Development and Physiology of the Oöcyte-Nurse Cell Syncytium

Telfer, William H.

doi:10.1016/s0065-2806(08)60164-2

Cited by 297 publications

(129 citation statements)

References 136 publications

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“…During oogenesis, eight sister germ cells are connected in a cluster and develop in parallel up to the pachytene stage. In contrast to Drosophila, all cells of the cluster form SCs (Telfer, 1975). After pachytene, seven cells are transformed into nurse cells and only one oocyte in a cluster completes meiosis.…”

Section: Introductionmentioning

confidence: 94%

“…All nuclei appear in the same pachytene substage, as judged from the appearance of SCs. The synchronized development of oocytes within a cluster until the end of pachytene appears to be a typical feature of Lepidoptera oogenesis (Telfer, 1975;King & Büning, 1985). In the middle of the cluster, a branched structure decorated with seven electron dense rings is visible.…”

Section: Microspreading Ofpachytene Nucleimentioning

confidence: 99%

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Synaptonemal complexes in female and male meiotic prophase of Ephestia kuehniella (Lepidoptera)

Marec

Traut

1993

Heredity

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Synaptonemal complex (SC) complements of oocyte and spermatocyte pachytene nuclei in the Mediterranean flour moth, Ephestia kuehniella, were investigated using a microspreading technique and electron microscopy. In both sexes, three autosomal SCs could be identified by their morphological landmarks; one SC has a prominent knob and two SCs have nucleolus organizer regions. In a later stage of SC development in oocytes, the two nucleolar SCs displayed electron dense terminal modifications of the lateral elements. In some oocytes, the sex chromosome bivalent was inconspicuous but in the majority it was recognized by heterochromatin tangles associated with the W chromosome, a shorter W chromosome axis and/or incomplete pairing. Male synaptonemal complexes in contrast to female ones contained recombination nodules (RNs). Almost every bivalent was associated with one RN, rarely none or two RNs. Along the SCs, RNs were preferentially located in distal positions. The presence of RNs in male SCs and their absence in female SCs corresponds with the presence of crossing over and chiasmata in male meiosis and their absence in female meiosis. The mean total length of SC complements was greater in males than in females, but in both sexes, variation was considerable. We assume that male SCs become longer with progression of the pachytene stage while in female SCs a period of elongation is followed by a period of shortening.

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Section: Introductionmentioning

confidence: 94%

Section: Microspreading Ofpachytene Nucleimentioning

confidence: 99%

Synaptonemal complexes in female and male meiotic prophase of Ephestia kuehniella (Lepidoptera)

Marec

Traut

1993

Heredity

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“…The fusome organizes the network microtubules within developing ovarian cysts and is required for the microtubuledependent restriction of oocyte markers (Grieder et al, 2000). In addition, the fusome directs the pattern of cystocyte interconnections by anchoring one pole of each mitotic spindle, thus orienting the plane of cell division (Telfer, 1975;Storto and King, 1989;Lin and Spradling, 1995).Mutations in genes that encode the cytoskeletal component of the fusome including ␣-spectrin and ␤-spectrin, and the adducin-like protein hts, result in a reduced number of cyst divisions and a block in oocyte differentiation (Lin et al, 1994;de Cuevas et al, 1996;de Cuevas and Spradling, 1998). In the absence of the fusome, cysts develop with random patterns of interconnections and no signs of polarity.…”

mentioning

confidence: 99%

The Fusome Mediates Intercellular Endoplasmic Reticulum Connectivity inDrosophilaOvarian Cysts

Snapp

Iida

Frescas

et al. 2004

MBoC

104

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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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“…Such conspicuous "extra DNA bodies" have not only been observed in dytiscid beetles but also in other beetles [24,25,33,48,49] and in taxonomic ally rather distant insect species (for refs. see Introduction and I.…”

mentioning

confidence: 94%

“…Among insects, three types of ribosome production during oogenesis have been distinguished (for reviews see [23,24]): (1) production in the oocyte using pre-rRNA copies present in the oocyte nucleus (panoistic ovaries; for rers. see , (2) production of complete ribosomes in nurse cells and transport 10 the 0o-plasm (all telotrophic and many of the polytrophicmeroistic ovarioles), and (3) contributions to ooplasmic ribosomes from both oocyte and nurse cells (these include but are not restricted to examples with an essentially polytrophic-meroistic organization; see rers.…”

Section: Introductionmentioning

confidence: 99%

Frequencies of Circular Units of Nucleolar DNA in Oocytes of Two Insects, Acheta domesticus and Dytiscus marginalis, and Changes of Nucleolar Morphology during Oogenesis

1977

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The organization of the extrachromosomal nucleolar material in oocytes of two insect species with different ovary types, the house cricket Acheta domesticus (panoistic ovary) and the water beetle Dytiscus marginalis (meroistic ovary), was studied with light and electron microscopic techniques. Stages early in oogenesis were compared with fully vitellogenic stages (mid-to-Iate diplotene). The arrangement of the nucleolar material undergoes a marked change from a densely aggregated to a dispersed state. The latter was characterized by high transcriptional activity. In spread and positively stained preparations of isolated nucleolar material, a high frequency of small circular units of transcribed rDNA was observed and rings with small numbers (1-5) of pre-rRNA genes were predominant. The observations suggest that the "extra DNA body" observed in early oogenic stages of both species represents a dense aggregate of numerous short circular units of nucleolar chromatin, with morphological subcomponents identifiable in ultrathin sections. These apparently remain in close association with the chromosomal nucleolar organizer(s). The observations further indicate that the individual small nucleolar subunit circles dissociate and are dispersed as actively transcribed rDNA units later in diplotene. The results are discussed in relation to principles of the ultrastructural organization of nucleoli in other cell types as well as in relation to possible mechanisms of gene amplification.

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Development and Physiology of the Oöcyte-Nurse Cell Syncytium

Cited by 297 publications

References 136 publications

Synaptonemal complexes in female and male meiotic prophase of Ephestia kuehniella (Lepidoptera)

Synaptonemal complexes in female and male meiotic prophase of Ephestia kuehniella (Lepidoptera)

The Fusome Mediates Intercellular Endoplasmic Reticulum Connectivity inDrosophilaOvarian Cysts

Frequencies of Circular Units of Nucleolar DNA in Oocytes of Two Insects, Acheta domesticus and Dytiscus marginalis, and Changes of Nucleolar Morphology during Oogenesis

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