A Pushing Mechanism for Microtubule Aster Positioning in a Large Cell Type

Meaders, Johnathan L.; Matos, Salvador N. de; Burgess, David R.

doi:10.1016/j.celrep.2020.108213

Cited by 31 publications

(35 citation statements)

References 68 publications

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“…We found that aMTOC-nucleated asters can indeed find the center of PDMS channels as well as annular cylinder hydrogel enclosures, suggesting that our model system might serve as a reasonable proxy to study the phenomenon. In agreement with recent published studies in sea urchin embryos, ( Meaders et al. , 2020 ), inhibition of dynein via p150-CC1 did not affect aster centration in our extracts.…”

Section: Discussionsupporting

confidence: 94%

Microtubule-dependent pushing forces contribute to long-distance aster movement and centration inXenopus laevisegg extracts

Sulerud

Sami

et al. 2020

MBoC

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During interphase of the eukaryotic cell cycle, the microtubule (MT) cytoskeleton serves as both a supportive scaffold for organelles and an arborized system of tracks for intracellular transport. At the onset of mitosis, the position of the astral MT network, specifically its center, determines the eventual location of the spindle apparatus and ultimately the cytokinetic furrow. Positioning of the MT aster often results in its movement to the center of a cell, even in large blastomeres hundreds of microns in diameter. This translocation requires positioning forces, yet how these forces are generated and then integrated within cells of varied sizes and geometries remains an open question. Here we describe a method that combines microfluidics, hydrogels, and Xenopus laevis egg extract to investigate the mechanics of aster movement and centration. We determined that asters were able to find the center of artificial channels and annular cylinders, even when cytoplasmic dynein-dependent pulling mechanisms were inhibited. Characterization of aster movement away from V-shaped hydrogel barriers provided additional evidence for a MT-based pushing mechanism. Importantly, the distance over which this mechanism seemed to operate was longer than that predicted by radial aster growth models, agreeing with recent models of a more complex MT network architecture within the aster. [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text] [Media: see text]

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Section: Discussionsupporting

confidence: 94%

Microtubule-dependent pushing forces contribute to long-distance aster movement and centration inXenopus laevisegg extracts

Sulerud

Sami

et al. 2020

MBoC

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“…Importantly, this centration was unaffected by perturbation of cytoplasmic dynein function. This observation undermined the possible contribution of motor-dependent pulling mechanisms, instead validating a mechanism that relied on microtubule-based pushing forces and one that had been previously observed in vivo [67]. The authors posited that microtubules pushed the aMTOCs away from proximal barriers by polymerizing against them, ultimately resulting in aster centration.…”

Section: Aster Centration and Cell-like Compartmentalization In Xenopus Egg Extractsmentioning

confidence: 87%

The Cytoskeleton and Its Roles in Self-Organization Phenomena: Insights from Xenopus Egg Extracts

Geisterfer

Gatlin

et al. 2021

Cells

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Self-organization of and by the cytoskeleton is central to the biology of the cell. Since their introduction in the early 1980s, cytoplasmic extracts derived from the eggs of the African clawed-frog, Xenopus laevis, have flourished as a major experimental system to study the various facets of cytoskeleton-dependent self-organization. Over the years, the many investigations that have used these extracts uniquely benefited from their simplified cell cycle, large experimental volumes, biochemical tractability and cell-free nature. Here, we review the contributions of egg extracts to our understanding of the cytoplasmic aspects of self-organization by the microtubule and the actomyosin cytoskeletons as well as the importance of cytoskeletal filaments in organizing nuclear structure and function.

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“…In line with this, analysis of C. elegans zygotes revealed that the movement of male and female pronuclei toward the zygote center is not only controlled by dynein-mediated length-dependent pulling forces exerted from the bulk of the cytoplasm, but also is affected by dynein motors associated with the cortex and female pronuclear envelope (Figure 3B;De Simone et al, 2018). Moreover, sperm aster centering in sea urchin zygotes was recently suggested to depend on microtubule polymerization-mediated pushing forces against the cortex rather than bulk dynein-mediated drag forces (Meaders et al, 2020). Collectively, these studies highlight the diverse nature of the forces driving aster positioning in zygotes and the requirement for investigating the individual contribution of each force-generating mechanism to completely understand this process.…”

Section: Aster Positioningmentioning

confidence: 96%

“…As a result, cortical actomyosin flows can trigger cytoplasmic flows and vice versa (Deneke et al, 2019;Mittasch et al, 2018). Likewise, microtubule polymerization-based pushing forces against the cortex (Meaders et al, 2020;Sulerud et al, 2020) and the motor-mediated pulling forces on microtubules generated in the bulk of the cytoplasm (Hamaguchi and Hiramoto, 1986;Tanimoto et al, 2016) can effectively lead to similar cytoplasmic movements. This makes it often difficult to unequivocally pinpoint the place within the cell where the forces driving those movements/flows are generated.…”

Section: Review Perspectivesmentioning

confidence: 99%