Lumenal Transmission of Decapentaplegic in Drosophila Imaginal Discs

Abstract

Drosophila imaginal discs are sac-like appendage primordia comprising apposed peripodial and columnar cell layers. Cell survival in disc columnar epithelia requires the secreted signal Decapentaplegic (DPP), which also acts as a gradient morphogen during pattern formation. The distribution mechanism by which secreted DPP mediates global cell survival and graded patterning is poorly understood. Here we report detection of DPP in the lumenal cavity between apposed peripodial and columnar cell layers of both wing and eye discs. We show that peripodial cell survival hinges upon DPP signal reception and implicate DPP-dependent viability of the peripodial epithelium in growth of the entire disc. These results are consistent with lumenal transmission of the DPP survival signal during imaginal disc development.

Apical and lateral cell protrusions interconnect epithelial cells in live Drosophila wing imaginal discs

“…The location and connectivity of apical protrusions (columnar cells to squamous cells) and lateral protrusions (columnar cells to columnar cells) makes them well suited to play a role in the exchange of such signaling molecules. Dpp is a member of the transforming growth factor-␤ family of secreted molecules that is important for the growth and patterning of wing imaginal discs (Spencer et al, 1982;Padgett et al, 1987;Capdevila and Guerrero, 1994;Zecca et al, 1995) and that has been shown to be present in the lumen between columnar cells and squamous cells (Gibson et al, 2002). To test whether apical or lateral protrusions could mediate the communication between cells by displaying a receptor for Dpp, we expressed a GFP-tagged version of the Dpp receptor Thickveins (Tkv; Hsiung et al, 2005) in the dorsal compartment of columnar wing imaginal disc cells.…”

“…Cells of the squamous and columnar epithelium exchange signals that are important for the growth and patterning of wing imaginal discs (Cho et al, 2000;Gibson and Schubiger, 2000;Gibson et al, 2002;Shashidhara, 2003, 2005). Cells of the squamous epithelium display long microtubule-based protrusions directed toward the columnar epithelium (Cho et al, 2000;Gibson and Schubiger, 2000).…”

Regulation and activity of JNK signaling in the wing disc peripodial membrane during adult morphogenesis in Drosophila

“…During metamorphosis, cells of PM may play an active role through the dramatic change of their shape, either by intensive stretching or contraction (Fristrom andFristrom, 1993, Milner et al, 1984). Earlier reports have established a signaling role for PM in patterning DP during wing morphogenesis (Cho et al, 2000;Gibson and Schubiger, 2000;Gibson et al, 2002;Pallavi andShashidhara, 2003, 2005;Pastor-pareja et al, 2004).…”

Position matters: Variability in the spatial pattern of BMP modulators generates functional diversity

“…This difference derives in part from the pattern of Dpp protein distribution. Several labs have used fluorescently tagged forms of Dpp (Dpp-GFP) to investigate behavior of Dpp protein in fixed and live tissue (Entchev et al, 2000;Gibson et al, 2002;Teleman and Cohen, 2000;Wang and Ferguson, 2005). There have been reports using antibodies against Dpp (Gibson et al, 2002;Sato et al, 2010) and high levels of BMP activity can be detected with antibodies against phosphorylated Mad (pMad; Dorfman and Shilo, 2001;Eldar et al, 2002;Mizutani et al, 2005;Ross et al, 2001;Shimmi and O'Connor, 2003;Tanimoto et al, 2000;Teleman and Cohen, 2000), a SMAD protein activated by phosphorylation upon binding of BMPs to transmembrane receptors (Fig.…”

“…However, the range of dpp action is broader than the mRNA expression domain, as revealed by dpp mutants that lead to loss of target gene expression far from the source (Lecuit et al, 1996;Nellen et al, 1996). Spread of Dpp protein in anterior (A) and posterior (P) directions generates a long-range gradient of the Dpp morphogen from the center to lateral regions of the disc (Entchev et al, 2000;Gibson et al, 2002;Lecuit et al, 1996;Nellen et al, 1996;Teleman and Cohen, 2000). Genes such as omb and spalt respond to different levels of Dpp, leading to the positioning of provein territories and ultimately the location of longitudinal veins (reviewed in Affolter and Basler, 2007;O'Connor et al, 2006).…”