Equipe Biologie de la Différenciation Epithéliale, UMR CNRS 5538, LEDAC, Institut Albert Bonniot, Université Joseph Fourier, Grenoble, France
* These authors contributed equally to this work
Present address: Division of Cell and Developmental Biology, School of Life Sciences, University of Dundee, Wellcome Trust Biocentre, Dow Street, Dundee DD1 5EH, UK
Author for correspondence (e-mail: danielle.dhouailly{at}ujf-grenoble.fr)
Accepted 18 July 2002
![]() |
SUMMARY |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: Chick, Dermomyotome, Dermatome, Dermis, Feather, En1, Medial somite, Neural tube, Notochord, Skin, Somite, Wnt1, Wnt11
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Somites appear as epithelial structures that bud off from the presomitic mesoderm (Maroto and Pourquié, 2001). Soon after segmentation they become patterned along the dorsoventral and mediolateral axes. The ventral part forms a mesenchyme called the sclerotome, which gives rise to the vertebrae and at least part of the ribs (for reviews, see Christ and Ordahl, 1995
; Ordahl et al., 2000
). The dorsal epithelial part, called the dermomyotome, is known to produce the precursors of the striated muscles, and the scapular blade, as well as the dorsal dermis (Aoyama and Asamoto, 1988
; Christ and Ordahl, 1995
; Huang and Christ, 2000
; Huang et al., 2000a
; Huang et al., 2000b
; Mauger, 1972a
). More precisely, the epaxial (dorsal) muscles (Denetclaw et al., 1997
; Denetclaw and Ordahl, 2000
; Kalcheim et al., 1999
; Ordahl et al., 2001
; Ordahl and le Douarin, 1992
), as well as the feather-forming dorsal dermis (Olivera-Martinez et al., 2000
), originate from the medial dermomyotome. Moreover, its dorsomedial lip (DML) has recently been shown (Ordahl et al., 2001
) to drive growth and morphogenesis of both the primary myotome and the dermomyotome.
Extrinsic cues provided by surrounding tissues are responsible for the patterning of the somites (Aoyama and Asamoto, 1988; Borycki and Emerson, 2000
; Dockter, 2000
; Monsoro-Burq and le Douarin, 2000
; Ordahl and le Douarin, 1992
). The dorsal ectoderm and the dorsal neural tube have a dorsalizing effect on the somites, while the ventral notochord and floorplate exert a ventralizing effect (Brand-Saberi et al., 1993
; Cossu et al., 1996a
; Cossu et al., 1996b
; Dietrich et al., 1997
; Hirsinger et al., 1998
). The lateral somite is specified by lateral plate-derived BMP4, that activates Sim1 (Pourquié et al., 1996
). This influence is antagonized by Noggin expression in the medial dermomyotome, which is activated by Wnt1 from the dorsal neural tube (Hirsinger et al., 1997
; Marcelle et al., 1997
). It is generally accepted that the epaxial myogenic lineage arises from the combined influences of notochord- and floorplate-derived Shh and dorsal neural tube Wnts (Borycki and Emerson, 2000
; Munsterberg et al., 1995
). In the absence of the neural tube and notochord, the medial somitic cells die, resulting in the absence of the vertebrae, dorsal muscles and ribs (Teillet et al., 1998
), and also of the dorsal feather field (Mauger, 1972b
; Olivera-Martinez et al., 2001
).
Recently, we showed that the survival and specification of dorsal dermal progenitors relied on a signal from the dorsal neural tube (Olivera-Martinez et al., 2001). Wnt1 cells grafted in place of the axial organs (neural tube plus notochord) specifically restore the formation of a competent dorsal dermis, while no axial cartilage and almost no epaxial muscle form. This restored dermis possesses all the abilities that are characteristic (Dhouailly, 1977
) of a dorsal dermis. It is able to induce the formation of a dorsal feather field in its overlying epidermis the feather buds arising in longitudinal rows in a spatiotemporal sequence in accordance with the anteroposterior level of the Wnt1 cell graft (Olivera-Martinez et al., 2001
).
