InteractiveFly: GeneBrief

Exo84: Biological Overview | References

Gene name - Exo84

Synonyms -

Cytological map position- 96F10-96F10

Function - signaling

Keywords - exocyst complex subunit, apical polarity, polarized exocytosis, vesicular transport vesicles

Symbol - Exo84

FlyBase ID: FBgn0266668

Genetic map position - 3R: 21,875,452..21,877,957 [-]

Classification - Exocyst complex 84-kDa subunit Pleckstrin Homology (PH) domain

Cellular location - cytoplasmic

NCBI link: EntrezGene

Exo84 orthologs: Biolitmine

The polarized architecture of epithelial tissues involves a dynamic balance between apical and basolateral membrane domains. This study shows that epithelial polarity in the Drosophila embryo requires the exocyst complex subunit homolog Exo84. Exo84 activity is essential for the apical localization of the Crumbs transmembrane protein, a key determinant of epithelial apical identity. Adherens junction proteins become mislocalized at the cell surface in Exo84 mutants in a pattern characteristic of defects in apical, but not basolateral, components. Loss of Crumbs from the cell surface precedes the disruption of Bazooka and Armadillo localization in Exo84 mutants. Moreover, Exo84 mutants display defects in apical cuticle secretion that are similar to crumbs mutants and are suppressed by a reduction in the basolateral proteins Dlg and Lgl. In Exo84 mutants at advanced stages of epithelial degeneration, apical and adherens junction proteins accumulate in an expanded recycling endosome compartment. These results suggest that epithelial polarity in the Drosophila embryo is actively maintained by exocyst-dependent apical localization of the Crumbs transmembrane protein (Blankenship, 2007).

Epithelial cells in the Drosophila embryo generate molecularly distinct apical and basolateral surfaces that provide structural integrity to the developing embryo. Specialized cell surface domains are separated by intercellular adherens junctions that initiate as diffuse apicolateral accumulations and subsequently coalesce to form a discrete apical band called the zonula adherens. The spatial organization of mature adherens junctions is actively maintained by input from both apical and basolateral proteins. The Crumbs EGF-repeat transmembrane protein and its cytoplasmic binding partners Stardust and PATJ localize to the apical cell surface and are required for epithelial structure and adherens junction morphology. In addition, overexpression of Crumbs leads to a selective expansion of the apical cell surface, demonstrating that Crumbs is necessary and sufficient for apical identity. The localization of mature adherens junctions also requires the basolateral PDZ-domain proteins Discs large (Dlg) and Scribble (Scrib) and the WD40-domain protein Lethal giant larvae (Lgl) Epithelial defects caused by disruption of apical Crumbs activity can be rescued by a simultaneous reduction in the activity of basolateral proteins, indicating that apical and basolateral domains function in opposition to maintain epithelial polarity (Blankenship, 2007 and references therein).

Misregulation of Crumbs activity can have severe effects on cell and tissue function and is associated with human retinal diseases. Multiple mechanisms contribute to Crumbs localization, stability and activity to precisely control its function. The basolateral proteins Dlg, Lgl and Scrib oppose Crumbs activity and restrict its localization in the Drosophila embryo, and the Yurt FERM-domain protein associates with the Crumbs cytoplasmic domain and negatively regulates Crumbs activity at the apicolateral cell surface. Endocytosis of Crumbs protein is also required for tissue morphology; mutations in the Avalanche syntaxin or the Rab5 GTPase lead to Crumbs accumulation and wing imaginal disc overgrowth (Lu, 2005). In addition, a complex containing the Rich1 Cdc42 GAP protein and the angiomotin scaffolding protein associates with cytoplasmic binding partners of Crumbs and provides a potential link between the Crumbs complex and the endocytic machinery (Wells, 2006). However, the mechanisms that govern the delivery of Crumbs protein to the cell surface are not known (Blankenship, 2007).

