Dynamics of filamentous actin organization in the sea urchin egg cortex during early cleavage divisions: Implications for the mechanism of cytokinesis

Wong, Gene K.; Allen, Philip G.; Begg, David A.

doi:10.1002/(sici)1097-0169(1997)36:1<30::aid-cm3>3.0.co;2-l

Cited by 52 publications

(20 citation statements)

References 52 publications

(71 reference statements)

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“…after treatment with jasplakinolide (this study) or in sea urchin eggs following fertilization (Wong et al, 1997). Another example is during microvillar formation in intestinal epithelial cells which begins in the crypts of Lieberkuln and continues on the villus before its cells are sloughed away from the villus tip 2-3 days later (Fath et al, 1990;Mamajiwalla et al, 1992).…”

Section: Microvillar Dynamicsmentioning

confidence: 90%

Microvilli appear to represent the first step in actin bundle formation inDrosophilabristles

Tilney

Connelly

Guild

2004

Journal of Cell Science

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During bristle development the emerging bristle shaft, socket cell, and the apical surface of thoracic epithelial cells form tiny protuberances or pimples that contain electron-dense material located on the cytoplasmic surface of the pimple tip. In a few cases short actin filaments extend from this material into the cortical cytoplasm. When cultured in the presence of jasplakinolide, an agent that prevents filament disassembly, pimples elongate to form microvilli containing a core of crosslinked filaments. Emerging-bristle mutants delay cortical bundle formation and are aggregated by forked protein crossbridges. Using these mutants and enhancing core bundle formation with jasplakinolide we found that microvillar formation represents the first stage in the morphogenesis of much larger actin bundles in Drosophila bristle shaft cells. Evidence is presented showing that socket cells do not contain forked protein crossbridges, a fact that may explain why cortical bundles only appear in bristle shaft cells. Furthermore, as pimples and microvilli form in the absence of both forked and fascin crossbridges, we also conclude that neither of these crossbridges account for core bundle formation in microvilli, but there must exist a third, as yet unidentified crossbridge in this system. Immunocytochemisty suggested that this new crossbridge is not Drosophila villin. Finally, ultrastructural comparisons suggest that microspikes and microvilli form very differently.

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Section: Microvillar Dynamicsmentioning

confidence: 90%

Microvilli appear to represent the first step in actin bundle formation inDrosophilabristles

Tilney

Connelly

Guild

2004

Journal of Cell Science

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“…It has been widely suggested that microvilli, which increase the surface area of sea urchin eggs 4-fold (34), might easily provide the required increase in surface area during cytokinesis. However, measurements of microvillar length through the cell cycle indicate that microvilli are not a likely source of membrane (34,35). The appearance of new hyalin at the cell surface after mitotic exit (Figs.…”

Section: Discussionmentioning

confidence: 99%

Targeted new membrane addition in the cleavage furrow is a late, separate event in cytokinesis

Shuster

Burgess

2002

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

103

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Cytokinesis in animal cells is accomplished in part by an actomyosin contractile ring. Recent work on amphibian, Drosophila, and Caenorhabditis elegans embryos implicates membrane trafficking and delivery as essential for cytokinesis. However, the relative contributions of contractile ring constriction versus membrane insertion to cytokinesis and the temporal relationship between these processes are largely unexplored. Here we monitor secretion of the extracellular matrix protein, hyalin, as a marker for new plasma membrane addition in dividing sea urchin zygotes. We find that new membrane addition occurs specifically in the cleavage furrow late in telophase independent of contractile ring constriction. The directed equatorial deposition of new furrow membrane requires astral microtubules and release of internal stores of Ca 2؉ , but not the presence of a central spindle. Further, cells arrested in M phase do not secrete hyalin, suggesting that mitotic exit is required for new membrane addition. These results demonstrate that astral overlap in equilaterally dividing cells not only serves to specify positioning and contraction of the contractile ring, but also to direct the delivery of new membrane to the furrow as a late, independent event during cytokinesis. T he fundamental mechanics by which chromosomes are segregated into daughter cells during mitosis are highly conserved in eukaryotic cells. The cyclin-dependent kinasemediated assembly of a microtubule-based mitotic spindle, the antagonistic actions of molecular motors, and the presence of a kinetochore-based mitotic checkpoint are common to all plant, animal, and fungal cells (1). In contrast, a variety of strategies are used to effect the physical partitioning of cytoplasm during cytokinesis (2), which has complicated the understanding of cleavage plane determination and daughter cell separation. Recent advances in model organisms, however, have revealed commonalties suggesting that the mechanisms of cytokinesis in diverse systems are more similar than previously appreciated (3). One component of cytokinesis that may be a requirement for both plant and animal cells is the generation of new plasma membrane (4, 5).Daughter cell separation in plant cells is driven by the generation of new cell surface at the cleavage plane. A microtubuleand microfilament-based structure termed the phragmoplast is formed at the spindle midzone that mediates the delivery of membrane vesicles that in turn fuse to form the new cell wall (6). Like plant cells, the mitotic apparatus in animal cells also specifies the cleavage plane, but does so by directing the assembly of an actomyosin contractile ring, which provides the contractile force for furrow ingression (7). The role of membrane addition in cytokinesis in most animal cells, however, is less clear.In large embryonic cells, such as dividing amphibian eggs, the requirement for new membrane addition has been appreciated for some time (8). In these cells, new membrane addition is independent of furrow constriction because inhi...