We report that the medial compartment of the dermomyotome, which is the origin of the dermis (Olivera-Martinez et al., 2000), expresses Wnt11 and En1 in a complementary pattern, prior to their expression in the subectodermal mesenchyme. This allowed us to examine further the mechanism of induction and the involvement of these genes in the dermal lineage, and particularly the link between the dermomyotomal and mesenchymal populations. Wnt11 has previously been shown to be expressed under the control of Wnt1 in the DML, and is suggested to be involved not only in myotomal but also in dorsal dermis development (Marcelle et al., 1997
; Tanda et al., 1995
). Active cell division in the DML leads to the formation of the dermomyotomal intervening space (Denetclaw et al., 1997
; Denetclaw and Ordahl, 2000
; Ordahl et al., 2001
), which expresses En1 and is suggested to produce myocytes in mice (Tajbakhsh and Buckingham, 2000
). During hindbrain development, En1 expression was shown to be controlled by Wnt1 (Danielian and McMahon, 1996
; Wurst et al., 1994
). We analysed the possibility that Wnt11 and En1 are expressed under the control of Wnt1 in the dermomyotome, and are involved in the specification of dermal as well as myogenic progenitors, by using different experimental conditions that alter, inhibit or restore the formation of the dermis. Our results indicate that the chick feather-forming dorsal dermis derives directly and indirectly from the DML. The most medial dermal progenitors originate from the DML, turn on Wnt11 under the influence of Wnt1 from the dorsal neural tube, and continue to express Wnt11 while migrating under the dorsomedial ectoderm. A second, smaller non migrating population of dermal progenitors is located in the intermediate domain and derives indirectly from the DML, probably turning off Wnt11 expression before turning on En1 under the control of the ectoderm.
![]() |
MATERIALS AND METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Microsurgery
Fertilized chick eggs (JA957 strain, SFPA, St Marcellin, France) were incubated at 38°C until the embryos reached HH12-15 (17 to 24 somites). Microsurgery was performed in ovo as previously described (Teillet et al., 1998). To visualize the embryos, India ink (Pelikan) in Tyrodes solution (1/10) was injected between the embryonic tissues and the vitelline layer.
DiI injections
Dorsomedial lips of somites IV and V in HH14-15 embryos were microinjected with 0.5% (weight/volume) DiI (Molecular probes D-282) in dimethylformamide. After an additional 24 hours incubation period, embryos were embedded, sectioned and analysed under an Olympus AX 70 fluorescent microscope.
Transplantation of somites from the left to the right side
To reverse the mediolateral axis of differentiated somites, five adjacent somites (VIII to XII) from the left side of a donor embryo were transplanted in place of the right matched somites of a host embryo of the same stage (HH15-16). After an additional 36 hours incubation period, embryos were fixed for whole-mount in situ hybridization.
Axial organs excision (neural tube and notochord) and Wnt1 cell graft
The neural tube and the notochord were removed from somite X to chordoneural hinge. Cell aggregates were grafted from somite V to the unsegmented paraxial mesoderm or presomitic mesoderm (PSM), along a length equivalent to five presumptive somites, in order to maintain two excised, ungrafted regions anteriorly and posteriorly to the grafts as controls. A stable Wnt1-producing fibroblast Rat-B1a cell-line and the control cells were a gift of Dr R. Nusse. The day before each operation, the cells were trypsinized and plated on uncoated bacterial Petri dishes to form the aggregates.
Neural tube excision
In order to study medial somitic lineages determination without the death observed in absence of the whole axial structures (Olivera-Martinez et al., 2001; Teillet et al., 1998
), the neural tube alone was removed from somite X to the chordoneural hinge, leaving in place the notochord at all axial levels. To help separating the neural tube from the notochord, a drop of dispase (0.1 mg/ml) was added, then rinsed with Tyrodes solution and inactivated by foetal calf serum or albumin.
Ectoderm removal
The ectoderm was removed with tungsten needles after enzymatic treatment with dispase (0.1 mg/ml). The anteroposterior extension of the removal was from somite V to an equivalent length in the PSM. Along the mediolateral axis, the ectoderm removal was unilateral or bilateral. For unilateral excisions, a slit in the ectoderm was made between the somitic mesoderm and the neural tube, and another one in the ectoderm overlying the lateral plate mesoderm, at a distance from the segmental plate equivalent to the width of a somite. For bilateral excisions the ectoderm was removed from the right lateral plate to the left lateral plate as previously.
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Wnt11 transcripts first appear in the dorsomedial lip (DML) of the rostral somites at HH14, then expand caudally, but not beyond somite IV (±1), as already described (Marcelle et al., 1997; Tanda et al., 1995
). We show that at HH18-19 at the forelimb level, Wnt11 expression is detected not only in the DML, but also in isolated cells located between the DML and the dorsal neural tube (Fig. 1A-C). The last isolated Wnt11-expressing cells appear on the medial edge of somite XVI (±1). At the same stage, En1 expression is detected in a subset of dermomyotomal cells, in a central position (Fig. 1D-F), from the VIIIth (±1) to the head somites. En1 domain can be allocated to the medial compartment since it is distinct from a third domain expressing Sim1 (Fig. 1G-I). This Sim1 somitic expression in chick characterizes the lateral territory (Pourquié et al., 1996
) (Fig. 1G-I). Committed myoblasts expressing MyoD are detected under the DML (Fig. 1J-L), as previously shown (Hirsinger et al., 2001
; Pownall and Emerson, 1992
; Saitoh et al., 1993
).
