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Balance of actively generated contractile and resistive forces controls cytokinesis dynamics.

ABSTRACT: Cytokinesis, the fission of a mother cell into two daughter cells, is a simple and dramatic cell shape change. Here, we examine the dynamics of cytokinesis by using a combination of microscopy, dynamic measurements, and genetic analysis. We find that cytokinesis proceeds through a single sequence of shape changes, but the kinetics of the transformation from one shape to another differs dramatically between strains. We interpret the measurements in a simple and quantitative manner by using a previously uncharacterized analytic model. From the analysis, wild-type cytokinesis appears to proceed through an active, extremely regulated process in which globally distributed proteins generate resistive forces that slow the rate of furrow ingression. Finally, we propose that, in addition to myosin II, a Laplace pressure, resulting from material properties and the geometry of the dividing cell, generates force to help drive furrow ingression late in cytokinesis.

SUBMITTER: Zhang W

PROVIDER: S-EPMC1129136 | biostudies-literature | 2005 May

REPOSITORIES: biostudies-literature

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Balance of actively generated contractile and resistive forces controls cytokinesis dynamics.

Zhang Wendy W Robinson Douglas N DN

Proceedings of the National Academy of Sciences of the United States of America 20050503 20

Cytokinesis, the fission of a mother cell into two daughter cells, is a simple and dramatic cell shape change. Here, we examine the dynamics of cytokinesis by using a combination of microscopy, dynamic measurements, and genetic analysis. We find that cytokinesis proceeds through a single sequence of shape changes, but the kinetics of the transformation from one shape to another differs dramatically between strains. We interpret the measurements in a simple and quantitative manner by using a prev ...[more]

PMID: 15870188

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Project description:Human neutrophils are mediators of innate immunity and undergo dramatic shape changes at all stages of their functional life cycle. In this work, we quantified the forces associated with a neutrophil's morphological transition from a nonadherent, quiescent sphere to its adherent and spread state. We did this by tracking, with high spatial and temporal resolution, the cell's mechanical behavior during spreading on microfabricated post-array detectors printed with the extracellular matrix protein fibronectin. Two dominant mechanical regimes were observed: transient protrusion and steady-state contraction. During spreading, a wave of protrusive force (75 ± 8 pN/post) propagates radially outward from the cell center at a speed of 206 ± 28 nm/s. Once completed, the cells enter a sustained contractile state. Although post engagement during contraction was continuously varying, posts within the core of the contact zone were less contractile (-20 ± 10 pN/post) than those residing at the geometric perimeter (-106 ± 10 pN/post). The magnitude of the protrusive force was found to be unchanged in response to cytoskeletal inhibitors of lamellipodium formation and myosin II-mediated contractility. However, cytochalasin B, known to reduce cortical tension in neutrophils, slowed spreading velocity (61 ± 37 nm/s) without significantly reducing protrusive force. Relaxation of the actin cortical shell was a prerequisite for spreading on post arrays as demonstrated by stiffening in response to jasplakinolide and the abrogation of spreading. ROCK and myosin II inhibition reduced long-term contractility. Function blocking antibody studies revealed haptokinetic spreading was induced by β2 integrin ligation. Neutrophils were found to moderately invaginate the post arrays to a depth of ∼1 μm as measured from spinning disk confocal microscopy. Our work suggests a competition of adhesion energy, cortical tension, and the relaxation of cortical tension is at play at the onset of neutrophil spreading.

Dataset Information

Balance of actively generated contractile and resistive forces controls cytokinesis dynamics.

Publications

Balance of actively generated contractile and resistive forces controls cytokinesis dynamics.

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