Distinct roles for the actin and microtubule cytoskeletons in the morphogenesis of epidermal hairs during wing development in Drosophila

Abstract

We have found that the actin and microtubule cytoskeletons have overlapping, but distinct roles in the morphogenesis of epidermal hairs during Drosophila wing development. The function of both the actin and microtubule cytoskeletons appears to be required for the growth of wing hairs, as treatment of cultured pupal wings with either cytochalasin D or vinblastine was able to slow prehair extension. At higher doses a complete blockage of hair development was seen. The microtubule cytoskeleton is also required for localizing prehair initiation to the distalmost part of the cell. Disruption of the microtubule cytoskeleton resulted in the development of multiple prehairs along the apical cell periphery. The multiple hair cells were a phenocopy of mutations in the inturned group of tissue polarity genes, which are downstream targets of the frizzled signaling/signal transduction pathway. The actin cytoskeleton also plays a role in maintaining prehair integrity during prehair development as treatment of pupal wings with cytochalasin D, which inhibits actin polymerization, led to branched prehairs. This is a phenocopy of mutations in crinkled, and suggests mutations that cause branched hairs will be in genes that encode products that interact with the actin cytoskeleton.

DrosophilaMob Family Proteins Interact with the Related Tricornered (Trc) and Warts (Wts) Kinases

“…The function of trc and its partner furry (fry) is required for the development of epidermal hairs, sensory bristles, arista laterals, and dendrite arborization (da) sensory neuron dendrites (Geng et al, 2000;Cong et al, 2001;He and Adler, 2001;Emoto et al, 2004). The morphogenesis of these cell extensions involves the regulated activation of both the actin and microtubule cytoskeletons (Fristrom et al, 1993;Wong and Adler, 1993;Verheyen and Cooley, 1994;Eaton et al, 1996;Hopmann et al, 1996;Turner and Adler, 1998;Tilney et al, 2000;Geng et al, 2000;He and Adler, 2001). Mutations in trc and fry result in split and multipled hairs and laterals, split and deformed bristles and dendrites with extra branching and tiling defects (Geng et al, 2000;Cong et al, 2001;Emoto et al, 2004).…”

The flare Gene, Which Encodes the AIP1 Protein of Drosophila, Functions to Regulate F-Actin Disassembly in Pupal Epidermal Cells

“…Among the model systems used to study actin and cellular morphogenesis are epidermal hairs, denticles, laterals, and bristles of insects such as Drosophila (Wong and Adler 1993;Petersen et al 1994;Tilney et al 1995;Dickinson and Thatcher 1997;Turner and Adler 1998;Baum 2002). These structures have dramatically polarized and reproducible morphologies and their development involves prominent actin filaments/bundles.…”

“…Mutations in these genes result in bent, twisted, and shortened bristles, arista laterals, and epidermal hairs. In addition to actin, growing hairs and bristles also contain centrally located microtubules (Petersen et al 1994;Turner and Adler 1998;Tilney et al 2000;He and Adler 2002;He et al 2005).…”

“…The hairs produced by both flr and tsr wing cells are far more abnormal than those seen due to mutations in genes that encode actin bundling proteins (Bryan et al 1993;Petersen et al 1994), capping protein (Hopmann et al 1996;Hopmann and Miller 2003;Frank et al 2006), cytoplasmic myosins such as myosin VII (Turner and Adler 1998;Kiehart et al 2004), or other proteins thought to modulate actin polymerization, such as profilin (Verheyen and Cooley 1994) or Arp2/3 (Hudson and Cooley 2002) . The reason for this is uncertain and leads to the question as to what is the basis for the extreme flr phenotype?…”

Rapid tissue‐specific expression assay in living embryos

“…40% of the injected embryos (n ϭ 15) express CFP-actin in epidermal cells and CFP-actin accumulates at the base of the forming hairs, a site of actin bundling (Fig. 2a,b;Turner and Adler, 1998). No macrophages are labelled.…”