|
|
|
Wnt11 and En1 fail to be activated in absence of the neural tube and notochord, their expression being restored by Wnt1 cell grafts
In the absence of neural tube and notochord, a proper dorsal dermis, which is able to induce the formation of feathers, does not form (Mauger, 1972b; Olivera-Martinez et al., 2001
). The graft of Wnt1-producing cells is sufficient to restore the survival and differentiation of the medial somitic cells towards the dermal lineage (Olivera-Martinez et al., 2001
). In order to investigate whether Wnt11 and En1 expression are both restored in the paraxial mesoderm, the expression of dermomyotomal and myotomal markers was analysed between 6 and 48 hours after removal of the axial organs and graft of Wnt1 cells (Fig. 4A).
|
The signal required to activate En1 expression in the dermomyotome originates from the ectoderm and not from the neural tube
An intrinsic experimental problem is that many of the factors produced by the axial organs that act as patterning signals are necessary also for cell survival. Shh from the notochord and the floorplate, known as a ventral and myogenic factor (for a review, see Dockter, 2000), also allows survival of the medial somite (Teillet et al., 1998
). Thus, we analysed the expression of Wnt11 and En1 in the presence of the notochord that allows medial somitic cells to survive, but in absence of the neural tube that expresses Wnt1 (Rong et al., 1992
; Teillet et al., 1998
; Teillet and le Douarin, 1983
).
Therefore, we excised only the neural tube, leaving the notochord in place (Fig. 5A). Forty-eight hours after the excision, somites segmented prior to the operation expressed Wnt11 (n=3) and En1 (n=3) (Fig. 5B,C,E,F). By contrast, only En1 expression was initiated in the former presomitic mesoderm, which fused in a single mass of cells forming a ribbon under the ectoderm (n=3) (Fig. 5B,D,E,G). Consequently, En1 onset does not require a neural tube factor and we set out to test if the ectoderm provided a signal involved in the activation of En1 in the dermomyotome.
|
|
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Some of the Wnt11 cells activated by neural tube Wnt1 migrate from the dorsomedial lip to form the dorsomedial dermis
The DML of the dermomyotome is a site of high mitotic activity (Borycki and Emerson, 2000; Denetclaw and Ordahl, 2000
; Kalcheim et al., 1999
; Ordahl et al., 2001
), and expresses Wnt11 from around somite IV (Marcelle et al., 1999
; Tanda et al., 1995
) (present work). While these cells are dividing, they are probably not committed to any lineage, although they express Myf5 (Hacker and Guthrie, 1998
; Hirsinger et al., 2000
). Moreover, it has recently been shown (Kiefer and Hauschka, 2001
) that only a subset of cells that initially express Myf5 will upregulate its expression and differentiate as muscle. This subset translocates from the DML under the epithelial dermomyotome, does no more express Wnt11, begins to express MyoD and forms the epaxial myogenic progenitors (Cinnamon et al., 2001
; Cinnamon et al., 1999
; Denetclaw et al., 1997
; Hirsinger et al., 2000
; Ordahl et al., 2001
; Ordahl and le Douarin, 1992
; Ordahl et al., 2000
). We show that beginning around somite XVI at stage HH18, Wnt11 transcripts are also present in mesenchymal cells dorsomedially to the lip, prior to their detection in the subectodermal mesenchyme of the dorsomedial region. DiI labelling (our results) (Denetclaw et al., 1997
), as well as chick/quail chimaeras of the DML (Ordahl et al., 2001
), demonstrate that cells from this region can migrate towards the midline. As these dermal precursors continue to express Wnt11 while migrating and when they have reached their target under the ectoderm, it is possible that Wnt11 coordinates the movement of dermal precursors in an autocrine or paracrine loop. Wnt11 has indeed been shown to be implicated in coordinating convergent extension movements during gastrulation in zebrafish (Heisenberg et al., 2000
) and Xenopus (Tada and Smith, 2000
) using a pathway that diverges from the canonical ß-catenin pathway at the level of Disheveled. Interestingly, after the transplantation of differentiated somites from left to the right, Wnt11 is still expressed by the DML that is now in a lateral location. More surprisingly, Wnt11-positive cells that detach from the DML still move towards the midline. These cells can thus either respond to attractive signals from the axial tissues, or have an affinity for extracellular materials present under the dorsomedial ectoderm and above the somite. Another possibility is that they are repelled or simply cannot move on the intermediate or lateral plate mesoderm. These possibilities still remain to be tested and the molecules involved identified.
