilkinson, 1995). The cDNA
templates for chicken Bmp2, Bmp4
(Francis et al., 1994
) and
Shh (Riddle et al.,
1993
) were generated by RT-PCR, while the Noggin and
follistatin probes were provided by Dr Hurle, and the Msx1
probe by Dr B. Robert. The stained embryos were processed for cryosections (30
µm) following inclusion in gelatin/sucrose. For immunohistochemistry,
embryos were fixed in Carnoy's fluid, embedded in paraffin wax and sectioned
at 7 µm. In order to distinguish quail cells from chick cells, we used the
monoclonal antibody QCPN (Developmental Studies Hybridoma Bank) as described
(Catala et al., 1996
); sections
were counterstained with Hematoxylin.
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Results |
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Noggin- or Shh-expressing cells can induce the formation of a supplementary pteryla in the embryonic midventral apterium
In order to identify what signals might be responsible for the formation of
the somatopleural derived feather tracts, we investigated the molecular
mechanisms of the induction of a supplementary pteryla in the midventral
apterium. First, we grafted (Fig.
3A) either fragments of stage HH13 anterior whole neural tube
associated with chord, the dorsal half of the neural tube or the ventral half
plus chord under the ectoderm of the presumptive midventral apterium. Second,
we grafted (Fig. 3A) aggregates
of cells engineered to produce diffusible signaling factors, including
Wnt1/Rat-B1a, Wnt3a/Rat-B1a, Shh/QT6 cells, Noggin/CHO cells and control cells
(Table 1). Only grafting the
ventral half of the neural tube plus chord
(Fig. 3B), Shh-(Fig. 3C) or
Noggin-producing cells (Fig.
3D) led, in about 27% of cases, to the formation of a
supplementary pteryla (13 independent and 20 fused ones out of 121 cases in
total). The graft of control QT6, CHO and Rat-B1a cells, and of Wnt1- and
Wnt3a-producing cells (182 cases in total) never caused the formation of a
supplementary pteryla.
|
|
Previous experiments have shown that overexpression of Noggin and
Shh at the time of feather primordia causes the formation of
supplementary primordia (Jiang et al.,
1999; Noramly and Morgan,
1998
; Morgan et al.,
1998
; Ting-Berreth and Chuong,
1996
). In order to determine whether or not the supernumerary
pterylae could result from such late effects of Noggin or Shh in our
experiments, the grafted cells (quail cells for the Shh-producing cells) were
localized at the time of feather formation (E9/E10). In five out of five
analyzed cases, they were detected in the deep mesenchyme, at the level of the
future semi-apteria, or under the ventral pteryla, but always a clear distance
away from the supplementary pteryla (Fig.
3H). This result rules out the possibility that the supplementary
pteryla could result from a late effect of grafted cells on feather
initiation. The induction of a supplementary pteryla is thus an effect of the
signaling factors at the time of grafting (E2) that leads to an autonomous
differentiation of the distal embryonic somatopleural mesoderm into dermal
progenitors, which are able to trigger the formation of feather primordia
several days later.
Distribution of Noggin, Bmp4 and Shh transcripts during ventral skin morphogenesis, as well as after the graft of Noggin- or Shh-producing cells
In order to determine which factors might be implicated in the induction of
the ventral pteryla, we followed the distribution of the transcripts for
Noggin, Bmp4 and Shh in the body wall region from E2 to E10.
Previous studies (Hirsinger et al.,
1997; Sela-Donenfeld and
Kalcheim, 2000
) have already described Noggin and
Bmp4 expression patterns in the somatopleure at stage HH13. At this
stage, Noggin is expressed in the dorsal neural tube and the
intermediate and lateral plate mesoderm beside the unsegmented presomitic
mesoderm (Fig. 4A),
Bmp4 is expressed throughout all the somatopleural mesoderm and the
proximal part of the splanchnopleural mesoderm
(Fig. 4B), and Shh is
expressed in the chord and part of the endoderm beneath the proximal lateral
plate mesoderm (Fig. 4C).
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Discussion |
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The early commitment of a ventral feather-forming dermis requires Noggin and possibly Shh
The grafts of quail proximal or distal somatopleural mesoderm or chick
proximal somatopleural mesoderm rotated 90° showed that, in contrast to
the distal somatopleure, the proximal somatopleural mesoderm is committed to
the formation of a feather-forming dermis at E2. At this stage, Bmp4
transcripts are detected throughout the whole somatopleural mesoderm, whereas
Msx1 transcripts are located only in its distal part, suggesting that
Bmp4 is active only in the distal somatopleure. The inhibition of Bmp4
signaling in the proximal part is therefore correlated to its determination as
a feather tract. Likewise, at the time of feather formation
(Jung et al., 1998), BMPs
signaling is blocked by their antagonists
(Chuong, 1998
), and forced
expression of Bmp4 leads to the formation of patches of bare skin
(Noramly and Morgan,
1998
).
A supplementary pteryla was obtained by the grafts of Noggin or Shh cells
in the prospective midventral apterium. No change of Bmp4 expression
was detected after the graft of Noggin cells, but the expression of
Msx1 was downregulated. Our data suggest that Noggin inhibits Bmp4
signaling directly, as it has been shown to in Xenopus
(Piccolo et al., 1996;
Zimmerman et al., 1996
). By
contrast, Bmp4 was rapidly downregulated in the distal mesoderm after
the graft of Shh cells, showing that in our model, Shh is able to act, either
directly or indirectly, on Bmp4 transcription levels. This hypothesis
is supported by the use of cyclopamine, an inhibitor of Shh signaling (e.g.
