The pruned gene encodes the Drosophila serum response factor and regulates cytoplasmic outgrowth during terminal branching of the tracheal system

Abstract

We identified a Drosophila gene, pruned, that regulates formation of the terminal branches of the tracheal (respiratory) system. These branches arise by extension of long cytoplasmic processes from terminal tracheal cells towards oxygen-starved tissues, followed by formation of a lumen within the processes. The pruned gene is expressed in terminal cells throughout the period of terminal branching. pruned encodes the Drosophila homologue of serum response factor (SRF), which functions with an ETS domain ternary complex factor as a growth-factor-activated transcription complex in mammalian cells. In pruned loss of function mutants, terminal cells fail to extend cytoplasmic projections. A constitutively activated SRF drives formation of extra projections that grow out in an unregulated fashion. An activated ternary complex factor has a similar effect. We propose that the Drosophila SRF functions like mammalian SRF in an inducible transcription complex, and that activation of this complex by signals from target tissues induces expression of genes involved in cytoplasmic outgrowth.

Wengen, a Tumour Necrosis Factor Receptor, regulates the Fibroblast Growth Factor pathway by an unconventional mechanism

“…in dorsal branches (DBs), lateral trunk (LT), ganglionic branches (GBs) and visceral branches (VB)) (Fig 1A-D, S1A-F). To determine the origin of these terminal branches we stained the embryos with DSRF, a marker for terminal cell differentiation 18,19 . We observed excess of DSRF positive cells that generated these adventitious terminal branches (Fig 1C -F).…”

Srf-/- ES cells display non-cell-autonomous impairment in mesodermal differentiation

“…Preparation of whole cell extracts and EMSA studies were performed as described previously (Heidenreich et al, 1999). A 32 P-labeled DNA fragment containing the c-fos SRE was used as DNA-binding probe together with <50% (v/v) whole cell extract prepared from ES cells.…”

“…Serum response factor (SRF) (Norman et al, 1988), a transcription factor of the MADS-box family (Sommer et al, 1990;Pellegrini et al, 1995;Shore and Sharrocks, 1995), mediates signal-stimulated transcriptional induction of immediate-early genes (IEGs) (Herschman, 1991;Johansen and Prywes, 1995;Morgan and Curran, 1995;Treisman, 1996). It also contributes to cell-type-speci®c gene control, e.g.…”

“…SRF function in gene control has been studied extensively in cultured cells but less is known about SRF activity at the level of the organism. Initial clues regarding SRF function in multicellular organisms were revealed by the two independent Drosophila melanogaster mutations pruned (Guillemin et al ., 1996) and blistered (Montagne et al ., 1996), two alleles of the gene encoding Drosophila SRF (Affolter et al ., 1994). Pruned affects the formation of the tracheal system by preventing terminal tracheal cells from projecting cytoplasmic outgrowths.…”

Unravelling the distinct contribution of cell shape changes and cell intercalation to tissue morphogenesis: the case of the Drosophila trachea

“…We also examined the activity of the Bnl/Btl pathway in Rab5 DN dorsal branches, as this pathway provides the pulling force for dorsal branch extension and cell intercalation [9,[11][12][13]. The DSRF transcription factor and the Fascin/Singed actin-cross-linker, well-known targets of the Bnl/Btl pathway [14][15][16] were normally expressed at the tip of the Rab5 DN dorsal branches (figure 2d-g). In addition, we observed thin cell extensions in the tip cells corresponding to filopodia, as in the control (figure 2b,c).…”