The fact that Wnt11 somitic expression relies on Wnt1 was already shown and confirmed by its ectopic activation in the lateral dermomyotome (Marcelle et al., 1997; Tanda et al., 1995
). We show further that the absence of the ectoderm does not interfere with Wnt11 onset in the dorsal dermal progenitors. The Wnt1 signal probably acts through the ß-catenin pathway in this system (Schmidt et al., 2000
). The fact that Wnt1 inhibits apoptosis through ß-catenin (Chen and Chuong, 2000
) is in agreement with the fact that Wnt1 could partially restore cell survival in the medial somite after removal of the neural tube and notochord (Olivera-Martinez et al., 2001
). In particular, this would permit the survival of cells of the growing intervening space that will come to express En1 under the control of the ectoderm.
Cells that detach from the highly mitotic DML undergo an epithelial-mesenchymal transition. The migration from the DML occurs over an extended period of time ranging from E2 to E5 at different levels of the anteroposterior axis in the chick embryo. Previous results have led to the conclusion that the epithelial-mesenchymal conversion of the dermomyotome requires a neurotrophin 3 (NT3) signal from the neural tube (Brill et al., 1995). However, in the absence of the neural tube, and thus in the absence of the NT3 signal, Wnt1 appears sufficient to restore the formation of a nearly normal dermis, suggesting that NT3 is not the only factor involved in the formation of the loose subectodermal mesenchyme. NT3 might be also one of the factors that allow the migration of the DML cells towards the dorsal neural tube. It would be interesting to study if NT3 controls the epithelial-mesenchymal transition by acting downstream of Wnt1 or by antagonizing ectodermal signals. Indeed, recent results show that the ectoderm is required to maintain the epithelial structure of the dermomyotome (Marcelle, personal communication). Wnt molecules, known to be expressed in the ectoderm from the mouse (Fan et al., 1997
) as well as from the chick (Cauthen et al., 2001
; Schubert et al., 2002
; Wagner et al., 2000
) may mediate this effect.
Some of the En1 cells controlled by the ectoderm delaminate from the intervening space to form the dorsolateral dermis
En1 is expressed in a central dermomyotomal population, next to the Wnt11-expressing cells, that was originally called a dermatome (Davidson et al., 1988; Davis et al., 1991
). Truly, it must still be considered to be dermomyotome as some of these cells give rise to myogenic cells (Hadchouel et al., 2000
; Ordahl et al., 2001
; Tajbakhsh and Buckingham, 2000
). As the En1-expressing region is distinct from the Sim1 domain, and given that Sim1 in the chick is considered as a marker of the lateral compartment (Pourquié et al., 1996
), then we conclude that the En1 domain can be allocated to the medial compartment of the dermomyotome. As the DML cells divide, they progressively generate an intervening space or central dermomyotome domain (Denetclaw and Ordahl, 2000
; Ordahl et al., 2001
) that corresponds to the En1-positive domain. As observed in other developmental systems such as the limb bud (Cygan et al., 1997
; Laufer et al., 1997
), the En1- and Wnt11-expressing cell populations do not appear to overlap. The cells that express En1 in the central dermomyotome might previously have expressed Wnt11, but if so they have subsequently turned it off. Indeed, grafting of quail medial presomitic mesoderm in chick (Olivera-Martinez et al., 2000
) leads to the formation of a dorsal dermal region that includes the Wnt11 and the En1 domains. Some of these En1-expressing cells constitute a second population of thoracic dermal precursors that undergo an epithelial-mesenchymal transition. These cells do not migrate, as they are already located at their final position and detach from the dermomyotome under the ectoderm to form the dorsolateral dermal region. This process might also be controlled by a NT3 signal from the dorsal neural tube (Brill et al., 1995
).
Engrailed is known to be activated by Wg/Wnt proteins in various organisms, from Drosophila to vertebrates (Danielian and McMahon, 1996; Heemskerk et al., 1991
; Ingham et al., 1988
; Logan et al., 1997
). We show here that the onset of En1 expression in the somite does not depend on Wnt1 from the neural tube, but on an ectodermal signal. After the ectoderm excision, the absence of En1 expression is transient, owing to the rapid healing of the ectoderm (our data) (Nodder and Martin, 1997
; Thévenet, 1969
) and does not lead to any perturbation of the dermis of the dorsal feather field as observed at 10 days (Olivera-Martinez et al., 2001
). Wnt family members described in the ectoderm (Cauthen et al., 2001
; Fan et al., 1997
; Wagner et al., 2000
) could be responsible for En1 onset in the dermomyotome. Wnt6 was recently shown to be expressed throughout the chick dorsal ectoderm (Schubert et al., 2002
), but its expression is strangely lowest above the zone of En1 expression in the central dermomyotome. Thus the identity of the ectodermal factor responsible for En1 activation remains to be elucidated and is currently under examination. A second interesting issue that remains to be explored is the role of En1 expression in this region. En1 is well known to be a repressor of transcription. It would be tempting to speculate that it could be acting as an inhibitor of dermal differentiation, given the fact that in the chick the initiation of skin differentiation proceeds in a gradient from the midline (where Wnt11 is expressed) to the lateral dermis (where En1 is expressed).
