Article

Serbus, L., Cha, B., Theurkauf, W. & Saxton, W. Dynein and the actin cytoskeleton control kinesin-driven cytoplasmic streaming in Drosophila oocytes. Development 132, 3743-3752

Department of Biology, Indiana University, Bloomington, 1001 East 3rd Street, IN 47405, USA.
Development (Impact Factor: 6.46). 09/2005; 132(16):3743-52. DOI: 10.1242/dev.01956
Source: PubMed

ABSTRACT

Mass movements of cytoplasm, known as cytoplasmic streaming, occur in some large eukaryotic cells. In Drosophila oocytes there are two forms of microtubule-based streaming. Slow, poorly ordered streaming occurs during stages 8-10A, while pattern formation determinants such as oskar mRNA are being localized and anchored at specific sites on the cortex. Then fast well-ordered streaming begins during stage 10B, just before nurse cell cytoplasm is dumped into the oocyte. We report that the plus-end-directed microtubule motor kinesin-1 is required for all streaming and is constitutively capable of driving fast streaming. Khc mutations that reduce the velocity of kinesin-1 transport in vitro blocked streaming yet still supported posterior localization of oskar mRNA, suggesting that streaming is not essential for the oskar localization mechanism. Inhibitory antibodies indicated that the minus-end-directed motor dynein is required to prevent premature fast streaming, suggesting that slow streaming is the product of a novel dynein-kinesin competition. As F-actin and some associated proteins are also required to prevent premature fast streaming, our observations support a model in which the actin cytoskeleton triggers the shift from slow to fast streaming by inhibiting dynein. This allows a cooperative self-amplifying loop of plus-end-directed organelle motion and parallel microtubule orientation that drives vigorous streaming currents and thorough mixing of oocyte and nurse-cell cytoplasm.

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    • "idence for asymmet - ric actomyosin flow related to polarity in Drosophila oocytes or embryos . However , a microtubule - and kinesin - dependent cytoplasmic streaming has been identified in Drosophila oocytes . Its function is not completely clear , but the streaming seems to be involved in establishment of the polarity ( Glotzer et al . , 1997 ; Serbus et al . , 2005 ; Ganguly et al . , 2012 ) ."
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    • "To fully characterize Kinesin function, we studied another process that is dependent on KHC: streaming of the ooplasm. From mid-oogenesis, there is constant mixing of the ooplasm driven by KHC-dependent transport (Ganguly et al., 2012; Palacios and St Johnston, 2002; Serbus et al., 2005). At st9, the movement is slow (Table 2). "
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    • "In the simplest model, MTs are highly polarized along the anteroposterior axis, such that minus ends are located at the anterior with plus ends extending toward the posterior (Clark et al., 1994, 1997), and MTs show an overall gradient of decreasing density from anterior to posterior (Micklem et al., 1997). In the second model, MTs are nucleated around the cortex of the oocyte, with the exception of the posterior, leading to plus ends of MTs being directed toward the center (Cha et al., 2002; Serbus et al., 2005). A variation on this model is one in which the MTs are nucleated predominantly from the oocyte nucleus (Januschke et al., 2006) rather than all over the anterior. "
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