Uncovering the balance of forces driving microtubule aster migration in C. elegans zygotes

Simone, Alessandro De; Spahr, Antoine; Busso, Coralie; Gönczy, Pierre

doi:10.1038/s41467-018-03118-x

Cited by 43 publications

(50 citation statements)

References 37 publications

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“…It is widely accepted that the nucleus is pulled forward to the centrosome by the minus-end-directed motor activity of cytoplasmic dynein, as the inhibition of dynein or its regulator LIS1 attenuates nuclear displacement (Hirotsune et al, 1998;Shu et al, 2004;Tanaka et al, 2004;Tsai et al, 2007). In this scenario, the centrosome has to be anchored to the cell cortex of the leading process in order to generate a traction force against the cell membrane or ECM, which pulls the nucleus forward (Aumais et al, 2001;De Simone et al, 2018). However, previous live imaging studies have revealed dynamic movement of the centrosome around the nucleus, raising doubts about whether the centrosome is tightly associated to the cell cortex (Umeshima et al, 2007; (Figure 3).…”

Section: Microtubule Based Nuclear Translocationmentioning

confidence: 99%

Mechanical Regulation of Nuclear Translocation in Migratory Neurons

Nakazawa

Kengaku

2020

Front. Cell Dev. Biol.

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Neuronal migration is a critical step during the formation of functional neural circuits in the brain. Newborn neurons need to move across long distances from the germinal zone to their individual sites of function; during their migration, they must often squeeze their large, stiff nuclei, against strong mechanical stresses, through narrow spaces in developing brain tissue. Recent studies have clarified how actomyosin and microtubule motors generate mechanical forces in specific subcellular compartments and synergistically drive nuclear translocation in neurons. On the other hand, the mechanical properties of the surrounding tissues also contribute to their function as an adhesive support for cytoskeletal force transmission, while they also serve as a physical barrier to nuclear translocation. In this review, we discuss recent studies on nuclear migration in developing neurons, from both cell and mechanobiological viewpoints.

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Section: Microtubule Based Nuclear Translocationmentioning

confidence: 99%

Mechanical Regulation of Nuclear Translocation in Migratory Neurons

Nakazawa

Kengaku

2020

Front. Cell Dev. Biol.

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“…Oocyte meiotic spindle formation Gonczy et al, 1999 Attachment of the centrosomes to the sperm pronucleus Nuclear surface ZYG-12, SUN-1 Gonczy et al, 1999;Malone et al, 2003 Centrosome separation Nuclear surface, Cell cortex ZYG-12, SUN-1, GPA-16, GOA-1 Gonczy et al, 1999;Malone et al, 2003;De Simone et al, 2018 Oocyte pronuclear migration Nuclear surface DNC-1, DNC-2 ZYG-12, SUN-1 Skop and White, 1998;Gonczy et al, 1999 Sperm pronuclear migration and centering Cytoplasm, Cell cortex (*2) DNC-1, DNC-2, DYRB-1 LIS-1/NudE ZYG-12, SUN-1, RILP-1 Skop and White, 1998;Gonczy et al, 1999;Cockell et al, 2004;Kimura and Onami, 2005;Goulding et al, 2007;Kimura and Kimura, 2011 Nuclear rotation Cell cortex, Cytoplasm DNC-1, DNC-2 Skop and White, 1998;Gonczy et al, 1999;Kimura and Onami, 2007 Mitotic spindle formation LIS-1/NudE SPDL-1, Rod/Zwilch/Zw10 Gassmann et al, 2008;Simoes et al, 2018 Spindle displacement Cell cortex DYRB-1 PAR-2, PAR-3, GPA-16, GOA-1, GPR-1, GPR-2, LIN-5 Grill et al, 2001;Colombo et al, 2003;Couwenbergs et al, 2007;Nguyen-Ngoc et al, 2007;Fielmich et al, 2018 Spindle rocking Cell cortex GPA-16, GOA-1, GPR-1, GPR-2…”

Section: Referencesmentioning

confidence: 99%

“…The cortical pulling force separates the centrosomes along the nuclear surface also in Drosophila embryo (Cytrynbaum et al, 2003). Dyneins on the nuclear surface and at the cortex both contribute to centrosome separation, where the knockdown of both functions results in defects in separation (De Simone et al, 2018).…”

Section: Network Of Dyneins For Centrosomementioning

confidence: 99%

The Generation of Dynein Networks by Multi-Layered Regulation and Their Implication in Cell Division

Torisawa

Kimura

2020

Front. Cell Dev. Biol.

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Cytoplasmic dynein-1 (hereafter referred to as dynein) is a major microtubule-based motor critical for cell division. Dynein is essential for the formation and positioning of the mitotic spindle as well as the transport of various cargos in the cell. A striking feature of dynein is that, despite having a wide variety of functions, the catalytic subunit is coded in a single gene. To perform various cellular activities, there seem to be different types of dynein that share a common catalytic subunit. In this review, we will refer to the different kinds of dynein as "dyneins." This review attempts to classify the mechanisms underlying the emergence of multiple dyneins into four layers. Inside a cell, multiple dyneins generated through the multi-layered regulations interact with each other to form a network of dyneins. These dynein networks may be responsible for the accurate regulation of cellular activities, including cell division. How these networks function inside a cell, with a focus on the early embryogenesis of Caenorhabditis elegans embryos, is discussed, as well as future directions for the integration of our understanding of molecular layering to understand the totality of dynein's function in living cells.

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“…Which pool of dynein, cortical, cytoplasmic, or a combination of both, contributes to aster centration has been a topic of numerous studies within the field. RNAi-mediated inhibition of cortical factors required for dynein recruitment results in faster migration of sperm asters during centering [17,18], while posterior displacement after rotation of the PNC is abrogated [17,[19][20][21][22]. These studies indicate that cytoplasmic dynein is the primary candidate for generating centering pulling forces on the sperm asters during centration, which are counteracted by cortical pulling forces ( Figure 1B inset).…”

Section: Sperm Aster Growth and Centration In C Elegansmentioning

confidence: 88%

Microtubule-Based Mechanisms of Pronuclear Positioning

Meaders

Burgess

2020

Cells

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The zygote is defined as a diploid cell resulting from the fusion of two haploid gametes. Union of haploid male and female pronuclei in many animals occurs through rearrangements of the microtubule cytoskeleton into a radial array of microtubules known as the sperm aster. The sperm aster nucleates from paternally-derived centrioles attached to the male pronucleus after fertilization. Nematode, echinoderm, and amphibian eggs have proven as invaluable models to investigate the biophysical principles for how the sperm aster unites male and female pronuclei with precise spatial and temporal regulation. In this review, we compare these model organisms, discussing the dynamics of sperm aster formation and the different force generating mechanism for sperm aster and pronuclear migration. Finally, we provide new mechanistic insights for how sperm aster growth may influence sperm aster positioning.

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Uncovering the balance of forces driving microtubule aster migration in C. elegans zygotes

Cited by 43 publications

References 37 publications

Mechanical Regulation of Nuclear Translocation in Migratory Neurons

Mechanical Regulation of Nuclear Translocation in Migratory Neurons

The Generation of Dynein Networks by Multi-Layered Regulation and Their Implication in Cell Division

Microtubule-Based Mechanisms of Pronuclear Positioning

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