Cell-Size-Dependent Spindle Elongation in the Caenorhabditis elegans Early Embryo

Proc. Natl. Acad. Sci. U.S.A.

2011

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Cytoplasmic streaming is a type of intracellular transport widely seen in nature. Cytoplasmic streaming in Caenorhabditis elegans at the one-cell stage is bidirectional; the flow near the cortex ("cortical flow") is oriented toward the anterior, whereas the flow in the central region ("cytoplasmic flow") is oriented toward the posterior. Both cortical flow and cytoplasmic flow depend on non-musclemyosin II (NMY-2), which primarily localizes in the cortex. The manner in which NMY-2 proteins drive cytoplasmic flow in the opposite direction from remote locations has not been fully understood. In this study, we demonstrated that the hydrodynamic properties of the cytoplasm are sufficient to mediate the forces generated by the cortical myosin to drive bidirectional streaming throughout the cytoplasm. We quantified the flow velocities of cytoplasmic streaming using particle image velocimetry (PIV) and conducted a threedimensional hydrodynamic simulation using the moving particle semiimplicit method. Our simulation quantitatively reconstructed the quantified flow velocity distribution resolved through PIV analysis. Furthermore, our PIV analyses detected microtubule-dependent flows during the pronuclear migration stage. These flows were reproduced via hydrodynamic interactions between moving pronuclei and the cytoplasm. The agreement of flow dynamics in vivo and in simulation indicates that the hydrodynamic properties of the cytoplasm are sufficient to mediate cytoplasmic streaming in C. elegans embryos. fluid dynamics | particle method | Newtonian fluid | cell polarity | algae

Section: Methodsmentioning

confidence: 99%

Hydrodynamic property of the cytoplasm is sufficient to mediate cytoplasmic streaming in the Caenorhabiditis elegans embryo

Niwayama

Shinohara

Proc. Natl. Acad. Sci. U.S.A.

2011

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“…C. elegans strains were maintained using standard techniques (52). RNAi was performed by injecting dsRNAs as described previously (53). Details of the strains and the procedure of RNAi experiments are described in SI Materials and Methods.…”

Section: Methodsmentioning

confidence: 99%

Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo

Proc. Natl. Acad. Sci. U.S.A.

2010

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132

168

The centrosome is generally maintained at the center of the cell. In animal cells, centrosome centration is powered by the pulling force of microtubules, which is dependent on cytoplasmic dynein. However, it is unclear how dynein brings the centrosome to the cell center, i.e., which structure inside the cell functions as a substrate to anchor dynein. Here, we provide evidence that a population of dynein, which is located on intracellular organelles and is responsible for organelle transport toward the centrosome, generates the force required for centrosome centration in Caenorhabditis elegans embryos. By using the database of full-genome RNAi in C. elegans, we identified dyrb-1, a dynein light chain subunit, as a potential subunit involved in dynein anchoring for centrosome centration. DYRB-1 is required for organelle movement toward the minus end of the microtubules. The temporal correlation between centrosome centration and the net movement of organelle transport was found to be significant. Centrosome centration was impaired when Rab7 and RILP, which mediate the association between organelles and dynein in mammalian cells, were knocked down. These results indicate that minus end-directed transport of intracellular organelles along the microtubules is required for centrosome centration in C. elegans embryos. On the basis of this finding, we propose a model in which the reaction forces of organelle transport generated along microtubules act as a driving force that pulls the centrosomes toward the cell center. This is the first model, to our knowledge, providing a mechanical basis for cytoplasmic pulling force for centrosome centration.endosome | lysosome | pronuclear migration | the centrosome-organelle mutual pulling model | yolk granule

“…2c). 25 Another possible mechanism for length-dependent pulling at the cortex established that cytoplasmic pulling is a major driving force for centrosome centration in (some) animal cells. Of course, there may be other mechanisms involved in this centration.…”

Section: The Centrosome-organelle Mutual Pulling Model As An Underlyimentioning

confidence: 99%

“…23 (C) When the anchors are rate-limiting, the probability of microtubules to encounter the anchor is proportional to the surface area they cover 21 and thus would be roughly proportional to the square length of microtubules (L 2 ). 25 (D) When cytoplasmic anchors are rate-limiting, the probability of microtubules to encounter the anchor is proportional to the volume they cover and thus be proportional to the cubic length of microtubules (L 3 ).…”

Section: Pulling At the Cortexmentioning

confidence: 99%

“…4,8 Because the centration depends on filamentous microtubules, the candidate mechanisms can be roughly divided into anticipated number of anchors to contact a single microtubule is proportional to the surface area covered by the microtubule, the force on a single microtubule should be roughly proportional to the squared length of the microtubule (L 2 ). 25 The assumption that the pulling force generator is limited in number is based on an experimental estimation. 26 A "servomechanical model" 23 assumes that in flat cells, microtubules elongate along the cell cortex until they reach the lateral cell boundaries.…”

mentioning

confidence: 99%

See 1 more Smart Citation

A novel mechanism of microtubule length-dependent force to pull centrosomes toward the cell center

2011

BioArchitecture

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t he centrosome is a major microtubule-organizing center in animal cells, and its intracellular positioning is critical for defining intracellular architecture. the centrosome positions itself at the cell center. centrosome centration depends on the microtubule cytoskeleton. to accomplish robust centration regardless of the cell size or cell shape, it has been assumed that the force mediated by the microtubules depends on microtubule length. however, a concrete mechanism to generate forces to pull the centrosome in a microtubule lengthdependent manner has been elusive. recently, we successfully demonstrated that centrosome-directed movement of intracellular organelles along microtubules drives centrosome centration in the Caenorhabditis elegans early embryo. based on this observation, we proposed the centrosome-organelle mutual pulling model in which the reaction forces of organelle transport generated along microtubules act as a driving force that pulls the centrosomes toward the cell center. this is the first experiment-based model that accounts for the microtubule length-dependent pulling force generated in the cytoplasm contributing to centrosome centration. intriguingly, this model is consistent with a recent estimation that the pulling force is proportional to the cubic length of microtubules. The Emergence of Order in Cell ArchitectureThe cell can be compared to a city. A population of macromolecules lives their lives inside the cell, and they utilize the a novel mechanism of microtubule length-dependent force to pull centrosomes toward the cell center