Interplay between Rab5 and PtdIns(4,5)<i>P</i>2 controls early endocytosis in the<i>Drosophila</i>germline

Compagnon, Julien; Gervais, Louis; Roman, Mabel San; Chamot-Boeuf, S.; Guichet, Antoine

doi:10.1242/jcs.033027

Cited by 34 publications

(44 citation statements)

References 39 publications

(64 reference statements)

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“…We next depleted Rab5, a protein that functions at early stages of endocytic maturation, and one that is often used as a marker for early endosomes (Chavrier et al 1990). Consistent with results observed using rab5 nulls (Compagnon et al 2009), oocytes depleted of Rab5 displayed minimal yolk autofluorescence ( Figure S2B). However, large vesicles were not observed in these oocytes ( Figure S2B9).…”

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confidence: 80%

“…The granules serve as a food source for the developing embryo. Thus, a defect in endocytic maturation will be reflected by a loss or reduction in the number of condensed yolk granules, a scenario that has been demonstrated using rab5 nulls (Compagnon et al 2009).The Dynactin complex is a core regulator of the Dynein motor. Dynamitin (Dmn/p50) is a central component of this complex.…”

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confidence: 98%

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Efficient Endocytic Uptake and Maturation in Drosophila Oocytes Requires Dynamitin/p50

et al. 2015

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Dynactin is a multi-subunit complex that functions as a regulator of the Dynein motor. A central component of this complex is Dynamitin/p50 (Dmn). Dmn is required for endosome motility in mammalian cell lines. However, the extent to which Dmn participates in the sorting of cargo via the endosomal system is unknown. In this study, we examined the endocytic role of Dmn using the Drosophila melanogaster oocyte as a model. Yolk proteins are internalized into the oocyte via clathrin-mediated endocytosis, trafficked through the endocytic pathway, and stored in condensed yolk granules. Oocytes that were depleted of Dmn contained fewer yolk granules than controls. In addition, these oocytes accumulated numerous endocytic intermediate structures. Particularly prominent were enlarged endosomes that were relatively devoid of Yolk proteins. Ultrastructural and genetic analyses indicate that the endocytic intermediates are produced downstream of Rab5. Similar phenotypes were observed upon depleting Dynein heavy chain (Dhc) or Lis1. Dhc is the motor subunit of the Dynein complex and Lis1 is a regulator of Dynein activity. We therefore propose that Dmn performs its function in endocytosis via the Dynein motor. Consistent with a role for Dynein in endocytosis, the motor colocalized with the endocytic machinery at the oocyte cortex in an endocytosis-dependent manner. Our results suggest a model whereby endocytic activity recruits Dynein to the oocyte cortex. The motor along with its regulators, Dynactin and Lis1, functions to ensure efficient endocytic uptake and maturation.KEYWORDS microtubule motors; endocytosis; cell polarity; kinesin; dynactin M ICROTUBULE motors such as cytoplasmic Dynein (hereafter referred to as Dynein) and proteins of the Kinesin superfamily play essential roles in cargo transport. Dynein is a minus-end motor and is responsible for the majority of minus-end transport within the cell (Kardon and Vale 2009). Mammalian genomes encode .40 different Kinesins, and most of these move cargo toward the plus-end of microtubules (Hirokawa et al. 2009). One type of cargo that is known to be transported by microtubule motors are vesicles of the endolysosomal system.Cargoes that enter the cell via endocytosis follow numerous sorting pathways that ultimately determine their fate. For example, nutrient receptors such as the Transferrin receptor, are recycled back to the plasma membrane (Mayor et al. 1993;Huotari and Helenius 2011). Growth factor receptors and signaling molecules are often targeted for degradation (Beguinot et al. 1984;Huotari and Helenius 2011). This is necessary to attenuate growth-promoting signals. Persistent and uncontrolled growth-promoting signals are associated with cancer (Normanno et al. 2006). Cargoes that are destined for degradation transit through vesicles that undergo maturation from early endosome to late endosome. Late endosomes eventually fuse with acidic, degradative organelles known as lysosomes. Endocytic maturation involves the progressive and ordered association of specifi...

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confidence: 80%

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Efficient Endocytic Uptake and Maturation in Drosophila Oocytes Requires Dynamitin/p50

et al. 2015

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“…In Drosophila melanogaster, a nutritional environment modulates hormonal conditions to regulate oogenesis through yolk protein synthesis and the progression of vitellogenesis (Bownes et al, 1988;Compagnon et al, 2009;Drummond-Barbosa and Spradling, 2001;Tufail and Takeda, 2009). Yolk proteins are the sole nutritional source for Drosophila embryogenesis.…”

Section: Introductionmentioning

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).…”

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confidence: 99%

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

et al. 2014

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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.

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The Endosomal Network: Mediators and Regulators of Endosome Maturation

Podinovskaia

Spang

2018

Endocytosis and Signaling

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Endocytosis is a means for the cell to sample its environment for nutrients and regulate plasma membrane (PM) composition and area. Whereas the majority of internalized cargo is recycled back to the cell surface, select material is sent to the lysosome for degradation. Endosomes further play major roles in central cell activities as diverse as establishment of cell polarity and signaling, lysosomal storage and immunity. The complexity of endosomal functions is reflected by the extensive changes to endosome properties as they mature. The identity of individual endosomes is influenced by the presence of specific Rab GTPases and phosphoinositides (PIPs), which coordinate membrane traffic and facilitate endosomal functions. Motors and tethers direct the endosomes to the required locations and moderate fusion with other organelles. The maintenance of the elaborate endosomal network is supported by the ER and the trans-Golgi network (TGN), which promote the exchange of membrane components, provide enzymes, and assist with signaling. Additionally, V-ATPase is emerging as an underappreciated coordinator of endosome maturation and cell signaling. The inputs of the various mediators of endosome maturation are tightly regulated and coordinated to ensure appropriate maintenance and functioning of endosomes at each stage of the maturation process. Perturbations in endosome maturation are implicated in devastating diseases, such as neurodegeneration and cancer, and the endosome maturation processes are manipulated and exploited by intracellular pathogens to meet their own needs. A greater understanding of coordination and fine-tuning of endosome maturation will help us address various pathologies more effectively.

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Interplay between Rab5 and PtdIns(4,5)P2 controls early endocytosis in theDrosophilagermline

Cited by 34 publications

References 39 publications

Efficient Endocytic Uptake and Maturation in Drosophila Oocytes Requires Dynamitin/p50

Efficient Endocytic Uptake and Maturation in Drosophila Oocytes Requires Dynamitin/p50

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

The Endosomal Network: Mediators and Regulators of Endosome Maturation

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