Regulation of Early Endosomal Entry by the<i>Drosophila</i>Tumor Suppressors Rabenosyn and Vps45

Morrison, Holly A.; Dionne, Heather; Rusten, Tor Erik; Brech, Andreas; Fisher, William W.; Pfeiffer, Barret D.; Celniker, S; Stenmark, Harald; Bilder, David

doi:10.1091/mbc.e08-07-0716

Cited by 85 publications

(127 citation statements)

References 57 publications

Supporting

Mentioning

116

Contrasting

Order By: Relevance

“…Another distinctive group in the multilayer category are genes involved in 'vesicle transport' (e.g. Rab5 and Shibire/Dynamin), confirming previous studies which show that regulation of endocytosis is central for epithelial integrity (Lu and Bilder, 2005;Georgiou et al, 2008;Harris and Tepass, 2008;Leibfried et al, 2008;Morrison et al, 2008). We further subdivided the group of genes whose knockdown resulted in the multilayer phenotype into genes affecting the whole tissue architecture (Fig.…”

Section: Multilayered Epitheliasupporting

confidence: 83%

A genome-scale in vivo RNAi analysis of epithelial development in Drosophila identifies new proliferation domains outside of the stem cell niche

Berns¹,

Woichansky²,

Friedrichsen³

et al. 2014

Development

View full text Add to dashboard Cite

The Drosophila oogenesis system provides an excellent model to study the development of epithelial tissues. Here, we report the first genome-scale in vivo RNA interference (RNAi) screen for genes controlling epithelial development. By directly analysing cell and tissue architecture we identified 1125 genes, which we assigned to seven different functions in epithelial formation and homeostasis. We validated the significance of our screen by generating mutants for Vps60, a component of the endosomal sorting complexes required for transport (ESCRT) machinery. This analysis provided new insights into spatiotemporal control of cell proliferation in the follicular epithelium. Previous studies have identified signals controlling divisions in the follicle stem cell niche. However, 99% of cell divisions occur outside of the niche and it is unclear how these divisions are controlled. Our data distinguish two new domains outside of the stem cell niche where there are differing controls on proliferation. One domain abuts the niche and is characterised by ESCRT, Notch and JAK/STAT-mediated control of proliferation. Adjacent to this domain, another domain is defined by loss of the impact of ESCRT on cell division. Thus, during development epithelial cells pass through a variety of microenvironments that exert different modes of proliferation control. The switch between these modes might reflect a decrease in the 'stemness' of epithelial cells over time.

show abstract

Section: Multilayered Epitheliasupporting

confidence: 83%

A genome-scale in vivo RNAi analysis of epithelial development in Drosophila identifies new proliferation domains outside of the stem cell niche

Berns¹,

Woichansky²,

Friedrichsen³

et al. 2014

Development

View full text Add to dashboard Cite

show abstract

“…Therefore, although many endocytosis-related genes play roles later in oogenesis for MT maintenance, Chc is needed for the establishment of MT organization already around oogenesis stage 6. Furthermore, establishment of MT polarity by Chc appears to be endocytosis independent because Rbsn-5 null mutant egg chambers (showing strong endocytosis defects) and Rab-5 null mutants (also required for vesicle fusion in early endocytosis) do not reveal a requirement for this process (Tanaka and Nakamura, 2008;Morrison et al, 2008) (supplementary material Fig. S4).…”

Section: Endocytosis-independent Function Of Chc In Establishing Mt Pmentioning

confidence: 99%

Clathrin heavy chain plays multiple roles in polarizing the Drosophila oocyte downstream of Bic-D

et al. 2014

View full text Add to dashboard Cite

Bicaudal-D (Bic-D), Egalitarian (Egl), microtubules and their motors form a transport machinery that localizes a remarkable diversity of mRNAs to specific cellular regions during oogenesis and embryogenesis. Bic-D family proteins also promote dynein-dependent transport of Golgi vesicles, lipid droplets, synaptic vesicles and nuclei. However, the transport of these different cargoes is still poorly understood. We searched for novel proteins that either mediate Bic-Ddependent transport processes or are transported by them. Clathrin heavy chain (Chc) co-immunopurifies with Bic-D in embryos and ovaries, and a fraction of Chc colocalizes with Bic-D. Both proteins control posterior patterning of the Drosophila oocyte and endocytosis. Although the role of Chc in endocytosis is well established, our results show that Bic-D is also needed for the elevated endocytic activity at the posterior of the oocyte. Apart from affecting endocytosis indirectly by its role in osk mRNA localization, Bic-D is also required to transport Chc mRNA into the oocyte and for transport and proper localization of Chc protein to the oocyte cortex, pointing to an additional, more direct role of Bic-D in the endocytic pathway. Furthermore, similar to Bic-D, Chc also contributes to proper localization of osk mRNA and to oocyte growth. However, in contrast to other endocytic components and factors of the endocytic recycling pathway, such as Rabenosyn-5 (Rbsn-5) and Rab11, Chc is needed during early stages of oogenesis (from stage 6 onwards) to localize osk mRNA correctly. Moreover, we also uncovered a novel, presumably endocytosis-independent, role of Chc in the establishment of microtubule polarity in stage 6 oocytes.

