Abstract
Symmetric or asymmetric positioning of intracellular structures including the nucleus and mitotic spindle steers various biological processes such as cell migration, division, and embryogenesis. In typical animal cells, both a sparse actomyosin meshwork in the cytoplasm and a dense actomyosin cortex underneath the cell membrane participate in the intracellular positioning. However, it remains unclear how these coexisting actomyosin structures regulate the positioning symmetry. To reveal the potential mechanism, we construct an in vitro model composed of cytoplasmic extracts and nucleus-like clusters confined in droplets. Here we find that periodic centripetal actomyosin waves contract from the droplet boundary push clusters to the center in large droplets, while network percolation of bulk actomyosin pulls clusters to the edge in small droplets. An active gel model quantitatively reproduces molecular perturbation experiments, which reveals that the tug-of-war between two distinct actomyosin networks with different maturation time-scales determines the positioning symmetry.
Highlights
Symmetric or asymmetric positioning of intracellular structures including the nucleus and mitotic spindle steers various biological processes such as cell migration, division, and embryogenesis
Active diffusion of actin-coated vesicles in cytoplasm driven by myosin V generates a pressure gradient, which targets the nucleus at the center in mouse oocytes[6]
Two distinct actomyosin structures often coexist in the same system, i.e., bulk actomyosin networks and actomyosin cortex beneath the cell membrane, and actomyosinregulated positioning of the nucleus and spindle is two-state, i.e., either at the center or close to the membrane boundary
Summary
Symmetric or asymmetric positioning of intracellular structures including the nucleus and mitotic spindle steers various biological processes such as cell migration, division, and embryogenesis. Both a sparse actomyosin meshwork in the cytoplasm and a dense actomyosin cortex underneath the cell membrane participate in the intracellular positioning It remains unclear how these coexisting actomyosin structures regulate the positioning symmetry. Two distinct actomyosin structures often coexist in the same system, i.e., bulk actomyosin networks and actomyosin cortex beneath the cell membrane, and actomyosinregulated positioning of the nucleus and spindle is two-state, i.e., either at the center or close to the membrane boundary These facts raise a fundamental question how the two-state geometry sensing (center or edge) is functioned by the two actomyosin structures located in spatially distinct places (bulk and surface). Spatial confinement of the extracts into droplets mimicking the cell boundary displays various actomyosin dynamics observed in living cells, such as symmetry breaking of the actin cortex[16,19] and spontaneous F-actin retrograde flow[13,22], providing insights into physical mechanisms of the cytoskeleton self-organization
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