The shavenoid Gene of Drosophila Encodes a Novel Actin Cytoskeleton Interacting Protein That Promotes Wing Hair Morphogenesis

Abstract

The simple cellular composition and array of distally pointing hairs has made the Drosophila wing a favored system for studying planar polarity and the coordination of cellular-and tissue-level morphogenesis. The developing hairs are filled with F-actin and microtubules and the activity of these cytoskeletons is important for hair morphogenesis. On the basis of mutant phenotypes several genes have been identified as playing a key role in stimulating hair formation. Mutations in shavenoid (sha) (also known as kojak) result in a delay in hair morphogenesis and in some cells forming no hair and others several small hairs. We report here the molecular identification and characterization of the sha gene and protein. sha encodes a large novel protein that has homologs in other insects, but not in more distantly related organisms. The Sha protein accumulated in growing hairs and bristles in a pattern that suggested that it could directly interact with the actin cytoskeleton. Consistent with this mechanism of action we found that Sha and actin co-immunopreciptated from wing disc cells. The morphogenesis of the hair involves temporal control by sha and spatial control by the genes of the frizzled planar polarity pathway. We found a strong genetic interaction between mutations in these genes consistent with their having a close but parallel functional relationship.

SoxNeuro and shavenbaby act cooperatively to shape denticles in the embryonic epidermis of Drosophila

“…For example, Svb directs the expression of forked, which encodes an actin-bundling protein that functions in denticle and dorsal hair formation (Chanut-Delalande et al, 2006) as well as in adult bristle formation (Grieshaber and Petersen, 1999). The genes singed (Cant et al, 1994) and shavenoid (Ren et al, 2006) are also controlled by Svb, and function during embryogenesis in actin dynamics and denticle formation. Other proteins that function in cytoskeletal dynamics, such as Diaphanous, Enabled and Arp2/3, are not influenced by Svb activity but localize to denticles and aid in their construction.…”

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

“…The activity of the fz-based planar/tissue polarity system restricts hair initiation to the distal-most part of the apical surface of cells (Wong and Adler 1993). Temporal control of hair initiation is likely to involve the turn on of expression of shavenoid/kojak (He and Adler 2002;Ren et al 2006), perhaps due to its expression being regulated by the shavenbaby and/or grainy head transcription factors (Lee and Adler 2004;Chanut-Delalande et al 2006). The planar cell polarity (PCP) proteins are known to become restricted to the proximal and distal sides of cells and it is generally believed that feedback interactions between these proteins lead to the formation of these two protein domains (Tree et al 2002;Amonlirdviman et al 2005).…”

The Balance Between the Novel Protein Target of Wingless and the Drosophila Rho-Associated Kinase Pathway Regulates Planar Cell Polarity in the Drosophila Wing

“…The sha gene encodes a putative actin-binding protein whose expression increases dramatically just prior to hair initiation (Ren et al 2006). Consistent with the expression of sha playing a key role in regulating hair initiation, sha mutant wing cells either fail to form a hair or have delayed hair formation.…”

“…Mutations in sha result in a delay in hair morphogenesis and, in some cells, no hair or only several small hairs form (He and Adler 2002). The morphogenesis of the hair involves temporal control by sha and spatial control by the genes of the Fz pathway, and there is a strong genetic interaction between mutations in these genes (Ren et al 2006). tow mutation caused an increased number of small hairs and multiple wing hairs in the hypomorphic sha VB13 background ( Figure 5, C and D).…”