Computer Simulations and Image Processing Reveal Length-Dependent Pulling Force as the Primary Mechanism for C. elegans Male Pronuclear Migration

Kimura, Asako; Onami, Shuichi

doi:10.1016/j.devcel.2005.03.007

Cited by 127 publications

(221 citation statements)

References 47 publications

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“…18 In a computer simulation assuming that the anchors are located in the cytoplasm, the in vivo profile of centrosome centration was reproduced in C. elegans. 14 The requirement of such a mechanism was supported by observations in early amphibian and fish embryonic cells where cells are so large that the plus-ends of microtubules hardly reach the cell cortex during centrosome centration. 3 However, no reports have elucidated the actual structure in the cytoplasm that anchors cytoplasmic dynein to pull the centrosomes.…”

Section: B(b) 2b and D]mentioning

confidence: 94%

“…The pushing force mediated by microtubules should be weaker for longer microtubules and thus account for the centration of centrosomes. 9,11,13,14 The pushing mechanism has been demonstrated to be sufficient for centrosome centration in vitro. 15 In living cells, yeast Saccharomyces cerevisiae 16 and Schizosaccharomyces pombe 13 use the pushing mechanism to position the spindle pole body (SPB; the centrosome counterpart in yeast) at the cell center.…”

Section: Pushing Mechanism: Microtubule Length Dependency and Experimmentioning

confidence: 99%

“…20 It is believed that the pulling mechanism is the major driving force for centrosome centration in animal cells. 14 Here, one remaining mystery has been the location where the pulling force that moves the centrosome to the cell center is generated, i.e., which structure inside the cell functions as a substrate to anchor force generators (i.e., dynein or the plusend of microtubules). 9,[21][22][23] We refer to the structure as the "centrosome centration anchor."…”

Section: Pulling Mechanism: Microtubule Length Dependency and Experimmentioning

confidence: 99%

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

Kimura

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

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Section: B(b) 2b and D]mentioning

confidence: 94%

Section: Pushing Mechanism: Microtubule Length Dependency and Experimmentioning

confidence: 99%

Section: Pulling Mechanism: Microtubule Length Dependency and Experimmentioning

confidence: 99%

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

Kimura

2011

BioArchitecture

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“…A cortically bound form of dynein, a minus end directed microtubule motor protein that is conserved from yeast to mammals, is indeed involved in nuclear migration, mitotic spindle orientation and cytoskeletal reorientation during wound healing [reviewed by Dujardin and Vallee, 2002;Yamamoto and Hiraoka, 2003]. Recent computer simulation approaches confirmed that the pulling force generated at the interface between the microtubule plus ends and the cell cortex is the primary driver for the movement of the nucleus and centrosome in C. elegans early embryos [Kimura and Onami, 2005;Kimura and Onami, 2007]. In contrast, microtubuledepolymerizing kinesins remove tubulin dimers from the ends ( Fig.…”

Section: Generation Of Asymmetry In the Microtubule Patternmentioning

confidence: 99%

Shaping microtubules into diverse patterns: Molecular connections for setting up both ends

Mimori-Kiyosue¹

2011

Cytoskeleton

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Microtubules serve as rails for intracellular trafficking and their appropriate organization is critical for the generation of cell polarity, which is a foundation of cell differentiation, tissue morphogenesis, ontogenesis and the maintenance of homeostasis. The microtubule array is not just a static railway network; it undergoes repeated collapse and reassembly in diverse patterns during cell morphogenesis. In the last decade much progress has been made toward understanding the molecular mechanisms governing complex microtubule patterning. This review first revisits the basic principle of microtubule dynamics, and then provides an overview of how microtubules are arranged in highly shaped and functional patterns in cells changing their morphology by factors controlling the fate of microtubule ends. V C 2011 Wiley Periodicals, Inc.

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“…In contrast, the major driving force for centrosome centration in animal cells is microtubule pulling forces through the action of cytoplasmic dynein, a minus end-directed motor protein complex (14,15). The pulling force, but not the pushing force, accounts for the behavior of the centrosomes in Caenorhabditis elegans embryos (16). However, it is still unclear where cytoplasmic dynein is anchored inside the cell to pull the centrosomes toward the center (6,(17)(18)(19)(20).…”

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confidence: 99%

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

Kimura

2010

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

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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

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Computer Simulations and Image Processing Reveal Length-Dependent Pulling Force as the Primary Mechanism for C. elegans Male Pronuclear Migration

Cited by 127 publications

References 47 publications

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

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

Shaping microtubules into diverse patterns: Molecular connections for setting up both ends

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

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