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The Mechanism of Cytoplasmic Streaming in Drosophila Melanogaster Oocytes

  • Author(s): Monteith, Corey
  • Advisor(s): Saxton, William
  • et al.
Creative Commons Attribution-ShareAlike 4.0 International Public License
Abstract

Background: The transport of cytoplasmic components can be profoundly affected by hydrodynamics. A striking example is ooplasmic streaming in Drosophila. Forces from kinesin-1 are initially directed by a disordered meshwork of oocyte microtubules, generating slow disordered cytoplasmic flows. When microtubules shift into parallel alignment, kinesin generates fast ordered flows that mix nurse cell and oocyte cytoplasms.

Results: To understand the hydrodynamic mechanism of streaming, we used fluorescence microscopy to analyze microtubule organization and cytoplasmic flows, while using mathematical modeling to identify physical conditions that contribute to kinesin-driven self-organization. In the fast ordered state, microtubules align and undergo correlated bending in a subcortical layer. Cytoplasmic flows follow the curving microtubule paths with velocities that are slow near the cortex, faster within the microtubule layer, and fastest beneath it. FRAP and photoconversion indicate that minus-ends of the aligned microtubules are stationary relative to the cortex. Using known values for microtubule stiffness and kinesin velocity, we developed and tested a coupled hydrodynamic model that revealed key variables that can shift the system between disordered and ordered states, including: 1) the distance from the cortex at which microtubules can lie parallel to its plane, and 2) the intensity of kinesin force on its cortical microtubule tracks, which can be controlled by cytoplasmic viscosity.

Conclusions: Cytoplasmic streaming in Drosophila oocytes is a result of viscous drag on moving kinesin motors that mediates equal and opposite forces on cytoplasmic fluid and on microtubules whose minus ends are embedded in the cortex. Fluid flows toward plus-ends and microtubules are forced toward stationary minus-ends. Under certain conditions, this causes microtubules to align in bending arrays, creating constantly varying directions of flow that facilitate cytoplasmic mixing

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