A dermatome does not exist as a discrete entity in the dermomyotome
Our data showing the role of the DML in the formation of dermis are in accordance with recent results (Ordahl et al., 2001) according to which this structure would give rise not only to epaxial muscles, as already well known, but also to dermal cells. Likewise, it is very likely that the En1 dermomyotomal domain contributes to lineages other than the dorsal dermis: in mice, this domain has been suggested to give rise to myotomal cells (Hadchouel et al., 2000
; Ordahl et al., 2001
; Tajbakhsh and Buckingham, 2000
). Wnt11 and En1 are thus expressed in, at least, bi-potential progenitors. Taken together, these data imply that a discrete dermatome cannot be distinguished in the dermomyotome. Indeed, the dermal, as well as the muscle cell precursors can be identified only when they leave the same region of the epithelial dorsal somite, which thus deserves to be called a dermomyotome in its entirety.
Comparison between formation of the dorsal populations in chick and in mouse
In the chick embryo, dorsal dermis forms mainly by Wnt11-migrating cells that colonize the dorsomedial space under the ectoderm. In a lesser proportion, En1 cells also contribute to the dermis that form the borders of the thoracic dorsal field. In this species, the first dense dorsal dermis expresses Dermo 1 over the neural tube (Scaal et al., 2001) where the first rows of feathers differentiate. In chick, Dermo 1 expression thus begins medially and then extends laterally, over both the territories previously labelled by Wnt11 and En1, and even beyond, in the ventral dermis. By contrast, in mouse embryo, both the expression of Dermo 1 (Li et al., 1995
) and the formation of the first cutaneous appendages appear laterally, and only later extend over the neural tube. In chick, a narrow dorsomedial Msx1 population was shown to be the origin of the spinous processes of the vertebra (Monsoro-Burq and le Douarin, 2000
), while in mouse dorsomedial Msx1-expressing cells have been interpreted as a population of dermal cells, as it appears to originate from the dermomyotome (Houzelstein et al., 2000
). An interesting comparison is a possible functional equivalence between Msx1 in mouse and En1 in the chick. As these proteins are known to be transcriptional repressors, they could indeed both prevent premature differentiation of the dermis, as already proposed in the case of Msx1 in the mouse (Houzelstein et al., 2000
). More precisely, the predermal cells that express En1 could be delayed in the acquisition of their feather-inducing abilities, corresponding with the delay in their expression of Dermo 1. Anyway, defining the precise dermomyotomal origin and the migratory behaviour of the somitically derived dermis remains an unresolved issue in the mouse. Moreover, it cannot be easily resolved by mouse/chick chimaeras as the site of initiation of dorsal dermis formation is different.
Origin, induction and migration of the dorsal thoracic feather-forming dermis
The present findings, together with our previous work and that of others studying somite patterning, lead us to propose the following model for the origin and specification of the dorsal predermal mesenchyme in the chick thoracic region (Fig. 7). The dermal progenitors arise from the medial somite that forms under the influence of Wnt1 from the dorsal neural tube. Subsequently, Wnt1 activates Wnt11 expression in the DML. While the DML divides, it receives different dorsal and/or ventral signals, and gives rise to at least three kinds of cells: (1) myogenic cells that translocate under the epithelial sheet and express MyoD; (2) dermal progenitors that detach from the lip, continue to express Wnt11 and migrate towards the dorsal midline; and (3) cells of the growing dermomyotomal intervening zone that begin to express En1 under the ectodermal influence and form, among other derivatives, a second group of dermal progenitors. Moreover, a narrow ribbon of Sim1 expressing cells forms the border between the epaxial and hypaxial domains and may form a third and small group of dorsal dermal progenitors. This population could give rise to the semi-apteric (semi-glabrous) region between the dorsal and ventral feather pterylae (feather fields); this possibility is currently under examination.
|
![]() |
ACKNOWLEDGMENTS |
---|
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Aoyama, H. and Asamoto, K. (1988). Determination of somite cells: independence of cell differentiation and morphogenesis. Development 104, 15-28.[Abstract]
Borycki, A. G. and Emerson, C. P. (2000). Multiple tissue interactions and signal transduction pathways control somite myogenesis. Curr. Top. Dev. Biol. 48, 165-224.[Medline]
Borycki, A. G., Strunk, K. E., Savary, R. and Emerson, C. P., Jr (1997). Distinct signal/response mechanisms regulate pax1 and QmyoD activation in sclerotomal and myotomal lineages of quail somites. Dev. Biol. 185, 185-200.[CrossRef][Medline]
Brand-Saberi, B., Ebensperger, C., Wilting, J., Balling, R. and Christ, B. (1993). The ventralizing effect of the notochord on somite differentiation in chick embryos. Anat. Embryol. 188, 239-245.[Medline]
Brill, G., Kahane, N., Carmeli, C., von Schack, D., Barde, Y. A. and Kalcheim, C. (1995). Epithelial-mesenchymal conversion of dermatome progenitors requires neural tube-derived signals: characterization of the role of Neurotrophin-3. Development 121, 2583-2594.