The targeting of transmembrane proteins to specific destinations at the cell surface is a widely used mechanism for establishing cell polarity. The spatial specificity of vesicle trafficking is thought to occur at a late step in this process through the tethering of exocytic vesicles at defined membrane sites by the eight-subunit exocyst (or Sec6/8) complex (Lipschutz, 2002; Whyte, 2002). Exocyst components were originally identified based on their role in polarized secretion in Saccharomyces cerevisiae and were subsequently shown to form a complex that is highly conserved from yeast to mammals. In multicellular organisms, exocyst components are required for multiple developmental processes including epithelial polarity, membrane integrity, photoreceptor morphogenesis, cell fate determination and synapse formation. These diverse functions demonstrate that polarized exocytosis is a fundamental mechanism for regulating cell morphology (Blankenship, 2007).

This study provided evidence that the Drosophila homolog of the Exo84 exocyst complex subunit is essential for epithelial polarity and apical protein localization in the Drosophila embryo. In Exo84 mutants, adherens junction proteins become mislocalized along the apical-basal axis in a manner reminiscent of cells lacking the Crumbs apical determinant. Loss of Crumbs from the apical surface is the earliest defect detected in Exo84 mutants. Exo84 mutants at advanced stages of epithelial degeneration display defects in trafficking apical and junctional proteins from the recycling endosome to the cell surface. These results demonstrate that the Drosophila homolog of the exocyst complex subunit Exo84 plays an essential role in epithelial polarity by regulating the localization of the Crumbs apical determinant (Blankenship, 2007).

It is concluded that epithelial polarity in the Drosophila embryo is actively maintained by the Exo84-dependent localization of the Crumbs transmembrane protein to the apical surface. Exo84 mutants display an aberrant distribution of junctional proteins that resembles the phenotype of crumbs mutants, and depletion of Crumbs from the apical surface is the earliest defect detected in Exo84 mutants. In addition, the onset of epithelial disruption at stage 9 in Exo84 mutants is comparable with the timing of the crumbs mutant defects, and the Crumbs protein still aggregates in Exo84 embryos with greatly reduced E-cadherin. Exo84 is likely to function as part of the exocyst complex in the Drosophila embryo, in light of the genetic interactions observed between Exo84 and the Sec5 and Sec6 exocyst subunits and the common defects in recycling endosome morphology caused by exocyst disruption in multiple cellular contexts (Jafar-Nejad, 2005; Langevin, 2005). These results suggest a role for exocyst-dependent membrane trafficking in the maintenance of apical epithelial identity in the Drosophila embryo (Blankenship, 2007).

In contrast to the relatively specific mislocalization of Crumbs in stage 9 Exo84 mutant embryos, by late stage 10 these embryos display defects in the delivery of multiple proteins to the cell surface. Epithelial polarity and the distribution of apical and junctional proteins are established correctly in Exo84 mutants, either because these processes occur independently of Exo84 or because of residual Exo84 activity in this mutant background. The earliest defect observed in Exo84 mutants is a loss of Crumbs from the apical surface during epithelial maturation. As a likely consequence of the loss of cell-surface Crumbs localization, adherens junction proteins become mislocalized to varying positions along the basolateral cell membrane. Mutant embryos at later stages display a cytoplasmic accumulation of apical and adherens junction proteins in an expanded Rab11 recycling endosome compartment, consistent with a defect in vesicular transport to the cell surface. The failure to deliver junctional proteins to the cell surface is unlikely to result from a defect in Crumbs localization, because the cytoplasmic accumulation of junctional proteins does not occur in crumbs mutants. These results indicate that disruption of exocyst-dependent membrane trafficking ultimately results in the failure to deliver both apical and junctional proteins from the recycling endosome to the cell surface. The mislocalization of apical and junctional proteins in Exo84 mutant embryos is associated with a loss of columnar morphology, demonstrating that Exo84 activity is essential for epithelial organization (Blankenship, 2007).

