Distinct roles of Bazooka and Stardust in the specification of Drosophila photoreceptor membrane architecture

Abstract

Photoreceptors form during Drosophila pupal development and acquire elaborate membrane structures, including the rhabdomeres and stalk membranes. Here, we show that the development of these cellular structures involves two distinct processes: the establishment of apical-basal polarity that requires Bazooka (Baz), and the regionalization of apical membrane into stalk membranes and rhabdomeres that requires Stardust (Sdt). In the absence of Baz, the apical-basal polarity is compromised in early pupal photoreceptors, and no identifiable apical membrane domain is formed. Sdt, in contrast, plays a more limited role in apical-basal polarity but is essential for the proper localization of transmembrane protein Crumbs (Crb), known to be required in the biogenesis of stalk membrane. Loss of Sdt causes strong defects in stalk membrane and rhabdomere resembling crb mutant phenotype. Thus, proteins required for establishing the early embryonic epithelial polarity are used later for the morphogenesis of photoreceptors, with Baz and Sdt functioning in different aspects of the formation of the apical-basal cellular architecture. D ifferent cell types exhibit different degrees of complexity in their morphogenesis. Epithelial cells are polarized to have distinct apical versus basolateral domains. Cascades of protein complexes have been found to specify this polarity (1). Many cells that are derived from epithelial cells have more complex morphology to carry out important functions, such as photoreceptors for vision. How these cells elaborate their different membrane domains is not well understood. In Drosophila, photoreceptors have clearly recognizable apical-basal polarity demarcated by zonula adherens (ZA) (2). Is this polarity established by the same protein complexes that specify epithelial polarity? How might this apical-basal polarity specification influence other structural specializations, e.g., the elaboration of rhabdomere perpendicular to the apical-basal axis? And, what are the mechanisms for regionalizing specific membrane domains in conjunction with the polarity?One approach to address these questions in Drosophila is to test whether similar organizations of genetic pathways in simple and relatively well studied embryonic epithelial polarity also underlie the development of polarity in more specialized cell types like photoreceptors. Drosophila embryonic epithelium represents one of the simplest polarized cell types, and its apical-basal polarity is controlled largely in concert by three protein complexes (1). Baz(DmPar-3)͞DmPar-6͞DaPKC (atypical protein kinase C) plays the earliest and essential role in initiating the apical-basal polarity, whereas Sdt͞Crb͞Dlt (Discs lost) maintains the ZA formation and polarity by counteracting the activity of Dlg (Discs large)͞Lgl (Lethal giant larvae)͞Scrib (Scribble) (3, 4). Except for DaPKC, Crumbs (Crb), and Lgl, all of these proteins contain one or more PDZ domains important for mediating protein-protein interactions (1). The first insight that at least some of these protei...

LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye

“…PRCs were frequently enlarged, and rhabdomeres were elongated (white arrowhead). These phenotypes are reminiscent of crb Ϫ/Ϫ clones in the retina (19,20). The lkb1 Ϫ/Ϫ phenotype could be rescued by transgenic expression of LKB1 (Fig.…”

“…The stalk domain was similarly affected in lkb1 mutant PRCs, as assessed by the stalk domain components, PatJ, Std, and Crb (Fig. S4) (19). The AJ marker Arm normally localizes just basal to the stalk membrane.…”

“…Developing ommatidia mutant for LKB1 lacked the regular size and shape seen in wild-type ommatidia. Members of the SAR complex (Crb, Std, and Patj) and members of the Par complex (aPKC, Baz, and Par-6) have similar defects in rhabdomere formation, resulting in mutant rhabdomeres that are often elongated, split, bulky, or fused (19,20,27,28). Because lkb1 adult PRC morphology resembled crb mutants, we tested whether PRC development was similarly affected.…”

Isoform‐specific interaction of Flamingo/Starry Night with excess Bazooka affects planar cell polarity in the Drosophila wing

“…In the forming blastoderm, the first epithelium in the Drosophila embryo to develop, Bazooka acts as an early apical cue required for positioning of the zonula adherens (ZA; Peifer, 2004, 2005). Similarly as in eye imaginal discs (Hong et al, 2003), however, cell clones in the wing imaginal discs homozygous mutant for the bazooka null allele baz Xi106 do not show any defect in apicobasal polarity ( Fig. 2A,B), as revealed by the proper localization of apical components, such as DaPKC ( Fig.…”

“…Unlike in the eye, neither loss of Bazooka nor reduction of DPATJ, which has been suggested to recruit DaPKC in the eye, has any effect on PCP development in the wing (this work and M. Richard and E. Knust, unpublished observations). The lack of any defect in apicobasal polarity in bazooka mutant cell clones in the wing or the eye imaginal disc (this work; Hong et al, 2003) is striking, given that it is absolutely required for the establishment of cell polarity in the embryo. In this respect, it does not differ from the behavior of crumbs or stardust mutant clones, which also develop normal apicobasal polarity in imaginal discs (Johnson et al, 2002;I.…”