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Cell coherence during production of the presomitic mesoderm and somitogenesis in the mouse embryo

Unité de Biologie moléculaire du Développement, Institut Pasteur, 25, rue du Docteur Roux, 75724 Paris Cédex 15, France

View larger version (70K): [in a new window]   Fig. 1. (A,B) Expression of the control R2Achnls lacZ transgene in E11.5 embryos, in toto X-gal staining (A) and a transverse section (B). (C-E) Examples of long clones. Arrowheads indicate the most anterior and the most posterior labelled segments for each side of the embryos. (C,D) Left and right sides of a mediolaterally regionalised long bilateral clone, SC590. (E) A long unilateral clone, SC276. (F-P) Examples of short plurisegmented clones. The number of each labelled segment is indicated. (F-H) Short unilateral plurisegmented clones. Clone LM53 (F, medial) and clone SC1 (G, lateral), contribute to two consecutive segments. Clone VG9 (H, intermediate), is five segments long. (I-P) Short bilateral clones. (I-N) In toto lateral views. (O,P) Transverse sections. Clone SC186 (I-J,O, medial) and clone VG13 (K-L,P, lateral) contribute to two consecutive segments, and clone VG4 (M-N, medial), is five segments long. FL, forelimb; HL, hindlimb; NT, neural tube; m, medial; l, lateral. In B,O,P, the arrowheads indicate the morphological indentation of the body wall.

View larger version (36K): [in a new window]   Fig. 2. (A) Definition of the mediolateral extension (MLE) of the labelling in pooled segments of a clone. (B,C) ML contribution of the short thoracic unilateral plurisegmented clones (B) and of the short bilateral clones (C). Each clone is represented by one (B) or by two white rectangles for the left and right sides of the embryo (C). The medial and lateral borders of the myotome are indicated. The height of the rectangles is proportional to the longitudinal extension of the clone (number of segments). Each segment is divided into a hundred parts of equal length. Each part with labelled cells is represented by a coloured bar. The number of labelled cells is colour coded: blue, one cell; green, two cells; yellow, three or four cells; red, five cells or more. m, medial; l, lateral; MB, medial border; LB, lateral border; MLE, mediolateral extension.

View larger version (32K): [in a new window]   Fig. 3. Correlation between the positions of the labelling in consecutive segments of short unilateral plurisegmented clones (B), of short bilateral clones (C) and between the positions of the labelling in the two sides of short bilateral clones (E). (A,D) Definition of the middle position of the labelling (MidP) in one segment (A) and in the segments of one side of the myotome (D). x and y axis represent MidP in, respectively, the most anterior and the most posterior of the two compared segments (B,C), or in the left and the right sides of the clone, respectively (E). In B, when the clone has only two labelled segments, the comparison between these two segments is represented in black, and when the clone has more than two labelled segments, the comparisons for the different couples of segments are represented with the same colour. In C, the comparisons for the different couples of segments of each unilateral contribution of a bilateral clone are represented by the same symbol and colour. |y-x|<20% area of the graphs is shaded. m, medial; l, lateral; MB, medial border; LB, lateral border.

View larger version (28K): [in a new window]   Fig. 4. Comparison of the middle position (MidP values) of the labelling in pooled labelled thoracic segments of the right and left sides of long clones contributing bilaterally to the thoracic level. (A) x axis and y axis represent MidP values in, respectively, the left and the right sides of the clone. |y-x|<20% area of the graph is shaded. (B) Definition of the maximal theoretical difference between the MidP values of the left and right labelling of a clone. To the left, the left and right labelling of a clone are represented as measured in the embryo. To the right, the left labelling of the same clone has been displaced to the medial extremity of the myotome, and its right labelling to the lateral extremity. Observed (obsMidP) and maximal theoretical (maxMidP) differences between the left and right MidP values are calculated as indicated by the double arrows. (C) The grey and blue shaded areas correspond to the observed difference between the MidP values inferior to 20% of the segment length. Clones outside this area are considered to be asymmetric. The grey area corresponds to observed difference between MidP inferior to 20% of the segment length but superior to the 20% maximal theoretical difference (non-informative clones). The blue area corresponds to the observed difference between MidP inferior to 20% of the segment length and inferior to the 20% maximal theoretical difference (symmetrical clones). m, medial; l, lateral; MB: medial border; LB, lateral border.