A precise balance between apical and basolateral determination is essential for epithelial integrity and the placement of the zonula adherens in the Drosophila embryo. This balance is actively maintained by Exo84-dependent localization of the Crumbs transmembrane protein to the apical cell surface. Loss of apical or basolateral identity leads to distinct patterns of junctional protein distribution, suggesting that the apical and basal limits of the zonula adherens are defined by different mechanisms. In crumbs mutants, DE-cadherin and Armadillo are restricted to focused puncta at varying locations at the cell surface. By contrast, in embryos defective for the basolateral proteins Dlg and Lgl, junctional proteins are dispersed along the plasma membrane rather than aggregating at a single site. A basolateral expansion of the apical Crumbs domain has also been reported in dlg and lgl mutants. These results suggest that basolateral proteins create a nonpermissive barrier to adherens junction expansion, whereas apical proteins may play a positive role in recruiting or stabilizing junctions at the apical cell surface. Consistent with this possibility, the apical Crumbs domain is closely apposed to the zonula adherens, and it was found that Bazooka and Armadillo colocalize at the cell surface and in the cytoplasm of Exo84 mutant embryos. Exocyst-dependent trafficking of Crumbs to the apical surface may reinforce the apical epithelial domain and stabilize the apicolateral localization of the zonula adherens (Blankenship, 2007).

The recycling endosome is the primary vesicular compartment affected in embryos mutant for the exocyst subunit homolog Exo84, while Golgi, early endosomal and late endosomal compartments remain largely intact. Exocyst proteins are required for recycling endosome morphology in several epithelial and sensory cell types (Jafar-Nejad, 2005; Langevin, 2005) and the Rab11 recycling endosome protein can associate directly with the exocyst subunits Sec5 and Sec15. It was found that Rab11 vesicles in maturing embryonic epithelia are enriched in the apical cytoplasm, where they preferentially accumulate in the plane of the adherens junctions. Conversely, a basal expansion of recycling endosomes during cellularization correlates with a basal bias in membrane addition. These results suggest that there is a spatial correlation between the sites of recycling endosome accumulation and the surface destinations of proteins trafficked through recycling endosomes. The redistribution of the recycling endosome compartment to the apical cytoplasm accompanies the transition from basolateral to apical membrane insertion and may reflect the onset of a critical requirement for Crumbs activity during epithelial maturation (Blankenship, 2007).

The requirement for Exo84 in apical protein localization in the Drosophila embryo is distinct from exocyst functions in other epithelia, in which exocyst components are required for the localization of basolateral or junctional proteins. The results indicate that Exo84 is also required for delivery of DE-cadherin to the cell surface in the embryo, consistent with the demonstrated roles for Sec5, Sec6 and Sec15 in DE-cadherin trafficking in the pupal epithelium (Langevin, 2005). However, although the mislocalization of the apical Crumbs protein is a primary defect of Exo84 mutant embryos, exocyst mutations do not appreciably affect Crumbs localization in pupal epithelial and photoreceptor cells (Beronja, 2005; Langevin, 2005). These results are consistent with a model in which distinct cargo proteins are trafficked by the exocyst complex in different cellular contexts. Alternatively, DE-cadherin and Crumbs may be delivered to the cell surface in an exocyst-dependent fashion in multiple cell types, but undergo different rates of turnover. For example, Crumbs may be dynamically trafficked in the embryo but stably maintained at the surface of pupal epithelial cells. Differential effects on specific target proteins are not atypical of exocyst function, because loss of Sec6 activity in Drosophila photoreceptor cells disrupts the localization of the rhabdomere proteins Chaoptin and Rhodopsin1, whereas the apical localization of Crumbs and DE-cadherin occurs normally (Beronja, 2005). The Drosophila embryonic epithelium undergoes pronounced changes in structure and organization during development that rely on a balance between apical and basolateral surface domains. A requirement for exocyst-dependent Crumbs trafficking during this process may facilitate the dynamic remodeling of epithelial polarity during morphogenesis (Blankenship, 2007).

Phosphatidylinositol 4,5-bisphosphate regulates cilium transition zone maturation in Drosophila melanogaster

Cilia are cellular antennae that are essential for human development and physiology. A large number of genetic disorders linked to cilium dysfunction are associated with proteins that localize to the ciliary transition zone (TZ), a structure at the base of cilia that regulates trafficking in and out of the cilium. Despite substantial effort to identify TZ proteins and their roles in cilium assembly and function, processes underlying maturation of TZs are not well understood. This study reports a role for the membrane lipid phosphatidylinositol 4,5-bisphosphate (PIP2) in TZ maturation in the Drosophila melanogaster male germline. Reduction of cellular PIP2 levels by ectopic expression of a phosphoinositide phosphatase or mutation of the type I phosphatidylinositol phosphate kinase Skittles induces formation of longer than normal TZs. These hyperelongated TZs exhibit functional defects, including loss of plasma membrane tethering. It is also reported that the onion rings (onr) allele of Drosophila exo84 decouples TZ hyperelongation from loss of cilium-plasma membrane tethering. These results reveal a requirement for PIP2 in supporting ciliogenesis by promoting proper TZ maturation (Gupta, 2018).

