Septate junctions are required for ommatidial integrity and blood–eye barrier function in Drosophila

Abstract

The anatomical organization of the Drosophila ommatidia is achieved by specification and contextual placement of photoreceptors, cone and pigment cells. The photoreceptors must be sealed from high ionic concentrations of the hemolymph by a barrier to allow phototransduction. In vertebrates, a blood-retinal barrier (BRB) is established by tight junctions (TJs) present in the retinal pigment epithelium and endothelial membrane of the retinal vessels. In Drosophila ommatidia, the junctional organization and barrier formation is poorly understood. Here we report that septate junctions (SJs), the vertebrate analogs of TJs, are present in the adult ommatidia and are formed between and among the cone and pigment cells. We show that the localization of Neurexin IV (Nrx IV), a SJ-specific protein, coincides with the location of SJs in the cone and pigment cells. Somatic mosaic analysis of nrx IV null mutants shows that loss of Nrx IV leads to defects in ommatidial morphology and integrity. nrx IV hypomorphic allelic combinations generated viable adults with defective SJs and displayed a compromised blood-eye barrier (BEB) function. These findings establish that SJs are essential for ommatidial integrity and in creating a BEB around the ion and light sensitive photoreceptors. Our studies may provide clues towards understanding the vertebrate BEB formation and function.

Developmental changes in β-subunit composition of Na,K-ATPase in the Drosophila eye

“…These sites corresponded to the location of septate junctions as visualized by staining for neurexin-IV (Fig. 4c, f, i), a marker for septate junctions (Baumgartner et al 1996;Banerjee et al 2008). Anti-α, in contrast, provided only faint labeling at these sites in pigment cells and cone cells (Fig.…”

“…In cone cells and pigment cells, the α-subunit and Nrv2 were localized on the basolateral membrane domain, with an enrichment apicolaterally (Fig. 7h, i) at the sites of septate junctions (Banerjee et al 2008). During the second half of pupal life, Nrv2 staining faded on the plasma membrane of the photoreceptor cells and the cytoplasmic staining for Nrv2 was particulate (Fig.…”

“…3b, e). Since the visual cells have no septate junctions (Banerjee et al 2008) but stain intensely with anti-α, we consider that the epitope for anti-α is masked in case of α-subunit at septate junctions.…”

The transmembrane protein Macroglobulin complement-related is essential for septate junction formation and epithelial barrier function inDrosophila

“…SJs are large multiprotein complexes containing cytoplasmic and integral membrane proteins, several of which were identified through genetic screens in Drosophila (reviewed by Furuse and Tsukita, 2006;Banerjee et al, 2008). Two distinct subtypes of SJs are known: pleated SJs (pSJs) are found in ectodermal organs (epidermis, salivary glands, foregut, hindgut, tracheal system), whereas the ultrastructurally distinct smooth SJs (sSJs) form epithelial barriers in endodermal organs, such as the midgut (Tepass and Hartenstein, 1994).…”

Axonal Ensheathment and Intercellular Barrier Formation in Drosophila

“…Vertebrate astrocytes, microglia, oligodendrocytes, and Schwann cells have been recognized to perform specialized roles in nervous system development and function, and complementary subtypes of Drosophila glia have been identified which show a substantial overlap in function with each major category of vertebrate glia (Edwards and Meinertzhagen, 2010; Freeman and Doherty, 2006). Studies on Drosophila glia have provided insights into glial function that would be difficult or impossible to obtain from the study of vertebrate glia (Allen and Barres, 2009; Banerjee et al, 2006a, 2008; Jacobs and Goodman, 1989). In particular, the parallel roles of Drosophila ensheathing glia with vertebrate Schwann cells and oligodendrocytes suggest that the study of axonal ensheathment in Drosophila is directly relevant to vertebrate nervous system function.…”