Nuage morphogenesis becomes more complex: two translocation pathways and two forms of nuage coexist in Drosophila germline syncytia

Abstract

We have developed a simple and reliable method of preserving antigen immunoreactivity with concomitant excellent retention of the cell ultrastructure. Using this method, we have been able to follow the origin and developmental stages of nuage accumulations within the nurse cell/oocyte syncytium in the ovary of the fruit fly, Drosophila melanogaster, at the ultrastructural level. We have found two morphologically and biochemically distinct forms of nuage material in the nurse cell cytoplasm: translocating accumulations of nuage containing the Vasa protein, termed sponge bodies and stationary polymorphic accumulations of nuage enriched in Argonaute and Survival of motor neuron proteins. Immunogold labeling combined with confocal fluorescent and ultrastructural analyses have revealed that the Vasa-containing nuage accumulations remain closely associated with the cisternae of the endoplasmic reticulum throughout their lifetimes. The migration mechanism of the Vasa-positive nuage appears distinct from the microtubule-dependent translocation of oskar ribonucleoprotein complexes. We postulate that these two distinct nuage translocation pathways converge in the formation of the polar granules within the polar/germ plasm of the oocyte posterior pole. We also provide morphological and immunocytochemical evidence that these polymorphic nuage accumulations correspond to the recently described cytoplasmic domains termed U body-P body complexes.

RNA Granules in Germ Cells

“…Unlike germ granules, the PATR-1 granules are partitioned symmetrically during mitosis and recruit additional P body proteins after segregation into somatic blastomeres . Similarly, in the sponge bodies of Drosophila nurse cells, structures resembling the P body/U body complexes of somatic cells (Liu and Gall 2007) can be distinguished from nuage Jaglarz et al 2011). Together, these observations suggest that germ cells contain bona fide P-bodies, or P body-related granules, which interact and may even exchange components with germ granules, but are maintained as distinct RNP assemblies.…”

“…Sponge bodies appear to derive from fragments of perinuclear nuage that associate with ER membranes, detach from the nucleus, and intermingle in the cytoplasm with other P-body-like granules (see below) (Wilsch-Brauninger et al 1997;Jaglarz et al 2011). Sponge bodies accumulate in the oocyte, apparently by movement along ER membranes that extend from the nurse cells through the ring canals into the oocyte (Jaglarz et al 2011). Sponge bodies movement has been hypothesized to transport perinuclear nuage material from the nurse cells to the germ (pole) plasm of the oocyte .…”

The Bic-C Family of Developmental Translational Regulators

“…In the Drosophila ovary Bic-C is present in cytoplasmic granules enriched for Trailer Hitch (Tral) and Me31B [31, 32], two proteins marking sponge bodies, ovarian organelles related to the repression of mRNA translation [33–35]. Mouse and Xenopus Bicc1 in cultured cells are also found within subcellular structures associated with mRNA silencing, the processing granules (P granules, [26, 27, 36]), strongly suggesting that the members of the Bic-C protein family may share a conserved function in translational control.…”

mRNP granules

“…Next, repressed mRNPs are typically localized to and anchored at particular cellular location via interactions with molecular motors and cytoskeletal elements, although sponge bodies are thought to move along ER membranes. 18 A signaling event often precedes the switch of localized mRNAs from repression to translation, followed by granule disassembly. 9,15,91 This topic has been well covered elsewhere, 92 thus the focus here will be on how granule formation may contribute to localization.…”