Balance of actively generated contractile and resistive forces controls cytokinesis dynamics

Zhang, Wendy; Robinson, Douglas N.

doi:10.1073/pnas.0502545102

Cited by 112 publications

(193 citation statements)

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“…Inward forces include Laplace pressure, contraction driven by myosin motors, and actin cross-linker dynamics coupled with actin polymer disassembly (18)(19)(20)22). An ideal process for studying these inward forces is cytokinesis, where cells must contract inward along the cleavage furrow to divide one cell into two.…”

Section: Forces Acting On the Cell Cortexmentioning

confidence: 99%

“…In fact, in Dictyostelium, normal myosin II activity leads to a slowing down of furrow ingression during late stages of cytokinesis (20). Wild-type Dictyostelium cells are more deformable in the polar cortex than at the furrow, whereas myosin II-null cells have a limited mechanical differential (4).…”

Section: Forces Acting On the Cell Cortexmentioning

confidence: 99%

“…Wild-type Dictyostelium cells are more deformable in the polar cortex than at the furrow, whereas myosin II-null cells have a limited mechanical differential (4). This differential leads to two consequences of cell mechanics that likely contribute to this slowdown of furrow ingression in wild-type cells (19,20). First, as the furrow ingresses, resistive stresses can build in the two daughter cell cortices and cytoplasm, slowing furrow ingression.…”

Section: Forces Acting On the Cell Cortexmentioning

confidence: 99%

“…2). Even this dynamic range underestimates the cell's capabilities, because without myosin II, the cells can divide using Laplace pressure, which can be an order of magnitude more powerful than myosin II-mediated contractility (19,20). Similarly, cells theoretically can increase the motor output of the Arp2/3 complex-actin network at the leading edge by an order of magnitude during migration by force opposition alone (53).…”

Section: Mechanochemical Signaling Allows Dynamic Escalation Of Forcementioning

confidence: 99%

“…1 C) (18). When parameterized with directly measured values, these models help account for cell behavior during retraction from an applied force (18), cytokinesis (19,20), and cell motility (17,21).…”

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Mechanochemical Signaling Directs Cell-Shape Change

Schiffhauer

Robinson

2017

Biophysical Journal

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For specialized cell function, as well as active cell behaviors such as division, migration, and tissue development, cells must undergo dynamic changes in shape. To complete these processes, cells integrate chemical and mechanical signals to direct force production. This mechanochemical integration allows for the rapid production and adaptation of leading-edge machinery in migrating cells, the invasion of one cell into another during cell-cell fusion, and the force-feedback loops that ensure robust cytokinesis. A quantitative understanding of cell mechanics coupled with protein dynamics has allowed us to account for furrow ingression during cytokinesis, a model cell-shape-change process. At the core of cell-shape changes is the ability of the cell's machinery to sense mechanical forces and tune the force-generating machinery as needed. Force-sensitive cytoskeletal proteins, including myosin II motors and actin cross-linkers such as a-actinin and filamin, accumulate in response to internally generated and externally imposed mechanical stresses, endowing the cell with the ability to discern and respond to mechanical cues. The physical theory behind how these proteins display mechanosensitive accumulation has allowed us to predict paralogspecific behaviors of different cross-linking proteins and identify a zone of optimal actin-binding affinity that allows for mechanical stress-induced protein accumulation. These molecular mechanisms coupled with the mechanical feedback systems ensure robust shape changes, but if they go awry, they are poised to promote disease states such as cancer cell metastasis and loss of tissue integrity.The concept ''form begets function begets form'' provides an excellent foundation for understanding the behavior of biological systems. Even specialized cells, the smallest unit of complex living systems, perform all of the necessary functions of an organism by assuming distinct shapes, mechanical properties, and physical behaviors. Different cell types use a common set of cytoskeletal elements to provide precise physical support for their distinct functions. For example, red blood cells and neurons have very different shapes that allow them to perform their specific roles. However, they both utilize alternating patterns of actin and spectrin to form cortices with appropriate viscous and elastic properties, albeit in different structural arrangements. Perturbations to this structural network cause a breakdown in the mechanical properties, or the form, of these cells, which inhibits cell function (1,2).Fascinatingly, the physical properties of cells are both determined and acted upon by the cytoskeletal apparatus. Cells are capable of modifying their own physical properties and driving changes in cell shape in response to internal and external chemical and mechanical stimuli. These modifications occur through the remodeling of the cell cortex, the network of cytoskeletal proteins directly under the plasma membrane. Much progress has been made recently in deciphering how chemical signa...

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Section: Forces Acting On the Cell Cortexmentioning

confidence: 99%

Section: Forces Acting On the Cell Cortexmentioning

confidence: 99%

Section: Forces Acting On the Cell Cortexmentioning

confidence: 99%

Section: Mechanochemical Signaling Allows Dynamic Escalation Of Forcementioning

confidence: 99%

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confidence: 99%

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Mechanochemical Signaling Directs Cell-Shape Change

Schiffhauer

Robinson

2017

Biophysical Journal

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Using Lessons from Cellular and Molecular Structures for Future Materials

LeDuc

Robinson

2007

Advanced Materials

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Cells and molecules exhibit robust and efficient characteristics that occur as a result of highly organized and hierarchical structures within these small scale living systems. These structures have the ability to adapt themselves to a wide variety of stimuli, including mechanical and chemical environmental changes, which ultimately affect behavior including cell life and death. The characteristics of these structures can be utilized as they provide unique advantages for building a future generation of material science technologies. In this article, we provide an overview of the similarities between materials and living cells, and discuss specific types of biological materials including cytoskeletal elements, DNA, and molecular motors that have already been leveraged to build unique functional materials. The future challenge will be to continue to use the scientific discoveries of today with upcoming discoveries in cellular and molecular science, and apply these principles to develop as yet unknown technologies and materials.

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Regulation and Assembly of Actomyosin Contractile Rings in Cytokinesis and Cell Repair

Dekraker

Boucher

Mandato

2018

The Anatomical Record

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Cytokinesis and single‐cell wound repair both involve contractile assemblies of filamentous actin (F‐actin) and myosin II organized into characteristic ring‐like arrays. The assembly of these actomyosin contractile rings (CRs) is specified spatially and temporally by small Rho GTPases, which trigger local actin polymerization and myosin II contractility via a variety of downstream effectors. We now have a much clearer view of the Rho GTPase signaling cascade that leads to the formation of CRs, but some factors involved in CR positioning, assembly, and function remain poorly understood. Recent studies show that this regulation is multifactorial and goes beyond the long‐established Ca2+‐dependent processes. There is substantial evidence that the Ca2+‐independent changes in cell shape, tension, and plasma membrane composition that characterize cytokinesis and single‐cell wound repair also regulate CR formation. Elucidating the regulation and mechanistic properties of CRs is important to our understanding of basic cell biology and holds potential for therapeutic applications in human disease. In this review, we present a primer on the factors influencing and regulating CR positioning, assembly, and contraction as they occur in a variety of cytokinetic and single‐cell wound repair models. Anat Rec, 301:2051–2066, 2018. © 2018 Wiley Periodicals, Inc.

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Balance of actively generated contractile and resistive forces controls cytokinesis dynamics

Cited by 112 publications

References 38 publications

Mechanochemical Signaling Directs Cell-Shape Change

Mechanochemical Signaling Directs Cell-Shape Change

Using Lessons from Cellular and Molecular Structures for Future Materials

Regulation and Assembly of Actomyosin Contractile Rings in Cytokinesis and Cell Repair

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