Microtubule-Based Mechanisms of Pronuclear Positioning

Meaders, Johnathan L.; Burgess, David R.

doi:10.3390/cells9020505

Cited by 19 publications

(19 citation statements)

References 66 publications

(102 reference statements)

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“…For all of the aforementioned reasons, we suggest using caution when extending our findings to explain aster and spindle positioning as it occurs in cells in vivo. Indeed, it is well established that cortical pulling forces play a major role in aster/spindle positioning in several eukaryotic systems (for excellent reviews, see Kotak and Gonczy, 2013 ; McNally, 2013 ; Meaders and Burgess, 2020 ). Furthermore, data in support of the cytoplasmic pulling model, which are largely based on observations of aster and spindle positioning in sea urchin and in C. elegans blastomeres, are compelling ( Hyman, 1989 ; Gonczy et al.…”

Section: Discussionmentioning

confidence: 99%

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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: Discussionmentioning

confidence: 99%

“…Whether the same mechanism functions in large cells in vivo is a different and, at present, unresolved question. However, recent in vivo experimental evidence argues that this might be the case ( Meaders et al. , 2020 ).…”

Section: Discussionmentioning

confidence: 99%

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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“…(2) Positioning of organelles and intracellular organization [57][58][59][60][61][62][63][64][65]. (3) Mechanotransduction [66].…”

Section: Control Of Microtubule Functionmentioning

confidence: 99%

“…Furthermore, microtubules are involved in: (1) Formation of primary cilia [ 54 ] as well as motile cilia contributing to cell movement [ 55 ] or the generation of liquid flow [ 56 ]. (2) Positioning of organelles and intracellular organization [ 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 ]. (3) Mechanotransduction [ 66 ].…”

Section: Microtubule Organization and Functionmentioning

confidence: 99%

Microtubule Organization in Striated Muscle Cells

Becker

Leone

Engel

2020

Cells

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Distinctly organized microtubule networks contribute to the function of differentiated cell types such as neurons, epithelial cells, skeletal myotubes, and cardiomyocytes. In striated (i.e., skeletal and cardiac) muscle cells, the nuclear envelope acts as the dominant microtubule-organizing center (MTOC) and the function of the centrosome—the canonical MTOC of mammalian cells—is attenuated, a common feature of differentiated cell types. We summarize the mechanisms known to underlie MTOC formation at the nuclear envelope, discuss the significance of the nuclear envelope MTOC for muscle function and cell cycle progression, and outline potential mechanisms of centrosome attenuation.

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“…The forces that act on MTs to move asters, centrosomes, and nuclei differ between systems ( Garzon-Coral et al, 2016 ; Grill and Hyman, 2005 ; Kotak and Gönczy, 2013 ; Meaders and Burgess, 2020 ; Xie and Minc, 2020 ). Centration movement of the sperm aster after fertilization and movement of sister asters away from the midzone after mitosis are thought to involve similar mechanics (ibid).…”

Section: Introductionmentioning

confidence: 99%

Co-movement of astral microtubules, organelles and F-actin by dynein and actomyosin forces in frog egg cytoplasm

Pelletier

Field

Fürthauer

et al. 2020

eLife

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How bulk cytoplasm generates forces to separate post-anaphase microtubule (MT) asters in Xenopus laevis and other large eggs remains unclear. Previous models proposed that dynein-based, inward organelle transport generates length-dependent pulling forces that move centrosomes and MTs outwards, while other components of cytoplasm are static. We imaged aster movement by dynein and actomyosin forces in Xenopus egg extracts and observed outward co-movement of MTs, endoplasmic reticulum (ER), mitochondria, acidic organelles, F-actin, keratin, and soluble fluorescein. Organelles exhibited a burst of dynein-dependent inward movement at the growing aster periphery, then mostly halted inside the aster, while dynein-coated beads moved to the aster center at a constant rate, suggesting organelle movement is limited by brake proteins or other sources of drag. These observations call for new models in which all components of the cytoplasm comprise a mechanically integrated aster gel that moves collectively in response to dynein and actomyosin forces.

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Microtubule-Based Mechanisms of Pronuclear Positioning

Cited by 19 publications

References 66 publications

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

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

Microtubule Organization in Striated Muscle Cells

Co-movement of astral microtubules, organelles and F-actin by dynein and actomyosin forces in frog egg cytoplasm

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