New components of the Drosophila fusome suggest it plays novel roles in signaling and transport

Howard Hughes Medical Institute Research Laboratories, Department of Embryology, Carnegie Institution, Baltimore, MD 21218, USA.
Developmental Biology (Impact Factor: 3.55). 06/2008; 317(1):59-71. DOI: 10.1016/j.ydbio.2008.02.009
Source: PubMed


The fusome plays an essential role in prefollicular germ cell development within insects such as Drosophila melanogaster. Alpha-spectrin and the adducin-like protein Hu-li tai shao (Hts) are required to maintain fusome integrity, synchronize asymmetric cystocyte mitoses, form interconnected 16-cell germline cysts, and specify the initial cell as the oocyte. By screening a library of protein trap lines, we identified 14 new fusome-enriched proteins, including many associated with its characteristic vesicles. Our studies reveal that fusomes change during development and contain recycling endosomal and lysosomal compartments in females but not males. A significant number of fusome components are dispensable, because genetic disruption of tropomodulin, ferritin-1 heavy chain, or scribble, does not alter fusome structure or female fertility. In contrast, rab11 is required to maintain the germline stem cells, and to maintain the vesicle content of the spectrosome, suggesting that the fusome mediates intercellular signals that depend on the recycling endosome.

    • "However, the structure of the germ cell clusters of D. parthenogeneticus suggests that this cluster is also formed as a result of four incomplete divisions, but in contrast to D. melanogaster not all of the cells undergo each division (asynchronous divisions). The fusome material that is present in the cytoplasm of cytoplasmic bridges that interconnect germ cells of D. melanogaster provides the synchrony of divisions (Lighthouse et al. 2008; Ong and Tan 2010). Fusome is not observed in D. parthenogeneticus, which may explain the asynchronism of divisions during the formation of germ cell clusters. "
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    ABSTRACT: Germ cell cluster organization and the process of oogenesis in Dactylobiotus parthenogeneticus have been described using transmission electron microscopy and light microscopy. The reproductive system of D. parthenogeneticus is composed of a single, sac-like, meroistic ovary and a single oviduct that opens into the cloaca. Two zones can be distinguished in the ovary: a small germarium that is filled with oogonia and a vitellarium that is filled with germ cell clusters. The germ cell cluster, which has the form of a modified rosette, consists of eight cells that are interconnected by stable cytoplasmic bridges. The cell that has the highest number of stable cytoplasmic bridges (four bridges) finally develops into the oocyte, while the remaining cells become trophocytes. Vitellogenesis of a mixed type occurs in D. parthenogeneticus. One part of the yolk material is produced inside the oocyte (autosynthesis), while the second part is synthesized in the trophocytes and transported to the oocyte through the cytoplasmic bridges. The eggs are covered with two envelopes: a thin vitelline envelope and a three-layered chorion. The surface of the chorion forms small conical processes, the shape of which is characteristic for the species that was examined. In our paper, we present the first report on the rosette type of germ cell clusters in Parachela.
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    • "A role for Rab11 in proliferation and differentiation of retinal tissues has been demonstrated in Zebrafish [5]. In Drosophila Rab11 has been shown to be involved in polarization of oocytes [6,7], post-Golgi trafficking of rhodopsin [8], ommatidal formation, activation of JNK signalling during eye development [9,10] maintenance of germ line stem cells [11], embryonic nervous system development [12] and promoting terminal differentiation of follicle cells in egg chamber [13]. Rab11 has been recently shown to be involved in regulating cell-cell interaction during collective cell migration [14]. "
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    ABSTRACT: Rab11, an evolutionary conserved, ubiquitously expressed subfamily of small monomeric GTPase has been known to regulate diverse cellular and developmental events, by regulating the exocytotic and transcytotic events inside the cell. Our studies show that Rab11 regulates Drosophila adult myogenesis by controlling proliferation and differentiation of the Adult muscle precursors (AMPs). Blocking Rab11 in the AMPs, which fuse to form the Indirect Flight Muscles (IFMs) of fly, renders flies completely flightless and non-viable. The indirect flight musculature, comprising of the differentially patterned dorsal longitudinal muscles (DLMs) and dorsal ventral muscles (DVMs), is affected to different extents. Abrogating or knocking down normal Rab11 function results in severely disrupted IFMs. DLMs forming from larval templates are reduced in number along with a significant reduction in their fibre size. The de novo developing DVMs are frequently absent. The DLMs in Rab11 hypomorphs are highly reduced, showing as a small constricted mass in one half of the thorax. Further, Rab11 function is essential for growth of these muscles during later half of adult myogenesis, as down regulation of Rab11 in IFMs results in degenerated muscles and broken fibres. Finally, we show that loss of Rab11 activity in the AMPs result in acquisition of migratory characteristic of myoblast as they show cellular protrusion at their polar ends accompanied with loss of cell-cell contacts. Our data provide the first evidence of a trafficking protein playing an indispensable role in regulating early stages of adult muscle development.
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    • "In addition to vesicle-related proteins, the female fusome contains recycling endosomal and lysosomal proteins [26], [27]. Therefore, the fusome has been proposed as a center of membrane recycling and a signal for the supply of ER-derived components to oocytes [26]. Furthermore, microtubule motors (e.g., Dhc and KLP61F) and microtubule-associated proteins (e.g., Lis1) are required to generate a normal female fusome structure [28], [29], [30]. "
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    ABSTRACT: Orbit, a Drosophila ortholog of microtubule plus-end enriched protein CLASP, plays an important role in many developmental processes involved in microtubule dynamics. Previous studies have shown that Orbit is required for asymmetric stem cell division and cystocyte divisions in germline cysts and for the development of microtubule networks that interconnect oocyte and nurse cells during oogenesis. Here, we examined the cellular localization of Orbit and its role in cyst formation during spermatogenesis. In male germline stem cells, distinct localization of Orbit was first observed on the spectrosome, which is a spherical precursor of the germline-specific cytoskeleton known as the fusome. In dividing stem cells and spermatogonia, Orbit was localized around centrosomes and on kinetochores and spindle microtubules. After cytokinesis, Orbit remained localized on ring canals, which are cytoplasmic bridges between the cells. Thereafter, it was found along fusomes, extending through the ring canal toward all spermatogonia in a cyst. Fusome localization of Orbit was not affected by microtubule depolymerization. Instead, our fluorescence resonance energy transfer experiments suggested that Orbit is closely associated with F-actin, which is abundantly found in fusomes. Surprisingly, F-actin depolymerization influenced neither fusome organization nor Orbit localization on the germline-specific cytoskeleton. We revealed that two conserved regions of Orbit are required for fusome localization. Using orbit hypomorphic mutants, we showed that the protein is required for ring canal formation and for fusome elongation mediated by the interaction of newly generated fusome plugs with the pre-existing fusome. The orbit mutation also disrupted ring canal clustering, which is essential for folding of the spermatogonia after cytokinesis. Orbit accumulates around centrosomes at the onset of spermatogonial mitosis and is required for the capture of one of the duplicated centrosomes onto the fusome. Moreover, Orbit is involved in the proper orientation of spindles towards fusomes during synchronous mitosis of spermatogonial cysts.
    Full-text · Article · Mar 2013 · PLoS ONE
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