Cilia are sensory organelles important for signalling in response to extracellular cues, and for cellular and extracellular fluid motility. Consistent with their importance, defects in cilium formation (i.e. ciliogenesis) are associated with genetic disorders known as ciliopathies, which can display neurological, skeletal and fertility defects, in addition to other phenotypes. Many ciliopathies are associated with mutations in proteins that localize to the transition zone (TZ), the proximal-most region of the cilium that functions as a diffusion barrier and regulates the bidirectional transport of protein cargo at the cilium base. For example, the conserved TZ protein CEP290 is mutated in at least six different ciliopathies and is important for cilium formation and function in humans and Drosophila (Basiri, 2014). Although the protein composition of TZs has been investigated in various studies, the process of TZ maturation, through which it is converted from an immature form to one competent at supporting cilium assembly, is relatively understudied (Gupta, 2018).

Ciliogenesis begins with assembly of a nascent TZ at the tip of the basal body (BB). During TZ maturation, its structure and protein constituents change, allowing for establishment of a compartmentalized space, bounded by the ciliary membrane and the TZ, where assembly of the axoneme, a microtubule-based structure that forms the ciliary core, and signalling can occur. In Drosophila, nascent TZs first assemble on BBs during early G2 phase in primary spermatocytes. This occurs concomitantly with anchoring of cilia to the plasma membrane (PM), microtubule remodelling within the TZ, and establishment of a ciliary membrane that will persist through meiosis (Gupta, 2018).

TZ maturation has been described in Paramecium, Caenorhabditis elegans and Drosophila (Gottardo, 2013), and is most readily observed in the Drosophila male germline by an increase in TZ length. Previous work has shown that the membrane lipid phosphatidylinositol 4,5-bisphosphate (PIP2) is essential for proper axoneme structure in the Drosophila male germline. PIP2, which is one of seven different phosphoinositides (PIPs) present in eukaryotes, localizes primarily to the PM, where it is required for vesicle trafficking among other processes. PIP2 has recently been linked to cilium function. Although the ciliary membrane contains very little PIP2 due to action of the cilium resident PIP phosphatase INPP5E, the cilium base is enriched in PIP2. Inactivation of INPP5E causes a buildup of intraciliary PIP2, which disrupts transport of Hedgehog signalling proteins in vertebrates and ion channels involved in mechanotransduction in Drosophila (Park, 2015). In light of current understanding of PIP2 as a modulator of cilium function, this study sought to investigate the cause of defects observed in axoneme assembly in Drosophila male germ cells with reduced levels of PIP2 (Gupta, 2018).

To investigate how reduction of cellular PIP2 affects ciliogenesis in the Drosophila male germline, transgenic flies were used expressing the Salmonella PIP phosphatase SigD under control of the spermatocyte-specific β2-tubulin promoter (hereafter β2t-SigD). To examine whether axoneme defects in β2t-SigD were caused by aberrant TZ function, localization of fluorescently-tagged versions of the core centriolar/BB protein Ana1 (CEP295 homolog) and the conserved TZ protein Cep290 was analyzed during early steps of cilium assembly. Cep290 distribution appeared similar in control and β2t-SigD in early G2 phase, when TZs are still immature. In contrast, Cep290-labelled TZs were significantly longer in β2t-SigD compared to controls by late G2, following TZ maturation. Unlike Drosophila cep290 mutants, which contain longer than normal BBs, Ana1 length was not affected in β2t-SigD, and no strong correlation was observed between Cep290 and Ana1 lengths. Consistent with this result, the ultrastructure of BBs in β2t-SigD is normal, and localization of the centriolar marker GFP-PACT is similar in controls and β2t-SigD. In contrast, TZ proteins Chibby (Cby) and Mks1 exhibited hyperelongation in β2t-SigD, indicating that this phenotype is not unique to Cep290. TZ hyperelongation was highly penetrant (>70%, n >200) and showed high correlation (>0.95) within syncytial germ cell cysts, suggesting a dosage-based response to a shared cellular factor, presumably SigD. Despite persistence of hyperelongated TZs through meiosis, axonemes were able to elongate in post-meiotic cells. Nonetheless, the ultrastructure of these axonemes is frequently aberrant, either lacking nine-fold symmetry or containing triplet microtubules in addition to the usual doublets (Gupta, 2018).

