Cadherin Cad99C is required for normal microvilli morphology in Drosophila follicle cells

Schlichting, Karin; Wilsch‐Bräuninger, Michaela; Demontis, Fabio; Dahmann, Christian

doi:10.1242/jcs.02831

Cited by 62 publications

(65 citation statements)

References 60 publications

(77 reference statements)

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“…One could speculate that close apposition of membranes through E-Cad-dependent adhesion somehow stabilizes protrusions, possibly by allowing specific contacts between protrusions. In epithelia, intermicrovillar adhesion is assured by protocadherins (48)(49)(50), and although any requirement for microvilli remains to be demonstrated, we envisage that they reinforce RCs anchorage. This remote action of E-Cad is somewhat reminiscent of another E-Cad function during oogenesis: E-Cad clusters at the nurse cells' PM control the orientation of the filopodia-like actin cables that position nuclei during later stages of oogenesis.…”

Section: Discussionmentioning

confidence: 75%

Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth

Loyer

Kolotuev

Pinot

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Intercellular bridges called "ring canals" (RCs) resulting from incomplete cytokinesis play an essential role in intercellular communication in somatic and germinal tissues. During Drosophila oogenesis, RCs connect the maturing oocyte to nurse cells supporting its growth. Despite numerous genetic screens aimed at identifying genes involved in RC biogenesis and maturation, how RCs anchor to the plasma membrane (PM) throughout development remains unexplained. In this study, we report that the clathrin adaptor protein 1 (AP-1) complex, although dispensable for the biogenesis of RCs, is required for the maintenance of the anchorage of RCs to the PM to withstand the increased membrane tension associated with the exponential tissue growth at the onset of vitellogenesis. Here we unravel the mechanisms by which AP-1 enables the maintenance of RCs' anchoring to the PM during size expansion. We show that AP-1 regulates the localization of the intercellular adhesion molecule E-cadherin and that loss of AP-1 causes the disappearance of the E-cadherin-containing adhesive clusters surrounding the RCs. E-cadherin itself is shown to be required for the maintenance of the RCs' anchorage, a function previously unrecognized because of functional compensation by N-cadherin. Scanning block-face EM combined with transmission EM analyses reveals the presence of interdigitated, actin-and Moesin-positive, microvilli-like structures wrapping the RCs. Thus, by modulating E-cadherin trafficking, we show that the sustained E-cadherin-dependent adhesion organizes the microvilli meshwork and ensures the proper attachment of RCs to the PM, thereby counteracting the increasing membrane tension induced by exponential tissue growth.

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Section: Discussionmentioning

confidence: 75%

Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth

Loyer

Kolotuev

Pinot

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Nine expression patterns were identified in the follicle cells throughout all stages of oogenesis, five of which are newly reported: fat2 , Cad86C , Cad87A , Cad88C and cals . Expression patterns for two genes, Cad74A and Cad99C were reported in the literature previously (D'Alterio et al, 2005; Schlichting et al, 2006; Zartman et al, In Press). Finally, expression of DE-Cad and DN-Cad were examined earlier, but later stages of mRNA expression were not previously shown explicitly (Becam et al, 2005; Godt and Tepass, 1998; Niewiadomska et al, 1999; Schnorr and Berg, 1996).…”

Section: Resultssupporting

confidence: 60%

Expression patterns of cadherin genes in Drosophila oogenesis

Zartman

Kanodia

Yakoby

et al. 2009

Gene Expression Patterns

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In Drosophila oogenesis, the follicular epithelium that envelops the oocyte is patterned by a small set of inductive signals and gives rise to an elaborate three-dimensional eggshell. Several eggshell structures provide sensitive readouts of the patterning signals, but the formation of these structures is still poorly understood. In other systems, epithelial morphogenesis is guided by the spatial patterning of cell adhesion and cytoskeleton genes. As a step towards developing a comprehensive description of patterning events leading to eggshell morphogenesis, we report the expression of Drosophila cadherins, calcium dependent adhesion molecules that are repeatedly used throughout development. We found that 9/17 of Drosophila cadherins are expressed in the follicular epithelium in dynamic patterns during oogenesis. In late oogenesis, the expression patterns of cadherin genes in the main body follicle cells is summarized using a compact set of simple geometric shapes, reflecting the integration of the EGFR and DPP inductive signals. The multi-layered composite patterning of the cadherins is hypothesized to play a key role in the formation of the eggshell. Of particular note is the complex patterning of the region of the follicular epithelium that gives rise to the dorsal appendages, which are tubular structures that serve as respiratory organs for the developing embryo.

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“…Mutations in PCDH15 are associated with Usher syndrome type 1F, a recessive disease characterised by retinopathy and hearing loss (Ahmed et al, 2001; Alagramam et al, 2001; El-Amraoui and Petit, 2005). Strikingly, the Drosophila homolog of PCDH15, Cad99C, is required for microvilli stability in the developing egg chamber (Schlichting et al, 2006). …”

Section: Discussionmentioning

confidence: 99%

chaoptin, prominin, eyes shut and crumbs form a genetic network controlling the apical compartment of Drosophila photoreceptor cells

2014

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The apical surface of epithelial cells is often highly specialised to fulfil cell type-specific functions. Many epithelial cells expand their apical surface by forming microvilli, actin-based, finger-like membrane protrusions. The apical surface of Drosophila photoreceptor cells (PRCs) forms tightly packed microvilli, which are organised into the photosensitive rhabdomeres. As previously shown, the GPI-anchored adhesion protein Chaoptin is required for the stability of the microvilli, whereas the transmembrane protein Crumbs is essential for proper rhabdomere morphogenesis. Here we show that chaoptin synergises with crumbs to ensure optimal rhabdomere width. In addition, reduction of crumbs ameliorates morphogenetic defects observed in PRCs mutant for prominin and eyes shut, known antagonists of chaoptin. These results suggest that these four genes provide a balance of adhesion and anti-adhesion to maintain microvilli development and maintenance. Similar to crumbs mutant PRCs, PRCs devoid of prominin or eyes shut undergo light-dependent retinal degeneration. Given the observation that human orthologues of crumbs, prominin and eyes shut result in progressive retinal degeneration and blindness, the Drosophila eye is ideally suited to unravel the genetic and cellular mechanisms that ensure morphogenesis of PRCs and their maintenance under light-mediated stress.

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Cadherin Cad99C is required for normal microvilli morphology in Drosophila follicle cells

Cited by 62 publications

References 60 publications

Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth

Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth

Expression patterns of cadherin genes in Drosophila oogenesis

chaoptin, prominin, eyes shut and crumbs form a genetic network controlling the apical compartment of Drosophila photoreceptor cells

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