Abstract
The generation of F-actin bundles is controlled by the action of actin-binding proteins. In Drosophila bristle development, two major actin-bundling proteins—Forked and Fascin—were identified, but still the molecular mechanism by which these actin-bundling proteins and other proteins generate bristle actin bundles is unknown. In this study, we developed a technique that allows recapitulation of bristle actin module organization using the Drosophila ovary by a combination of confocal microscopy, super-resolution structured illumination microscopy, and correlative light and electron microscope analysis. Since Forked generated a distinct ectopic network of actin bundles in the oocyte, the additive effect of two other actin-associated proteins, namely, Fascin and Javelin (Jv), was studied. We found that co-expression of Fascin and Forked demonstrated that the number of actin filaments within the actin bundles dramatically increased, and in their geometric organization, they resembled bristle-like actin bundles. On the other hand, co-expression of Jv with Forked increased the length and density of the actin bundles. When all three proteins co-expressed, the actin bundles were longer and denser, and contained a high number of actin filaments in the bundle. Thus, our results demonstrate that the Drosophila oocyte could serve as a test tube for actin bundle analysis.
Highlights
Parallel actin bundles are composed of tightly packed filaments, all with the same polarity, crosslinked by an actin-bundling protein [1,2,3]
In contrast to Forked (Figure 1A, arrowhead shows the asymmetric actin bundles network), expression of Fascin (Figure 1B) or Jv (Figure 1C) revealed that the proteins were distributed throughout the oocyte during mid-oogenesis, with Fascin showing a noticeable accumulation on the oocyte membrane
The Drosophila Ovary as a Model Tissue to Study Bristle Actin Bundle Formation
Summary
Parallel actin bundles are composed of tightly packed filaments, all with the same polarity, crosslinked by an actin-bundling protein [1,2,3] These actin bundles are key components of eukaryotic cytoskeleton structures, such as the brush border of intestinal epithelial cells [4,5,6], stereocilia of hair cells of the vertebrate and ear [7,8], Sertoli cellspermatid ectoplasmic specialization [9,10], the nurse-cell strut in Drosophila eggs [11,12], and insect epidermal cell types, such as bristles and scales [13,14,15]. An additional crosslinking protein enables the formation of thick bundles, as found in bristles [22]
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