View larger version (27K): [in a new window]   Fig. 5. Models for the relationship of the precursor cells before and after bilateralisation. The pool of precursors (the large circle) before bilateralisation is represented above the myotomal segments of the left and right sides. Green arrows represent the ML axis of the left and right myotomes (below the myotomal segments) and red arrows represent the prefiguration of this axis in the pool of precursor cells before bilateralisation (above or to the right of the pool). Gradient of colours represents the ML regionalisation of the myotome, in the myotomal segments and in the precursor pool. (A) ML axis of the myotome is prefigured in ML axis of the pool, with an at least partial separation of the left and right precursors (red double arrow). Medial cells (white circle) in the pool contribute medially to the myotome, and lateral cells (black circle) laterally. Lateral cells contribute to a single side of the embryo, resulting in the absence of bilateral lateral clones. (B) No representation of the ML axis of the myotome in the pool before bilateralisation. Therefore, there is no relationship between the position of the precursors within the pool and the ML position of their myotomal descendants. (C) The ML axis of the myotome is prefigured in the ML axis of the pool, without separation between left and right precursors. Cells to the left of the pool (white circle) contribute to the lateral part of the left myotome and to the medial part of the right myotome, and this is inverted for cells to the right of the pool (black circle), resulting in complete asymmetry of the bilateral clones. (D) Orthogonal representation of the ML axis of the myotome in the pool before bilateralisation. All cells contributing either medially (white circle) or laterally (black circle) to the myotome can do so bilaterally. m, medial; l, lateral.

View larger version (27K): [in a new window]   Fig. 6. Coefficient of bilaterality of the long (A) and short bilateral (B) clones. The coefficient of bilaterality was calculated as (nR-nL)/(nR+nL), where nR and nL are the number of labelled segments in respectively the right side and the left side of the embryo. The number of clones (y axis) for each value (x axis) of the coefficient is represented. 0 corresponds to a perfectly equal contribution of clones to the right and left sides and –1 and +1 to unilateral clones.

View larger version (35K): [in a new window]   Fig. 7. Schematic representation of a model for cell organisation and axis transformation of the pool of myotomal precursors in the primitive streak, non-bilateralised mesoderm and bilateralised paraxial mesoderm. Posterior is above and anterior is below. Note that there was no attempt to represent the exact dimension and position of the pools of cells in these abstract representations of the structures of the embryo. The pool of self-renewing cells involved in axiogenesis is located in the primitive streak. The colour gradient symbolises regionalisation along an axis orthogonal to the ML axis of myotome. Most anterior cells (black circles) contribute to medial part of the paraxial mesoderm, in the presomitic mesoderm, the dermomyotome and myotome (black arrows). More posterior cells (white circles) contribute more laterally to the paraxial mesoderm (white arrows). This results in a reorientation of the axis, symbolised by the change of the gradient orientation. Maintenance of the regionalisation established in the primitive streak until the formation of the dermomyotome and myotome and is represented by the conservation of the gradient in these structures. Note the symmetry of the gradient between the left and right parts of the paraxial mesoderm. Medial cells in the pool of self-renewing cells (black and white circles) contribute bilaterally to the paraxial mesoderm (black and white arrows), and the most lateral cells (grey circle) contribute only to the side where they are located (grey arrow). Note that it is not known whether the relative position of the cells in the pool before bilateralisation are conserved during the topographic transformation occurring during gastrulation. The different length of the black, grey and white arrows illustrate the hypothesis that relative cell positions are not conserved. Clonal separation between medial and lateral parts of the somite (thick black lines) (Eloy-Trinquet and Nicolas, 2002), which persists in the myotome, is superimposed on the mediolateral regionalisation of the paraxial mesoderm established in the self-renewing cell pool situated in the primitive streak. A, anterior; P, posterior; l, lateral; m, medial; PS, primitive streak; PSM, presomitic mesoderm; S, somite; D, dermomyotome; M, myotome.