Trends in Cell Biology
ReviewGermline cysts: a conserved phase of germ cell development?
Section snippets
A germline cyst stage prior to meiosis is widely conserved
In males and higher insect females, meiosis occurs throughout much of adult life. Consequently, morphological evidence of cysts, such as intercellular bridges (also called ring canals) and synchronous mitotic divisions, can be readily observed. Moreover, cysts in these species are long lived. By contrast, meiosis in vertebrate females and in lower insects is generally confined to the pre-adult gonad, where observation is more difficult. No evidence of cysts can be found in adult female ovaries.
Organelle aggregates are found in forming cysts
A central feature of cysts in Drosophila and other higher insects is the presence of an unusual intracellular organelle known as the fusome (reviewed in 5, 14; see Fig. 2a,b). Genetic studies have strongly implicated the fusome in the process of cyst formation. After summarizing current knowledge of fusome structure and function, we will consider whether vertebrate cysts contain structures that might serve a corresponding role. In Drosophila, the fusome in cystoblasts is round but branches
The cyst-forming cell cycle
Cysts are formed by reiterating a specialized cell cycle. Progress has come from a detailed analysis of the cyst-forming cell cycle in the Drosophila ovary24 (see Fig. 3). The fusome plays a central role in the process, and its behaviour has been followed during specific cell-cycle phases. Fig. 3e–h shows an example of one such cell cycle. In mitosis, the fusome segregates to only one of the two daughter cells, thus clearly marking the division as asymmetric (Fig. 3e). During S phase, a ‘plug’
Cyst initiation
Surprisingly, many steps in the cyst-forming cell cycle take place in germ cells prior to cyst formation. In Drosophila, the precursor to the cystoblast – a germline stem cell – undergoes a very similar cell cycle, but the ring canal formed is unstable and is lost in G2 of the cycle (Fig. 3). During mitosis, G1 and S phase, the behaviour of the fusome in a stem cell (Fig. 3a–c) resembles that in a cystoblast (Fig. 3e–g). At G2, the ring canal connecting the stem cell and its daughter closes and
Termination of cyst divisions
What mechanisms ensure that a particular number of cyst-forming divisions will occur prior to entering meiosis? BAM is present within dividing cysts and disappears after the final mitosis, and thus BAM degradation might serve as a termination signal. The rate of cyst-forming cell cycles during the time that BAM is present may determine cyst cell number. Mutations in the gene encoding cyclin E (CycE) reduce cyst size without disrupting synchrony. Flies with only one wild-type dose of CycE
What is the functional significance of germline cysts?
Cysts in males and higher insect females serve important functions. In males, the cellular interconnections ensure developmental synchrony and permit gene products to be shared between developing spermatocytes that contain different haploid genomes44. In females, the existence of cysts allows one cell to specialize as the oocyte and receive large amounts of egg components from the other cells, which serve as nurse cells.
It is less clear what the function of cysts might be early in
Acknowledgements
We thank Leslie Coggins, Larry Etkins, Don Fawcett, David Gard, Robert Hardy, Tom Hays and Ting Xie for images. We thank Nicole Grieder and Erika Matunis for critically reading the manuscript. This work was supported by the Howard Hughes Medical Institute.
References (53)
Differentiation
(1973)Adv. Insect. Physiol.
(1975)- et al.
Trends Cell Biol.
(1996) Semin. Cell Dev. Biol.
(1998)Curr. Opin. Cell Biol.
(1998)- et al.
Dev. Biol.
(1994) - et al.
Dev. Biol.
(1995) - et al.
Dev. Biol.
(1973) Mech. Dev.
(1998)- et al.
Cell
(1998)