Shape–motion relationships of centering microtubule asters

Tanimoto, Hirokazu; Kimura, Asako; Minc, Nicolas

doi:10.1083/jcb.201510064

Cited by 74 publications

(158 citation statements)

References 33 publications

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“…These asters are organized around the nucleus from a pair of centrosomes, and may be positioned and oriented from dynein-mediated MT forces exerted in the cytoplasm. These findings outline a geometrical model in which length-dependent MT forces may convert aster geometry into a net force and torque to specify division positioning (Hamaguchi and Hiramoto, 1986; Minc et al, 2011; Mitchison et al, 2012; Tanimoto et al, 2016; Wuhr et al, 2009; Wuhr et al, 2010). These designs contrast with deterministic inputs that guide division positioning from cortical polarity cues that influence MT forces by promoting dynein activity or MT depolymerization at the cortex (Gonczy, 2008; Grill and Hyman, 2005; Kozlowski et al, 2007).…”

Section: Introductionmentioning

confidence: 71%

Generic Theoretical Models to Predict Division Patterns of Cleaving Embryos

et al. 2016

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Summary Life for all animals starts with a precise 3D-choreography of reductive divisions of the fertilized egg, known as cleavage patterns. These patterns exhibit conserved geometrical features and striking inter-species invariance within certain animal classes. To identify the generic rules that may govern these morphogenetic events, we developed a 3D-modelling framework that iteratively infers blastomere division positions and orientations, and consequent multicellular arrangements. From a minimal set of parameters, our model predicts detailed features of cleavage patterns in the embryos of fishes, amphibians, echinoderms and ascidians, as well as the genetic and physical perturbations that alter these patterns. This framework demonstrates that a geometrical system based on length-dependent microtubule forces that probe blastomere shape and yolk gradients, biased by cortical polarity domains, may dictate division patterns and overall embryo morphogenesis. These studies thus unravel the default self-organization rules governing early embryogenesis, and how they are altered by deterministic regulatory layers.

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Section: Introductionmentioning

confidence: 71%

Generic Theoretical Models to Predict Division Patterns of Cleaving Embryos

et al. 2016

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“…Third, the structure, and therefore the mechanical properties, of the network do not depend on the distance from the centrosome. As a speculation, the physical interconnection of the microtubules may facilitate the transduction of mechanical forces across the cell in a way unattainable in the radial array predicted by the standard model (Tanimoto et al, 2016; Wühr et al, 2010). …”

Section: Discussionmentioning

confidence: 99%

“…Specifically, astral microtubules transport organelles (Grigoriev et al, 2008; Wang et al, 2013; Waterman-Storer and Salmon, 1998), support cell motility by mediating mechanical and biochemical signals (Etienne-Manneville, 2013), and are required for proper positioning of the nucleus, the mitotic spindle, and the cleavage furrow (Field et al, 2015; Grill and Hyman, 2005; Neumüller and Knoblich, 2009; Tanimoto et al, 2016; Wilson, 1896). Within asters, individual microtubules undergo dynamic instability (Mitchison and Kirschner, 1984): They either grow (polymerize) or shrink (depolymerize) at their plus ends and stochastically transition between these two states.…”

Section: Introductionmentioning

confidence: 99%

Physical basis of large microtubule aster growth

Ishihara

Korolev

Mitchison

2016

eLife

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Microtubule asters - radial arrays of microtubules organized by centrosomes - play a fundamental role in the spatial coordination of animal cells. The standard model of aster growth assumes a fixed number of microtubules originating from the centrosomes. However, aster morphology in this model does not scale with cell size, and we recently found evidence for non-centrosomal microtubule nucleation. Here, we combine autocatalytic nucleation and polymerization dynamics to develop a biophysical model of aster growth. Our model predicts that asters expand as traveling waves and recapitulates all major aspects of aster growth. With increasing nucleation rate, the model predicts an explosive transition from stationary to growing asters with a discontinuous jump of the aster velocity to a nonzero value. Experiments in frog egg extract confirm the main theoretical predictions. Our results suggest that asters observed in large fish and amphibian eggs are a meshwork of short, unstable microtubules maintained by autocatalytic nucleation and provide a paradigm for the assembly of robust and evolvable polymer networks.DOI: http://dx.doi.org/10.7554/eLife.19145.001

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“…But how do asters “know” which way to move? describe how the asters associated with sperm pronuclei guide themselves to the center of sea urchin eggs after fertilization (1). …”

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confidence: 99%

“…Together with his postdoc, Hirokazu Tanimoto, and his collaborator, Akatsuki Kimura, from the National Institute of Genetics in Mishima, Japan, Minc tracked the three-dimensional movements of sperm asters inside sea urchin eggs, which have a diameter of ∼100 µm (1). A few minutes after entering the egg, asters moved directly toward the center at a constant speed of ∼5 µm/min, only slowing down as they neared their destination.…”

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confidence: 99%