Identification of TER94, an AAA ATPase Protein, as a Bam-dependent Component of the<i>Drosophila</i>Fusome

León, Arlene; McKearin, Dennis M.

doi:10.1091/mbc.10.11.3825

Cited by 89 publications

(76 citation statements)

References 41 publications

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“…From this assay, we identified a number of proteins in the Bam immunoprecipitants. In addition to the known Bam-associated partners, Ter94 (24) and eIF4A (25), observed in Bam immunoprecipitants (Fig. S1A), we also found that ubiquitin was highly enriched in Bam complexes in our assays (Fig.…”

Section: Resultssupporting

confidence: 68%

Bam-dependent deubiquitinase complex can disrupt germ-line stem cell maintenance by targeting cyclin A

et al. 2017

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

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Drosophila germ-line stem cells (GSCs) provide an excellent model to study the regulatory mechanisms of stem cells in vivo. Bag of marbles (bam) has been demonstrated to be necessary and sufficient to promote GSC and cystoblast differentiation. Despite extensive investigation of its regulation and genetic functions, the biochemical nature of the Bam protein has been unknown. Here, we report that Bam is an ubiquitin-associated protein and controls the turnover of cyclin A (CycA). Mechanistically, we found that Bam associated with Otu to form a deubiquitinase complex that stabilized CycA by deubiquitination, thus providing a mechanism to explain how ectopic expression of Bam in GSCs promotes differentiation. Collectively, our findings not only identify a biochemical function of Bam, which contributes to GSC fate determination, but also emphasizes the critical role of proper expression of cyclin proteins mediated by both ubiquitination and deubiquitination pathways in balancing stem cell self-renewal and differentiation.

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Section: Resultssupporting

confidence: 68%

Bam-dependent deubiquitinase complex can disrupt germ-line stem cell maintenance by targeting cyclin A

et al. 2017

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

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“…Cul-1 has been implicated in the regulated destruction of a wide array of proteins involved in both cell cycle regulation and signal transduction (reviewed in Deshaies, 1999). Interestingly, the membrane-associated protein TER94/VSC/p97, which localizes to the fusome (Leon and McKearin, 1999), has also been implicated in ubiquitin-dependent degradation in mammals (Dai and Li, 2001). Thus, the ER component of the fusome may provide a surface for regulated protein degradation.…”

Section: Discussionmentioning

confidence: 99%

“…This was suggested by the observation that Drosophila fusome structures are enriched with the cytoplasmic protein TER94, which associates with both the Golgi complex and the ER in vertebrates (Leon and McKearin, 1999;Uchiyama et al, 2002). To characterize the structure and origin of the membranous component of the fusome, we expressed the lumenal ER-marker protein, Lys-GFP-KDEL, the resident ER membrane protein, Sec61␣-GFP, or the Golgi marker, GalTase-GFP (Cole et al, 1996), in ovarian cysts.…”

Section: The Fusome Contains Continuous Er Membranesmentioning

confidence: 99%

The Fusome Mediates Intercellular Endoplasmic Reticulum Connectivity inDrosophilaOvarian Cysts

