Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs

Abstract

The appendage primordia of Drosophila are subdivided into compartments by the localized expression of transcription factors. Interaction between cells in adjacent compartments establishes organizing centres responsible for generating spatial pattern and promoting cell proliferation in the developing appendages. Localized expression of hedgehog (hh) in the posterior compartment of the leg imaginal disc directs expression of wingless (wg) in ventral-anterior cells and decapentaplegic (dpp) in dorsal-anterior cells near the anterior-posterior compartment boundary; wg then acts to specify ventral cell fate and to organize the dorsal-ventral axis of the leg. Interaction between wg-expressing ventral cells and dorsal cells near the anterior-posterior compartment boundary promotes axis formation in the leg. Here we show that the combined action of wg-expressing cells in the ventral-anterior compartment and dpp-expressing cells in the dorsal-anterior compartment activates expression of Distal-less, a gene required for proximal-distal axis formation in the limbs. These results demonstrate that sequential interaction between anterior-posterior and dorsal-ventral compartments establishes the proximal-distal axis of the limbs.

Expression of genes encoding bone morphogenetic proteins and sonic hedgehog in talpid (ta3) limb buds: Their relationships in the signalling cascade involved in limb patterning

“…It is at present unclear whether their expression across the a-p axis is responsible for the low polarizing activity or a consequence of it. In Drosophilu wing development, Drosophilu hedgehog gene expression activates expression of dpp, the homologue of BMP-2 and BMP-4, in neighbouring cells and hedgehog is thought to pattern the mesenchyme by acting through dpp (Basler and Struhl, 1994;Diaz-Benjumea et al, 1994). As the domains of shh and Bmp-2 are similar in the developing chick limb, with both genes being expressed in the polarizing region, a similar pathway may operate in vertebrate limbs.…”

Insulin signaling and limb-patterning: candidate pathways for the origin and evolutionary diversification of beetle ‘horns’

“…Cells at their point of intersection (ie with high levels of both signals) become the distal tip of the growing appendage, and gradients of Wg and Dpp protein determine the amount of growth along the new proximal/distal (outgrowth) axis (Struhl and Basler, 1993;Diaz-Benjumea et al, 1994;Held et al, 1994;Serrano and O'Farrell, 1997). As a result of their role in determining the precise location of the axis of outgrowth, and their role in determining the amount of outgrowth, the patterning genes wg and dpp are candidates for genetic changes in horn location, and in horn size.…”

“…Four of these patterning genes are expressed specifically at the distal tips of outgrowths/appendages (distal-less (dll), arista-less (al), epidermal growth factor receptor (egfr)), or in the medial regions of appendages (dachshund (dac)), and are required for growth of their respective regions within an appendage (eg Diaz-Benjumea et al, 1994;Serrano and O'Farrell, 1997;Galindo et al, 2002;Kojima, 2004;Weihe et al, 2005). If they function similarly in scarabs, then changes in levels or domains of expression of any of these genes could alter the shape, the final size, or even the presence/absence of a beetle horn.…”

BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration

“…Here we describe the roles of these genes, and of a Schmidtea mediterranea BMP-like gene (smedbmp4-1), in regeneration and homeostasis. BMPs are TGF-␤ signaling ligands that mediate a number of developmental events, such as embryonic dorsal-ventral patterning and Drosophila imaginal disc patterning (Diaz-Benjumea et al, 1994;Martindale, 2005;Padgett et al, 1987;Spencer et al, 1982). Little is known about the role this pathway may play in the maintenance of differentiated structures and their regeneration after amputation.…”