Reversible response of protein localization and microtubule organization to nutrient stress during Drosophila early oogenesis

Abstract

Summary The maturation of animal oocytes is highly sensitive to nutrient availability. During Drosophila oogenesis, a prominent metabolic checkpoint occurs at the onset of yolk uptake (vitellogenesis): under nutrient stress, egg chambers degenerate by apoptosis. To investigate additional responses to nutrient deprivation, we studied the intercellular transport of cytoplasmic components between nurse cells and the oocyte during previtellogenic stages. Using GFP protein-traps, we showed that Ypsilon Schachtel (Yps), a putative RNA binding protein, moved into the oocyte by both microtubule (MT)-dependent and -independent mechanisms, and was retained in the oocyte in a MT-dependent manner. These data suggest that oocyte enrichment is accomplished by a combination of MT-dependent polarized transport and MT-independent flow coupled with MT-dependent trapping within the oocyte. Under nutrient stress, Yps and other components of the oskar ribonucleoprotein complex accumulated in large processing bodies in nurse cells, accompanied by MT reorganization. This response was detected as early as 2 hrs after starvation, suggesting that young egg chambers rapidly respond to nutrient stress. Moreover, both Yps aggregation and MT reorganization were reversed with re-feeding of females or the addition of exogenous insulin to cultured egg chambers. Our results suggest that egg chambers rapidly mount a stress response by altering intercellular transport upon starvation. This response implies a mechanism for preserving young egg chambers so that egg production can rapidly resume when nutrient availability improves.

Somatic insulin signaling regulates a germline starvation response in Drosophila egg chambers

“…They reside within ribonucleoprotein complexes (mRNPs) containing proteins that repress mRNA translation until they reach their destination in the oocyte. Enrichment of mRNPs in the oocyte depends on the microtubule (MT) network extending from the oocyte into nurse cells and dynein-mediated transport to the oocyte, combined with diffusion and localized retention in the oocyte (Koch and Spitzer, 1983; Shimada et al, 2011; Theurkauf et al, 1993). The oskar mRNP is one such complex, and includes the initiation factor eIF4E, the Y-box protein Yps, and the RNA helicase Me31B (Nakamura et al, 2001; Nakamura et al, 2004; Wilhelm et al, 2000).…”

Intercellular protein movement in syncytial Drosophila follicle cells

“…The following protein-trap lines were used: Vsg-GFP (CA7004), Oda-GFP (YD0523), RpL30-GFP (YB0151), Yps-GFP (ZCL1607) Quinones-Coello et al, 2007;Shimada et al, 2011). Protein-trap lines are available at Flytrap (http://flytrap.med.yale.edu/).…”

Shining light on Drosophila oogenesis: live imaging of egg development

“…Imaging of Staufen (Stau), a protein associated with RNPs containing oskar mRNA, revealed that oskar mRNA is randomly transported on MTs in all directions with a weak posterior bias [53]. Interestingly, Shimada et al recently discovered that the mRNA-binding protein Ypsilon Schachtel (Yps) is transported via both MT-dependent and MT-independent mechanisms and this transport is regulated by nutrient availability and insulin signaling, possibly as part of a mechanism to preserve oocytes during periods of nutrient deprivation and allowing for rapid resumption of reproduction when conditions improve [56 ].…”