Cauthen, C. A., Berdougo, E., Sandler, J. and Burrus, L. W. (2001). Comparative analysis of the expression patterns of Wnts and Frizzleds during early myogenesis in chick embryos. Mech. Dev. 104, 133-138.[CrossRef][Medline]
Chen, C. W. and Chuong, C. M. (2000). Dynamic expression of lunatic fringe during feather morphogenesis: a switch from medial-lateral to anterior-posterior asymmetry. Mech. Dev. 91, 351-354.[CrossRef][Medline]
Christ, B., Jacob, H. J. and Jacob, M. (1977). Experimental analysis of the origin of the wing musculature in avian embryos. Anat. Embryol. 150, 171-186.[Medline]
Christ, B. and Ordahl, C. P. (1995). Early stages of chick somite development. Anat. Embryol. 191, 381-396.[Medline]
Cinnamon, Y., Kahane, N. and Kalcheim, C. (1999). Characterization of the early development of specific hypaxial muscles from the ventrolateral myotome. Development 126, 4305-4315.
Cinnamon, Y., Kahane, N., Bachelet, I. and Kalcheim, C. (2001). The sub-lip domain: a distinct pathway for myotome precursors that demonstrate rostral-caudal migration. Development 128, 341-351.
Cossu, G., Kelly, R., Tajbakhsh, S., di Donna, S., Vivarelli, E. and Buckingham, M. (1996a). Activation of different myogenic pathways: myf-5 is induced by the neural tube and MyoD by the dorsal ectoderm in mouse paraxial mesoderm. Development 122, 429-437.
Cossu, G., Tajbakhsh, S. and Buckingham, M. (1996b). How is myogenesis initiated in the embryo? Trends Genet. 12, 218-223.[CrossRef][Medline]
Cygan, J. A., Johnson, R. L. and McMahon, A. P. (1997). Novel regulatory interactions revealed by studies of murine limb pattern in Wnt-7a and En-1 mutants. Development 124, 5021-5032.
Danielian, P. S. and McMahon, A. P. (1996). Engrailed-1 as a target of the Wnt-1 signalling pathway in vertebrate midbrain development. Nature 383, 332-334.[CrossRef][Medline]
Davidson, D., Graham, E., Sime, C. and Hill, R. (1988). A gene with sequence similarity to Drosophila engrailed is expressed during the development of the neural tube and vertebrae in the mouse. Development 104, 305-316.[Abstract]
Davis, C. A., Holmyard, D. P., Millen, K. J. and Joyner, A. L. (1991). Examining pattern formation in mouse, chicken and frog embryos with an En-specific antiserum. Development 111, 287-298.[Abstract]
Denetclaw, W. F., Jr, Christ, B. and Ordahl, C. P. (1997). Location and growth of epaxial myotome precursor cells. Development 124, 1601-1610.
Denetclaw, W. F. and Ordahl, C. P. (2000). The growth of the dermomyotome and formation of early myotome lineages in thoracolumbar somites of chicken embryos. Development 127, 893-905.
Dhouailly, D. (1977). Dermo-epidermal interactions during morphogenesis of cutaneous appendages in amniotes. Front. Matrix Biol. 4, 86-121.
Dietrich, S., Schubert, F. R. and Lumsden, A. (1997). Control of dorsoventral pattern in the chick paraxial mesoderm. Development 124, 3895-3908.
Dockter, J. L. (2000). Sclerotome induction and differentiation. Curr. Top. Dev. Biol. 48, 77-127.[Medline]
Fan, C. M., Lee, C. S. and Tessier-Lavigne, M. (1997). A role for WNT proteins in induction of dermomyotome. Dev. Biol. 191, 160-165.[CrossRef][Medline]
Hacker, A. and Guthrie, S. (1998). A distinct developmental programme for the cranial paraxial mesoderm in the chick embryo. Development 125, 3461-3472.
Hadchouel, J., Tajbakhsh, S., Primig, M., Chang, T. H.-T., Daubas, P., Rocancourt, D. and Buckingham, M. (2000). Modular long-range regulation of Myf5 reveals unexpected heterogeneity between skeletal muscles in the mouse embryo. Development 127, 4455-4467.
Heemskerk, J., DiNardo, S., Kostriken, R. and OFarrell, P. H. (1991). Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature 352, 404-410.[CrossRef][Medline]
Heisenberg, C. P., Tada, M., Rauch, G. J., Saude, L., Concha, M. L., Geisler, R., Stemple, D. L., Smith, J. C. and Wilson, S. W. (2000). Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405, 76-81.[CrossRef][Medline]
Hirsinger, E., Duprez, D., Jouve, C., Malapert, P., Cooke, J. and Pourquié, O. (1997). Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP4 in avian somite patterning. Development 124, 4605-4614.
