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Differential regulation of the chick dorsal thoracic dermal progenitors from the medial dermomyotome

Isabel Olivera-Martinez^*,, Sylvain Missier^*, Sandrine Fraboulet, Jacques Thélu and Danielle Dhouailly

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

View larger version (99K): [in a new window]   Fig. 1. Wnt11 and En1 are expressed in complementary domains in the chick medial dermomyotome. Dorsal views at HH18 of the forelimb (fo) level, and corresponding transversal sections, hybridized with Wnt11 (A-C), En1 (D-F), Sim1 (G-I) and MyoD (J-L) probes. Rectangles outline one somite that involves three regions along the mediolateral axis. (A-C) Wnt11 transcripts are detected in the dorsomedial lip (dml) (region 1) in the dermomyotomal cells closest to the dorsal neural tube (nt). Isolated Wnt11-expressing cells are also detected dorsomedially to the lip, under the ectoderm (ec). (D-F) En1 is expressed in a central compartment of the dermomyotome (region 2), in a domain distinct from that of Wnt11. (G-I) The lateral third of the dermomyotome expresses Sim1 (region 3) and is distinct from the En1 domain. (J-L) MyoD positive cells are detected under the dermomyotomal epithelial sheet. nc: notochord. Scale bars: 100 µm in A,B,D,E,G,H,J,K; 50 µm in C,F,I,L.

View larger version (93K): [in a new window]   Fig. 2. Wnt11 and En1 are expressed in distinct populations of the chick dorsal subectodermal mesenchyme in the epaxial domain. Dorsal views at HH23 of the forelimb (fo) level, and corresponding sections, hybridized with Wnt11 (A-C), En1 (D-F), Sim1 (G-I) and MyoD (J-L) probes. (A-C) Wnt11 transcripts are detected in the dorsomedial subectodermal mesenchyme. (D-F) En1 expression is detected in the dorsolateral mesenchyme. (G-I) Sim1 is detected in a few mesenchymal cells on each side of a notch (arrowhead) in the ectoderm, at the limit between the epaxial and the hypaxial domain, as well as in the Wolffian duct (Wd). (J-L) MyoD-positive cells are localized below the En1-and the Sim1-expressing cells, in the myotome (my). ec, ectoderm; dml, dorsomedial lip; nc, notochord; nt, neural tube. Scale bars: 100 µm in A,B,D,E,G,H,J,K; 50 µm for C,F,I,L.

View larger version (125K): [in a new window]   Fig. 3. Migratory behaviour of cells from the chick somitic dorsomedial lip. (A-C) DiI labelling of the dorsomedial lip (dml) of somite X (SX) (A, schematic) shows that dml cells (B, time zero, transverse section) give rise (C) to two distinct populations that migrate in opposite directions after 24 hours (red arrows). (D-F) Transplantation of five left-side somites, from a donor to the right side of a host embryo (D, schematic). (E-G) Hybridization with Wnt11 probe shows that after 24 hours, the Wnt11 cells have migrated from the transposed dorsomedial lip (tdml) over the entire dermomyotome towards the midline (m). This is seen in an external view of the right side (E) and in a transversal section (F, arrows). A higher magnification (G) clearly shows the migration of the cells from the tdml under the ectoderm (red arrows). nc, notochord; nt, neural tube; PSM, presomitic mesoderm. Scale bars: 50 µm in B,C; 300 µm in E; 70 µm in F,G.

View larger version (56K): [in a new window]   Fig. 4. Wnt1 cells grafted in place of neural tube and notochord inhibit Sim1 and trigger both Wnt11 and En1 expression in the medial dermomyotome. (A) A fragment of neural tube (NT) plus notochord (NC) was excised at HH13 between somite X (SX) and the chordoneural hinge (arrows). Wnt1 cell aggregates were grafted from somite V (SV) to the unsegmented presomitic mesoderm (PSM) in a length equivalent to five presumptive somites (red arrowheads), in order to maintain two excised ungrafted regions as controls. Embryos were fixed 12 hours (B-D), 24 hours (E-F) or 48 hours (G-J) after the operation. Dorsal views and corresponding transversal section, hybridized with Sim1 (B-D), MyoD (E, F), Wnt11 (G, H) and En1 (I, J) probes. (B-D) Sim1 expression expanded medially in excised ungrafted regions (B,C), while its normal lateral domain of expression was restored around the Wnt1 cell aggregate (asterisk) (B,D). (E,F) MyoD was expressed on both sides of the Wnt1 cell aggregate, in a deep position (F). (G,H) Wnt11 was activated on both sides of the Wnt1 cell aggregate (asterisk) in superficial epithelial structures reminiscent of the dorsomedial lip (H). (I,J) En1 was detected around the graft, in an intermediate mesenchymal population (J). Scale bars: 50 µm.

View larger version (86K): [in a new window]   Fig. 5. After only neural tube removal, En1 but not Wnt11 is activated at the level of the presomitic mesoderm (PSM). (A) The neural tube (nt) was removed from somite X to the PSM (between the arrows) leaving the notochord (nc) in place. Embryos were fixed after 48 hours (in B, the bracket indicates a region where a ventral part of neural tube was accidentally left in place). Dorsal views and corresponding transverse sections of embryos hybridized with Wnt11 (B-D) or En1 (E-G) probes. (B,C,E,F) At the anterior level, where somites were already segmented, Wnt11 (B,C) and En1 (E,F) are expressed in distinct domains of the mesenchyme. (B,D,E,G) At the posterior level, where somites were still unsegmented, Wnt11 is not activated (B,D), in contrast to En1, the expression domains of which are fused in a single medial band (E,G). ec, ectoderm; dml, dorsomedial lip. Scale bars: 50 µm.

View larger version (84K): [in a new window]   Fig. 6. The activation of En1 but not of Wnt11 depends on an ectodermal signal. (A) The ectoderm was removed bilaterally (or unilaterally, see text), over the dorsal region, from somite V (SV) to an equivalent length in the presomitic mesoderm (PSM). Dorsal views and corresponding transverse sections of the thoracic region, 24 hours after bilateral (B,C) or unilateral (D,E) ectodermal excision (indicated by the brackets), hybridized with Wnt11 (B,C) or En1 (D,E) probes. Note the complete healing of the ectoderm (ec), as shown in transverse sections (C,E). (B,C) Wnt11 transcripts are detected (arrowhead) in all somites, although in the central region of the excision they are smaller than normal. (D,E) En1 is absent (arrowhead) from the operated side, in contrast to the non-operated side. nc, notochord; nt, neural tube. Scale bars: 50 µm.

View larger version (32K): [in a new window]   Fig. 7. Regulation and localization of the thoracic dermal progenitors in chick embryo. At E3, activation by the dorsal neural tube of Wnt11 in the DML, then by the ectoderm of En1 in the intervening space of the medial dermomyotome. At E4, formation by migration of the dorsomedial and by delamination of the dorsolateral mesenchyme, which continue to express respectively Wnt11 and En1. It should be noted that a narrow third population that expresses Sim1 forms the border between the epaxial and hypaxial domains. ao, aorta; fo, forelimb; nc, notochord; nt, neural tube; Wd, Wolffian duct.