Although PIP2 is its major substrate in eukaryotic cells in vivo, SigD can dephosphorylate multiple PIPs in vitro. To address whether TZ hyperelongation observed in β2t-SigD represented a physiologically relevant phenotype due to decreased PIP2, attempts were made to rescue this phenotype by co-expressing β2t-SigD with fluorescently-tagged Skittles (Sktl) under control of the β2- tubulin promoter. Sktl expression was able to suppress TZ hyperelongation to various degrees in a cilium-autonomous manner. Furthermore, the BB/TZ protein Unc-GFP exhibited TZ hyperelongation at a low penetrance in sktl2.3 mutant clones, indicating that Sktl is important for TZ maturation. Vertebrate type I PIP kinase PIPKIγ is important for cilium formation in cultured cells. The Drosophila PIPKIs, Sktl and PIP5K59B, arose from recent duplication of the ancestral PIPKI gene, and are not orthologous to specific vertebrate PIPKI isoforms. Sktl has diverged more than its paralog PIP5K59B and seems to be functionally related to PIPKIγ and the C. elegans PPK-1 in having roles at cilia. However, unlike the human PIPKIγ, which licenses TZ assembly by promoting CP110 removal from BBs, the current results suggest that Sktl functions in regulating TZ length but not TZ assembly. Consistent with this, neither inactivation nor overexpression of cp110 affects cilium formation in Drosophila, and Cp110 is removed from BBs in early primary spermatocytes (Gupta, 2018).

Attempts were made to examine whether TZ hyperelongation due to SigD expression affected TZ function. Following meiosis in the Drosophila male germline, TZs detach from BBs and migrate along growing axonemes, maintaining a ciliary compartment at the distal-most ~2μm, where tubulin is incorporated into the axoneme. As shown by Unc and Cep290 localization, TZs in β2t-SigD were frequently incapable of detaching from BBs and migrating along axonemes despite axoneme and cell elongation. Indeed, the previously reported 'comet-shaped' Unc-GFP localization in β2t-SigD persists during cell elongation after meiosis despite elongation of the axoneme (Gupta, 2018).

In Drosophila and humans, BBs consist of microtubule triplets, whereas axonemes contain microtubule doublets due to termination of C-tubules at the TZ (Gottardo, 2013). Consistent with a defect in this transition and the presence of microtubule triplets in axonemes in β2t-SigD, a subset of cilia (<5%) in β2t-SigD contained puncta of Ana1 at the distal tips of TZs. Treatment of germ cells with the microtubule-stabilizing drug Taxol increased penetrance of this phenotype from <5% in untreated cells to >25% in cells treated with 4 μM Taxolwithout significantly affecting Cep290 length. Taxol-treated controls did not exhibit TZ- distal Ana1 puncta. Fluorescently-tagged Asterless (CEP152 homolog), a pericentriolar protein, did not localize to TZ-distal puncta in β2t-SigD suggesting these TZ-distal sites are not fully centriolar in protein composition. Taxol has been hypothesized to disrupt TZ maturation by inhibiting microtubule remodelling in the Drosophila male germline (Riparbelli, 2013). Indeed, similar to β2t-SigD, Taxol-treated male germ cells assemble long axonemes that contain triplet microtubules (Riparbelli, 2013), further supporting a functional relationship between PIP2 and microtubule reorganization in TZ maturation (Gupta, 2018).