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“…Cells were then fixed and permeablized using a protocol optimized for visualizing the actin cytoskeleton (Wong et al, 1997). Cells were then washed, blocked with 3% bovine serum albumin in phosphate-buffered saline/2 mM NaF, and processed for tubulin (DM1A; Sigma-Aldrich), activated myosin II [rabbit or mouse anti-phospho(Ser19)-myosin regulatory light chain; Cell Signaling Technology, Beverly, MA], or egg myosin II localization.…”

Section: Detection Of Ser19 Phosphorylation In Vivomentioning

confidence: 99%

A Global, Myosin Light Chain Kinase-dependent Increase in Myosin II Contractility Accompanies the Metaphase–Anaphase Transition in Sea Urchin Eggs

Lucero

Stack

Bresnick

et al. 2006

MBoC

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Myosin II is the force-generating motor for cytokinesis, and although it is accepted that myosin contractility is greatest at the cell equator, the temporal and spatial cues that direct equatorial contractility are not known. Dividing sea urchin eggs were placed under compression to study myosin II-based contractile dynamics, and cells manipulated in this manner underwent an abrupt, global increase in cortical contractility concomitant with the metaphase-anaphase transition, followed by a brief relaxation and the onset of furrowing. Prefurrow cortical contractility both preceded and was independent of astral microtubule elongation, suggesting that the initial activation of myosin II preceded cleavage plane specification. The initial rise in contractility required myosin light chain kinase but not Rho-kinase, but both signaling pathways were required for successful cytokinesis. Last, mobilization of intracellular calcium during metaphase induced a contractile response, suggesting that calcium transients may be partially responsible for the timing of this initial contractile event. Together, these findings suggest that myosin II-based contractility is initiated at the metaphaseanaphase transition by Ca 2؉ -dependent myosin light chain kinase (MLCK) activity and is maintained through cytokinesis by both MLCK-and Rho-dependent signaling. Moreover, the signals that initiate myosin II contractility respond to specific cell cycle transitions independently of the microtubule-dependent cleavage stimulus. INTRODUCTIONAt its most fundamental level, cytokinesis in animal cells is brought about by regional differences in cortical contractility that drives partitioning of the cytoplasm into two daughter cells (Wang, 2005). Force generation is accomplished by the transient assembly of a contractile ring, and recent genetic and proteomic approaches have significantly increased our knowledge of ring components and regulatory molecules (Echard et al., 2004;Eggert et al., 2004;Skop et al., 2004). Studies in yeast using green fluorescent protein-tagged ring components have demonstrated that ring components are recruited to the division site in a hierarchical manner that involves the progressive assembly of more complex structures (Lippincott and Li, 1998;Wu et al., 2003;Wu and Pollard, 2005). In contrast, the temporal sequence in which ring components are recruited to the division site in animal cells is not as well resolved; thus, it remains unclear whether the contractile ring assembles in a similar sequential manner. Moreover, it is not known how ring assembly is coordinated in space and time with chromosome segregation. Thus, although great advances have been made in our understanding of the contractile ring itself, fundamental gaps remain in our understanding of the spatiotemporal regulation of cytokinesis.The mechanical nature of cytokinesis was appreciated by early cell biologists (Wilson, 1928;Rappaport, 1996), and for decades investigators have taken advantage of the large size and regular geometry of echinoderm eggs to st...

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Dynamics of filamentous actin organization in the sea urchin egg cortex during early cleavage divisions: Implications for the mechanism of cytokinesis

Cited by 52 publications

References 52 publications

Microvilli appear to represent the first step in actin bundle formation inDrosophilabristles

Microvilli appear to represent the first step in actin bundle formation inDrosophilabristles

Targeted new membrane addition in the cleavage furrow is a late, separate event in cytokinesis

A Global, Myosin Light Chain Kinase-dependent Increase in Myosin II Contractility Accompanies the Metaphase–Anaphase Transition in Sea Urchin Eggs

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