show abstract

“…To dissect further in which endocytic steps D-EndoB is involved, we performed genetic interaction between D-EndoB and endocytic components by FM4-64 incorporation assay. Although Rbsn5, the Rab5 effector protein, did not interact with D-EndoB genetically (Table 1) (Morrison et al, 2008), D-EndoB displayed significant genetic interaction with the Sec5-Sec6 complex ( Fig. 7E-H ; Table 1), which regulates the endocytic recycling of Yolkless (Langevin et al, 2005;Sommer et al, 2005).…”

Section: D-endob Regulates Endocytosis Activity In the Oocytementioning

confidence: 99%

“…Yolk proteins are the sole nutritional source for Drosophila embryogenesis. They are synthesized in follicle cells and fat bodies, and are taken up by the oocytes through endocytosis during Drosophila oogenesis (Compagnon et al, 2009;Morrison et al, 2008;Richard et al, 2001). Drosophila oogenesis can be divided into 14 stages involving a process of egg chamber growth and maturation.…”

Section: Introductionmentioning

confidence: 99%

“…Recently, the role of Long Oskar in the yolk endocytosis and the F-actin projection at the posterior pole were found (Vanzo et al, 2007). Rab5 and its effector protein, Rbsn5, are also involved in yolk endocytosis (Compagnon et al, 2009;Morrison et al, 2008). Rbsn5 acts downstream of Long Oskar for the pole plasm and endosomal protein anchorage (Tanaka and Nakamura, 2008).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Endophilin B is required for the Drosophila oocyte to endocytose yolk downstream of Oskar

et al. 2014

View full text Add to dashboard Cite

The nutritional environment is crucial for Drosophila oogenesis in terms of controlling hormonal conditions that regulate yolk production and the progress of vitellogenesis. Here, we discovered that Drosophila Endophilin B (D-EndoB), a member of the endophilin family, is required for yolk endocytosis as it regulates membrane dynamics in developing egg chambers. Loss of D-EndoB leads to yolk content reduction, similar to that seen in yolkless mutants, and also causes poor fecundity. In addition, mutant egg chambers exhibit an arrest at the previtellogenic stage. D-EndoB displayed a crescent localization at the oocyte posterior pole in an Oskar-dependent manner; however, it did not contribute to pole plasm assembly. DEndoB was found to partially colocalize with Long Oskar and Yolkless at the endocytic membranes in ultrastructure analysis. Using an FM4-64 dye incorporation assay, D-EndoB was also found to promote endocytosis in the oocyte. When expressing the full-length D-endoB FL or D-endoB ∆SH3 mutant transgenes in oocytes, the blockage of vitellogenesis and the defect in fecundity in D-endoB mutants was restored. By contrast, a truncated N-BAR domain of the D-EndoB only partially rescued these defects. Taken together, these results allow us to conclude that D-EndoB contributes to the endocytic activity downstream of Oskar by facilitating membrane dynamics through its N-BAR domain in the yolk uptake process, thereby leading to normal progression of vitellogenesis.

show abstract

Regulation of Early Endosomal Entry by theDrosophilaTumor Suppressors Rabenosyn and Vps45

Cited by 85 publications

References 57 publications

A genome-scale in vivo RNAi analysis of epithelial development in Drosophila identifies new proliferation domains outside of the stem cell niche

A genome-scale in vivo RNAi analysis of epithelial development in Drosophila identifies new proliferation domains outside of the stem cell niche

Clathrin heavy chain plays multiple roles in polarizing the Drosophila oocyte downstream of Bic-D

Endophilin B is required for the Drosophila oocyte to endocytose yolk downstream of Oskar

Contact Info

Product

Resources

About