Male flies homozygous for the onion rings (onr) mutant of Drosophila exo84 are sterile and exhibit defects in cell elongation and polarity similar to β2t-SigD. Exo84 is a component of the octameric exocyst complex, which binds PIP2 at the PM. To investigate whether defects in TZ hyperelongation could be explained by defective Exo84 function, TZs were examined in onr mutants. Unlike β2t-SigD, onr did not display hyperelongated TZs, suggesting Exo84 is dispensable for TZ maturation. Due to involvement of the exocyst in membrane trafficking, whether cilium- associated membranes were affected in β2t-SigD or onr mutants in a manner similar to dilatory; cby mutants (Vieillard, 2016) was examined. Dilatory (Dila), a conserved TZ protein, cooperates with Cby to assemble TZs in the Drosophila male germline (Vieillard, 2016). TZs in β2t-SigD and onr cells were able to dock at the PM initially, but were unable to maintain membrane connections, and were rendered cytoplasmic, similar to TZs in dila; cby mutants. In addition, fluorescently-tagged Exo70, a PIP2-binding exocyst subunit, localized to BBs. The current results suggest that the exocyst, and Exo84 in particular, regulates cilium-PM association, similar to PIP2, and that TZ hyperelongation and loss of cilium-PM association are genetically separable phenotypes (Gupta, 2018).

Maturation of a TZ from a nascent to a fully functional state, leading ultimately to axoneme assembly and ciliary signalling, requires orchestration of various proteins and cellular pathways. The current results indicate that normal execution of this process requires PIP2, and that depletion of PIP2 induces TZs to grow longer than normal. Similar to β2t-SigD, Drosophila dila; cby and cby mutants display hyperelongated TZs, whereas mks1 mutants have shorter TZs. Because both Cby and Mks1 are hyperelongated in β2t-SigD cells, PIP2 regulates TZ length independently of an effect on Cby or Mks1 recruitment. This study shows that hyperelongated TZs are dysfunctional. Similar to dila; cby (Vieillard, 2016) and cep290 (Basiri, 2014) mutants, axonemes can assemble in β2t-SigD, albeit with aberrant ultrastructure, despite lack of functional TZs or membrane association. The presence of TZ-distal Ana1 puncta in β2t-SigD, without the increase in BB length seen in cep290 mutants lacking a functional TZ barrier, suggests that β2t-SigD selectively disrupts the ability of TZs to restrict C-tubules and Ana1 without abolishing the TZ barrier entirely. CEP295, the human Ana1 ortholog, regulates post-translational modification of centriolar microtubules, which might explain the presence of TZ-distal Ana1 along with supernumerary microtubules in β2t-SigD cells. Asterless (Asl), a pericentriolar protein important for centrosome formation and centriole duplication, did not exhibit this TZ-distal localization, possibly due to differences in dynamics of Ana1 and Asl loading onto centrioles or the more peripheral nature of Asl distribution within the centriole (Gupta, 2018).

The majority of PIP2 at the PM is produced by PIPKIs. Mutation of the PIPKI Sktl induced hyperelongated TZs, and expression of Sktl could suppress TZ hyperelongation in β2t-SigD, suggesting Sktl might function in situ to regulate TZ length. In humans, PIPKIC is linked to lethal congenital contractural syndrome type 3 (LCCS3), which has been suggested to represent a ciliopathy. The recent discovery of a role for another LCCS-associated protein in cilium function corroborates this hypothesis. The current data support the idea that PIPKIs might represent ciliopathy-associated genes or genetic modifiers of disease. Members of the exocyst complex are important for cilium formation in cultured cell lines and zebrafish, but their precise roles in ciliogenesis are not well understood. The subunits Sec3 and Exo70 regulate exocyst targeting to the PM through a direct interaction with PIP2. Previous work has shown that the onr allele of Drosophila exo84 phenocopies defects in cell polarity and elongation observed in β2t-SigD. This study showed that the onr mutation phenocopies loss of cilium-membrane contacts in β2t-SigD but not TZ hyperelongation. Thus, TZ hyperelongation is not a prerequisite for failure of cilium-PM association in male germ cells, and Exo84 uniquely regulates the latter process, potentially by supplying membrane required to maintain cilium-PM tethering. That the TZ is dispensable for this function is supported by the Drosophila cep290 mutant, which lacks a functional TZ but retains cilium-PM association. Notably, EXOC8, which encodes the human Exo84, has been linked to the ciliopathy Joubert syndrome, and a similar defect in ciliogenesis might be present in humans with mutations in EXOC8 (Gupta, 2018).