Snapp

Iida

Frescas

et al. 2004

MBoC

107

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Drosophila ovarian cysts arise through a series of four synchronous incomplete mitotic divisions. After each round of mitosis, a membranous organelle, the fusome, grows along the cleavage furrow and the remnants of the mitotic spindle to connect all cystocytes in a cyst. The fusome is essential for the pattern and synchrony of the mitotic cyst divisions as well as oocyte differentiation. Using live cell imaging, greenfluorescent protein-tagged proteins, and photobleaching techniques, we demonstrate that fusomal endomembranes are part of a single continuous endoplasmic reticulum (ER) that is shared by all cystocytes in dividing ovarian cysts. Membrane and lumenal proteins of the common ER freely and rapidly diffuse between cystocytes. The fusomal ER mediates intercellular ER connectivity by linking the cytoplasmic ER membranes of all cystocytes within a cyst. Before entry into meiosis and onset of oocyte differentiation (between region 1 and region 2A), ER continuity between cystocytes is lost. Furthermore, analyses of hts and Dhc64c mutants indicate that intercellular ER continuity within dividing ovarian cysts requires the fusome cytoskeletal component and suggest a possible role for the common ER in synchronizing mitotic cyst divisions. INTRODUCTIONGametogenesis takes place within germline cysts in a wide array of organisms (Telfer, 1975;Bü ning, 1994;de Cuevas et al., 1997). In Drosophila a single oocyte develops within the environment of a 16-cell cyst. The development of this cyst occurs in a series of morphologically defined regions (see Figure 1A). Cyst production begins when a germline stem cell divides asymmetrically to produce a cystoblast. The cystoblast undergoes four synchronous mitotic divisions (regions 1 and 2a), with incomplete cytokinesis, to produce a cluster of 16 cells that are connected via arrested mitotic cleavage furrows (reviewed in de Cuevas et al., 1997). Later in oogenesis, the arrested cleavage furrows mature into stable ring canals and are reinforced with an actin cytoskeleton (reviewed in Mahajan-Miklos and Cooley, 1994). Initially, all 16 cystocytes develop in synchrony. However, as development proceeds, differentiation within the cyst becomes asynchronous. Ultimately, only one cell commits to meiosis and differentiates as the oocyte, whereas the other 15 cystocytes enter the endocycle and develop as trophic nurse cells.A unique membranous organelle, the fusome, grows and branches along the spindle equators after each mitotic division to physically connect all cells within a cyst. The fusome is found in the germline cysts of Drosophila as well as other insects (reviewed in Telfer, 1975;McKearin, 1997). The Drosophila fusome is comprised of cytoplasmic endomembranes, membrane skeletal proteins and polarized microtubules (reviewed in de Cuevas et al., 1997;McKearin, 1997).Molecular genetic studies over the last ten years indicate the fusome mediates several essential steps in germline cyst development (reviewed in McKearin, 1997). The differentiation of the oocyte depends on the pr...

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“…), the study of these proteins has been made easier. This is particularly true for dNSF1 (comt;Siddiqi and Benzer, 1976), TER94 (Leon and McKearin, 1999), and sed5 (Ashburner et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Biogenesis of Golgi Stacks in Imaginal Discs ofDrosophila melanogaster

Kondylis

Goulding

Dunne

et al. 2001

MBoC

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We provide a detailed description of Golgi stack biogenesis that takes place in vivo during one of the morphogenetic events in the lifespan of Drosophila melanogaster. In early third-instar larvae, small clusters consisting mostly of vesicles and tubules were present in epithelial imaginal disk cells. As larvae progressed through mid-and late-third instar, these larval clusters became larger but also increasingly formed cisternae, some of which were stacked. In white pupae, the typical Golgi stack was observed. We show that larval clusters are Golgi stack precursors by 1) localizing various Golgi-specific markers to the larval clusters by electron and immunofluorescence confocal microscopy, 2) driving this conversion in wild-type larvae incubated at 37°C for 2 h, and 3) showing that this conversion does not take place in an NSF1 mutant (comt 17). The biological significance of this conversion became clear when we found that the steroid hormone 20-hydroxyecdysone (ecdysone) is critically involved in this conversion. In its absence, Golgi stack biogenesis did not occur and the larval clusters remained unaltered. We showed that dGM130 and sec23p expression increases approximately three-and fivefold, respectively, when discs are exposed to ecdysone in vivo and in vitro. Taken together, these results suggest that we have developed an in vivo system to study the ecdysone-triggered Golgi stack biogenesis.

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Identification of TER94, an AAA ATPase Protein, as a Bam-dependent Component of theDrosophilaFusome

Cited by 89 publications

References 41 publications

Bam-dependent deubiquitinase complex can disrupt germ-line stem cell maintenance by targeting cyclin A

Bam-dependent deubiquitinase complex can disrupt germ-line stem cell maintenance by targeting cyclin A

The Fusome Mediates Intercellular Endoplasmic Reticulum Connectivity inDrosophilaOvarian Cysts

Biogenesis of Golgi Stacks in Imaginal Discs ofDrosophila melanogaster

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