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Review
. 2001 Dec;2(12):1083-8.
doi: 10.1093/embo-reports/kve255.

Generating Patterns From Fields of Cells. Examples From Drosophila Segmentation

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Free PMC article
Review

Generating Patterns From Fields of Cells. Examples From Drosophila Segmentation

B Sanson. EMBO Rep. .
Free PMC article

Erratum in

  • EMBO Rep 2002 Feb;3(2):197

Abstract

In Drosophila, a cascade of maternal, gap, pair-rule and segment polarity genes subdivides the antero/posterior axis of the embryo into repeating segmental stripes. This review summarizes what happens next, i.e. how an intrasegmental pattern is generated and controls the differentiation of specific cell types in the epidermis. Within each segment, cells secreting the signalling molecules Wingless (the homologue of vertebrate Wnt-1) and Hedgehog are found in narrow stripes on both sides of the parasegmental boundary. The Wingless and Hedgehog organizing activities help to establish two more stripes per segment that localize ligands for the Epidermal Growth Factor and the Notch signalling pathways, respectively. These four signals then act at short range and in concert to control epidermal differentiation at the single cell level across the segment. This example from Drosophila provides a paradigm for how organizers generate precise patterns, and ultimately different cell types, in a naïve field of cells.

Figures

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Fig. 1. Patterning along the A/P axis of the Drosophila embryo. A cascade of maternal and zygotic genes is activated in the syncitial embryo to subdivide the ectoderm into smaller domains (see Flybase, http://fly.ebi.ac.uk:7081/, for nomenclature and information about Drosophila genes). The embryo cellularizes and undergoes gastrulation after activation of the pair-rule genes. The segment polarity genes and the Hox genes are activated by the pair-rule genes but a subset of gap genes also influences directly the Hox genes. Both segment polarity and Hox genes are thought to act in concert to control the differentiation of each segment of the future larva.
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Fig. 2. Generation of an intrasegmental pattern in the Drosophila embryo. This sequence is accurate for the ventral side of the abdomen. PS designates the parasegmental boundaries and S the segmental boundaries. The anterior of the embryo is to the left, the posterior to the right. The apical side of the cells is up, the basal side is down. Small violet dots represent the extracellular gradient of Wg protein. At stage 9–10, Wg and En/Hh expression is interdependent, and the Wg gradient symmetrical. At stage 11, Wg and En/Hh expression become independent, and the Wg gradient becomes asymmetric. At the same time, the Ser domain is delimited by the repressive action of both Wg and Hh. This generates one Ser stripe, two to three cells wide, per parasegment. At stage 12, Hh activates Rho expression in two rows of cells posterior to the En/Hh domain, and Ser activates Rho in one row of cells anterior to its domain. This results in a stripe of Rho expression precisely three cells wide. Anterior to the En/Hh domain, Wg signalling represses Rho expression. At the end of stage 12, the PS boundaries are no longer visible, and the segment grooves have formed immediately posterior to the En cells. At the end of embryogenesis, the posterior row of En cells and the Rho and Ser cells secrete denticles which make up the ventral denticle belts of the larval abdomen. Wg signalling specifies smooth cuticle in asymmetric fashion, three to four cell diameters in the anterior direction, but only extending through the first row of En cells to the posterior. The Ser-expressing cells secrete rows 5 and 6 of the denticle belts
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Fig. 3. Control of epidermal differentiation by the intrasegmental pattern. (A) Wg and Spi ligands are distributed across two domains of roughly equal size. Their gradients overlap within the En-expressing cells, where a mechanism of competition leads to activation of Wg signalling in the anterior En cell, and to activation of EGFR signalling in the posterior En cell. Svb is expressed in the cells that will secrete denticles on the ventral side of the future larva, and its domain coincides with the domain of EGFR activation. Cells under the influence of Wg signalling repress Svb expression and secrete a smooth cuticle. The photograph shows a larval cuticle visualized by dark field microscopy. (B) The ligands Wg, Hh and Spi act at short-distance and anisotropically to stimulate the expression of the protein Stripe in three rows of cells in the ventral epidermis.
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Bénédicte Sanson

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