Cytoplasmic flows as signatures for the mechanics of mitotic positioning.
The proper positioning of mitotic spindle in the single-cellCaenorhabditis elegansembryo is achieved initially by the migration and rotation of the pronuclear complex (PNC) and its two associated astral microtubules (MTs). Pronuclear migration produces global cytoplasmic flows that couple the mechanics of all MTs, the PNC, and the cell periphery with each other through their hydrodynamic interactions (HIs). We present the first computational study that explicitly accounts for detailed HIs between the cytoskeletal components and demonstrate the key consequences of HIs for the mechanics of pronuclear migration. First, we show that, because of HIs between the MTs, the cytoplasm-filled astral MTs behave like a porous medium, with its permeability decreasing with increasing the number of MTs. We then directly study the dynamics of PNC migration under various force-transduction models, including the pushing or pulling of MTs at the cortex and the pulling of MTs by cytoplasmically bound force generators. Although achieving proper position and orientation on reasonable time scales does not uniquely choose a model, we find that each model produces a different signature in its induced cytoplasmic flow. We suggest that cytoplasmic flows can be used to differentiate between mechanisms.
Center for Computational Biology, Flatiron Institute, New York, NY 10010 enazockdast@simonsfoundation.org mshelley@simonsfoundation.org.|Courant Institute of Mathematical Sciences, New York University, New York, NY 10012.
Ehssan
E
Nazockdast
Courant Institute of Mathematical Sciences, New York University, New York, NY 10012.
Abtin
A
Rahimian
School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138.
Daniel
D
Needleman
Center for Computational Biology, Flatiron Institute, New York, NY 10010 enazockdast@simonsfoundation.org mshelley@simonsfoundation.org.|Courant Institute of Mathematical Sciences, New York University, New York, NY 10012.
Michael
M
Shelley
D000818:Animals; D001696:Biomechanical Phenomena / Q000502:physiology; D017173:Caenorhabditis elegans / Q000196:embryology / Q000378:metabolism; D003198:Computer Simulation; D003593:Cytoplasm / Q000502:physiology; D003600:Cytosol / Q000378:metabolism; D004398:Dyneins / Q000378:metabolism; D057446:Hydrodynamics; D008870:Microtubules / Q000378:metabolism; D008938:Mitosis / Q000502:physiology*; D008941:Spindle Apparatus / Q000502:physiology*
D004398:Dyneins