Search PubMed for articles about Drosophila Exo84

Basiri, M. L., Ha, A., Chadha, A., Clark, N. M., Polyanovsky, A., Cook, B. and Avidor-Reiss, T. (2014). A migrating ciliary gate compartmentalizes the site of axoneme assembly in Drosophila spermatids. Curr Biol 24(22): 2622-2631. PubMed ID: 25447994

Beronja, S., Laprise, P., Papoulas, O., Pellikka, M., Sisson, J. and Tepass, U. (2005). Essential function of Drosophila Sec6 in apical exocytosis of epithelial photoreceptor cells. J. Cell Biol. 169(4): 635-46. PubMed ID: 15897260

Blankenship, J. T., Fuller, M. T. and Zallen, J. A. (2007). The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity. J. Cell Sci. 120: 3099-3110. PubMed ID: 17698923

Gottardo, M., Callaini, G. and Riparbelli, M. G. (2013). The cilium-like region of the Drosophila spermatocyte: an emerging flagellum? J Cell Sci 126(Pt 23): 5441-5452. PubMed ID: 24105264

Gupta, A., Fabian, L. and Brill, J. A. (2018). Phosphatidylinositol 4,5-bisphosphate regulates cilium transition zone maturation in Drosophila melanogaster. J Cell Sci 131(16). PubMed ID: 30054387

Jafar-Nejad, H., Andrews, H. K., Acar, M., Bayat, V., Wirtz-Peitz, F., Mehta, S. Q., Knoblich, J. A. and Bellen, H. J. (2005). Sec15, a component of the exocyst, promotes notch signaling during the asymmetric division of Drosophila sensory organ precursors. Dev. Cell 9(3): 351-63. PubMed ID: 16137928

Langevin, J., et al. (2005). Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane. Dev. Cell 9(3): 355-76. PubMed ID: 16224820

Lipschutz, J. H. and Mostov, K. E. (2002). Exocytosis: the many masters of the exocyst. Curr. Biol. 12: 212-214. PubMed ID: 9136678

Lu, H. and Bilder, D. (2005). Endocytic control of epithelial polarity and proliferation in Drosophila. Nat. Cell Biol. 7: 1232-1239. PubMed ID: 16258546

Park, J., Lee, N., Kavoussi, A., Seo, J. T., Kim, C. H. and Moon, S. J. (2015). Ciliary Phosphoinositide Regulates Ciliary Protein Trafficking in Drosophila. Cell Rep 13(12): 2808-2816. PubMed ID: 26723017

Riparbelli, M. G., Cabrera, O. A., Callaini, G. and Megraw, T. L. (2013). Unique properties of Drosophila spermatocyte primary cilia. Biol Open 2(11): 1137-1147. PubMed ID: 24244850

Vieillard, J., Paschaki, M., Duteyrat, J. L., Augiere, C., Cortier, E., Lapart, J. A., Thomas, J. and Durand, B. (2016). Transition zone assembly and its contribution to axoneme formation in Drosophila male germ cells. J Cell Biol 214(7): 875-889. PubMed ID: 27646273

Wells, C. D., Fawcett, J. P., Traweger, A., Yamanaka, Y., Goudreault, M., Elder, K., Kulkarni, S., Gish, G., Virag, C., Lim, C., et al. (2006). Rich1/Amot complex regulates the Cdc42 GTPase and apical-polarity proteins in epithelial cells. Cell 125: 535-548. PubMed ID: 16678097

Whyte, J. R. and Munro, S. (2002). Vesicle tethering complexes in membrane traffic. J. Cell Sci. 115: 2627-2637. PubMed ID: 12077354

Biological Overview

date revised: 13 December 2018

Home page: The Interactive Fly © 2007 Thomas Brody, Ph.D.

The Interactive Fly resides on the
Society for Developmental Biology's Web server.