Hirsinger, E., Jouve, C., Malapert, P. and Pourquié, O. (1998). Role of growth factors in shaping the developing somite. Mol. Cell. Endocrinol. 140, 83-87.[CrossRef][Medline]
Hirsinger, E., Jouve, C., Dubrulle, J. and Pourquié, O. (2000). Somite formation and patterning. Int. Rev. Cytol. 198, 1-65.[Medline]
Hirsinger, E., Malapert, P., Dubrulle, J., Delfini, M. C., Duprez, D., Henrique, D., Ish-Horowicz, D. and Pourquié, O. (2001). Notch signalling acts in postmitotic avian myogenic cells to control MyoD activation. Development 128, 107-116.
Houzelstein, D., Cheraud, Y., Auda-Boucher, G., Fontaine-Perus, J. and Robert, B. (2000). The expression of the homeobox gene Msx1 reveals two populations of dermal progenitor cells originating from the somites. Development 127, 2155-2164.
Huang, R. and Christ, B. (2000). Origin of the epaxial and hypaxial myotome in avian embryos. Anat. Embryol. 202, 369-374.[CrossRef][Medline]
Huang, R., Zhi, Q., Patel, K., Wilting, J. and Christ, B. (2000a). Dual origin and segmental organisation of the avian scapula. Development 127, 3789-3794.
Huang, R., Zhi, Q., Schmidt, C., Wilting, J., Brand-Saberi, B. and Christ, B. (2000b). Sclerotomal origin of the ribs. Development 127, 527-532.
Ingham, P. W., Baker, N. E. and Martinez-Arias, A. (1988). Regulation of segment polarity genes in the Drosophila blastoderm by fushi tarazu and even skipped. Nature 331, 73-75.[CrossRef][Medline]
Jacob, M., Christ, B. and Jacob, H. J. (1978). On the migration of myogenic stem cells into the prospective wing region of chick embryos. A scanning and transmission electron microscope study. Anat. Embryol. 153, 179-193.[Medline]
Kalcheim, C., Cinnamon, Y. and Kahane, N. (1999). Myotome formation: a multistage process. Cell Tissue Res. 296, 161-173.[CrossRef][Medline]
Kiefer, J. C. and Hauschka, S. D. (2001). Myf-5 is transiently expressed in nonmuscle mesoderm and exhibits dynamic regional changes within the presegmented mesoderm and somites I-IV. Dev. Biol. 232, 77-90.[CrossRef][Medline]
Laufer, E., Dahn, R., Orozco, O. E., Yeo, C. Y., Pisenti, J., Henrique, D., Abott, U. K., Fallon, J. F. and Tabin, C. (1997). Expression of Radical fringe in limb-bud ectoderm regulates apical ectodermal ridge formation. Nature 386, 366-373.[CrossRef][Medline]
Li, L., Cserjesi, P. and Olson, E. N. (1995). Dermo-1: a novel twist-related bHLH protein expressed in the developing dermis. Dev. Biol. 172, 280-292.[CrossRef][Medline]
Logan, C., Hornbruch, A., Campbell, I. and Lumsden, A. (1997). The role of Engrailed in establishing the dorsoventral axis of the chick limb. Development 124, 2317-2324.
Marcelle, C., Ahlgren, S. and Bronner-Fraser, M. (1999). In vivo regulation of somite differentiation and proliferation by Sonic Hedgehog. Dev. Biol. 214, 277-287.[CrossRef][Medline]
Marcelle, C., Stark, M. R. and Bronner-Fraser, M. (1997). Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124, 3955-3963.
Maroto, M. and Pourquié, O. (2001). A molecular clock involved in somite segmentation. Curr. Top. Dev. Biol. 51, 221-248.[Medline]
Mauger, A. (1972a). The role of somitic mesoderm in the development of dorsal plumage in chick embryos. I. Origin, regulative capacity and determination of the plumage-forming mesoderm. J. Embryol. Exp. Morphol. 28, 313-341.[Medline]
Mauger, A. (1972b). Rôle du tube neural dans le développement du plumage dorsal de lembryon de poulet. Wilhelm Rouxs Archiv. 170, 244-266.
Monsoro-Burq, A. H. and le Douarin, N. (2000). Duality of molecular signaling involved in vertebral chondrogenesis. Curr. Top. Dev. Biol. 48, 43-75.[Medline]
Munsterberg, A. E., Kitajewski, J., Bumcrot, D. A., McMahon, A. P. and Lassar, A. B. (1995). Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev. 9, 2911-2922.[Abstract]
Nodder, S. and Martin, P. (1997). Wound healing in embryos: a review. Anat. Embryol. 195, 215-228.[CrossRef][Medline]
Olivera-Martinez, I., Coltey, M., Dhouailly, D. and Pourquié, O. (2000). Mediolateral somitic origin of ribs and dermis determined by quail-chick chimeras. Development 127, 4611-4617.