Chen et al., 2002
). When chick
embryos were treated at E2, significant expression of Msx1 persisted
at E4.5. Unfortunately, the embryos did not survive until day 11, precluding
the analysis of pteryla and apteria formation. The toxicity of cyclopamine at
an early stage might suggest effects beyond those on Shh activity, given that
the Shh-null mouse survives until late stages of embryogenesis
(Chiang et al., 1996
).
Moreover, we cannot exclude a possible role of other Bmps, such as Bmp2 or
Bmp7, that were not analyzed in our study.
At the onset of somatopleural development, the inhibition of Bmp4
signaling, which correlates with the determination of the ventral pteryla, may
be due to the production of Noggin by the intermediate mesoderm and, possibly,
Shh by the endoderm. Interactions between Shh and Bmp4 have been already
observed during the morphogenesis of several vertebrate organs and tissues
(Capdevila et al., 1999;
Hirsinger et al., 1997
;
Merino et al., 1999
;
Schilling et al., 1999
;
Watanabe et al., 1998
;
Zhang and Yang, 2001
),
suggesting that this may act as a common mechanism to establish and maintain
distinct compartments. In our system, exogenous expression of either
noggin or Shh alone was sufficient to produce a
supplementary pteryla in the distal embryonic somatopleure. The potential
complementary factor, either Shh or Noggin, is not far away, diffusing from
the intermediate mesoderm and the proximal endoderm, respectively, and may act
in synergy with the ectopic grafted factor. The Shh signal is known to act at
a long-range during limb bud polarization
(Drossopoulou et al., 2000
).
Besides the fact that inhibiting Shh signaling with cyclopamine led to a
larger Bmp4-signaling domain, there is another observation supporting the
hypothesis that Shh acts synergistically with Noggin: both are required
simultaneously to induce a feather-forming skin in the extra-embryonic
somatopleure. This can, however, be explained either by the fact that both
endogenous source are too far away, or, alternatively, by a potential effect
of Shh on mesodermal cell proliferation
(Duprez et al., 1998
). It is
therefore conceivable that, in the case of ventral pteryla commitment, Shh
might diffuse from the endoderm to the proximal somatopleural mesoderm, and
hence acts together with Noggin to inhibit Bmp4 signaling to initiate
commitment of the ventral pteryla, which will be later sustained by the
lateral extension of noggin expression in the somatopleure.
The feather field morphogenetic wave is a consequence of the lateral extension of noggin expression
As the embryo develops, the mesodermal expression of noggin shifts
more distally, and so pushes back the activity of Bmp4, i.e. the Msx1
expression in the midventral region and amnion. The ventral shift of
noggin expression appears to reflect the ventral expansion of
mesodermal cells, which is illustrated by the behavior of GFP-labeled cells.
Depending to the stage of injection of the GFP plasmid in the proximal
somatopleure, the labeled cells were later found in a compartment
corresponding to the expression domain of noggin, or in the most
distal half of the noggin expression domain, respectively. These
cells then shifted slightly more ventrally, concurrent with the
noggin expression domain. The expression of Msx1, which
shifts progressively towards the midventral line, might correlate with the
delay, and finally, end of the formation of the ventral dense dermis. This
confirms that the formation of the midventral apterium is due to the lack of
differentiation of a true dermis (Sengel
et al., 1969).
Autonomous somatopleural formation of supplementary pterylae
The dermis of the induced ectopic pterylae, in either the embryonic or
extra-embryonic somatopleure is comprised exclusively of chick host
somatopleural cells. This is clearly shown by the use of quail
Shh-producing cells, and has already been shown by using mouse
tissues for the inducer (Dhouailly,
1978). The fact that the inducing cells are always found at a
distance and proximally to the ectopic pterylae suggests that there is a
narrow window of induction, corresponding to the short-lived contact between
the cell clump and the distal somatopleural mesoderm. This is also confirmed
by the fact that the formation of the independent ectopic pteryla starts from
one central point, expands slightly in a circular wave and ends. The lack of
rostral-caudal orientation in the supernumerary circular pterylae show that
they are not integrated with endogenous positional information. This contrasts
with the usual appearance of feathers in rows more or less parallel to the
rostrocaudal axis. The formation of the fused pteryla might result from a
slightly different mechanism, as they also start independently, but as a row.
Such a difference is probably linked to the location of the cell clump at the
time of grafting, closer to the proximal somatopleure.
Ventral skin feather macropattern formation
Integrating all our results, we propose a model
(Fig. 9) for the formation of
the ventral pteryla versus the mid-ventral apterium. Noggin, which is produced
by the intermediate mesoderm, and possibly Shh, which is secreted by the
proximal endoderm at E2, act to commit the proximal somatopleural mesoderm to
differentiate into a dense feather-forming dermis by inhibiting Bmp4
signaling. During the expansion of the somatopleure, proximal somatopleural
mesodermal cells expressing noggin shift distally and push the zone
of distal mesodermal cells expressing Msx1 under Bmp4 signaling
action back towards the ventral closure. Msx1 expressing cells might
delay the commitment to form a feather-forming dense dermis and, finally, give
rise to the loose dermal cells of the midventral apterium.
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ACKNOWLEDGMENTS |
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Footnotes |
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