A computational model of nuclear self-organisation in syncytial embryos

Abstract

Syncytial embryos develop through cycles of nuclear division and rearrangement within a common cytoplasm. A paradigm example is Drosophila melanogaster in which nuclei form an ordered array in the embryo surface over cell cycles 10–13. This ordering process is assumed to be essential for subsequent cellularisation. Using quantitative tissue analysis, it has previously been shown that the regrowth of actin and microtubule networks after nuclear division generates reordering forces that counteract its disordering effect (Kanesaki et al., 2011). We present here an individual-based computer simulation modelling the nuclear dynamics. In contrast to similar modelling approaches e.g. epithelial monolayers or tumour spheroids, we focus not on the spatial dependence, but rather on the time-dependence of the interaction laws. We show that appropriate phenomenological inter-nuclear force laws reproduce the experimentally observed dynamics provided that the cytoskeletal network regrows sufficiently quickly after mitosis. Then repulsive forces provided by the actin system are necessary and sufficient to regain the observed level of order in the system, after the strong disruption resulting from cytoskeletal network disassembly and spindle formation. We also observe little mixing of nuclei through cell cycles. Our study highlights the importance of the dynamics of cytoskeletal forces during this critical phase of syncytial development and emphasises the need for real-time experimental data at high temporal resolution.