Olivera-Martinez, I., Thélu, J., Teillet, M. A. and Dhouailly, D. (2001). Dorsal dermis development depends on signal from the dorsal neural tube, which can be substituted by Wnt-1. Mech. Dev. 100, 233-244.[CrossRef][Medline]
Ordahl, C. P., Berdougo, E., Venters, S. J. and Denetclaw, W. F. (2001). The dermomyotome dorsomedial lip drives growth and morphogenesis of the primary myotome and dermomyotome epithelium. Development 128, 1731-1744.
Ordahl, C. P. and le Douarin, N. M. (1992). Two myogenic lineages within the developing somite. Development 114, 339-353.[Abstract]
Ordahl, C. P., Williams, B. A. and Denetclaw, W. (2000). Determination and morphogenesis in myogenic progenitor cells: an experimental embryological approach. Curr. Top. Dev. Biol. 48, 319-367.[Medline]
Pourquié, O., Fan, C. M., Coltey, M., Hirsinger, E., Watanabe, Y., Breant, C., Francis-West, P., Brickell, P., Tessier-Lavigne, M. and le Douarin, N. M. (1996). Lateral and axial signals involved in avian somite patterning: a role for BMP4. Cell 84, 461-471.[Medline]
Pownall, M. E. and Emerson, C. P., Jr (1992). Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Dev. Biol. 151, 67-79.[Medline]
Rong, P. M., Teillet, M. A., Ziller, C. and le Douarin, N. M. (1992). The neural tube/notochord complex is necessary for vertebral but not limb and body wall striated muscle differentiation. Development 115, 657-672.
Saitoh, O., Fujisawa-Sehara, A., Nabeshima, Y. and Periasamy, M. (1993). Expression of myogenic factors in denervated chicken breast muscle: isolation of the chicken Myf5 gene. Nucleic Acids Res. 21, 2503-2509.[Abstract]
Scaal, M., Fuchtbauer, E. M. and Brand-Saberi, B. (2001). cDermo-1 expression indicates a role in avian skin development. Anat. Embryol. 203, 1-7.[CrossRef][Medline]
Schmidt, M., Tanaka, M. and Munsterberg, A. (2000). Expression of (beta)-catenin in the developing chick myotome is regulated by myogenic signals. Development 127, 4105-4113.
Schubert, F. R., Mootoosamy, R. C., Walters, E. H., Graham, A., Tumiotto, L., Munsterberg, A. E., Lumsden, A. and Dietrich, S. (2002). Wnt6 marks sites of epithelial transformations in the chick embryo. Mech. Dev. 114, 143-148.[CrossRef][Medline]
Solursh, M., Drake, C. and Meier, S. (1987). The migration of myogenic cells from the somites at the wing level in avian embryos. Dev. Biol. 121, 389-396.[Medline]
Tada, M. and Smith, J. C. (2000). Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127, 2227-2238.
Tajbakhsh, S. and Buckingham, M. (2000). The birth of muscle progenitor cells in the mouse: spatiotemporal considerations. Curr. Top. Dev. Biol. 48, 225-268.[Medline]
Tanda, N., Ohuchi, H., Yoshioka, H., Noji, S. and Nohno, T. (1995). A chicken Wnt gene, Wnt-11, is involved in dermal development. Biochem. Biophys. Res. Commun. 211, 123-129.[CrossRef][Medline]
Teillet, M., Watanabe, Y., Jeffs, P., Duprez, D., Lapointe, F. and le Douarin, N. M. (1998). Sonic hedgehog is required for survival of both myogenic and chondrogenic somitic lineages. Development 125, 2019-2030.
Teillet, M. A. and le Douarin, N. M. (1983). Consequences of neural tube and notochord excision on the development of the peripheral nervous system in the chick embryo. Dev. Biol. 98, 192-211.[Medline]
Thévenet, A. (1969). Sur les modalités de la cicatrisation de lectoderme dorsal chez lembryon de poulet au cours du 3ème jour dincubation. Ann. Embryol. Morpholog. 2, 71-85.
Wagner, J., Schmidt, C., Nikowits, W., Jr and Christ, B. (2000). Compartmentalization of the somite and myogenesis in chick embryos are influenced by wnt expression. Dev. Biol. 228, 86-94.[CrossRef][Medline]
Wilkinson, D. G. and Nieto, M. A. (1993). Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol. 225, 361-373.[Medline]
Wurst, W., Auerbach, A. B. and Joyner, A. L. (1994). Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development 120, 2065-2075.