Interactions between Myosin and Actin Crosslinkers Control Cytokinesis Contractility Dynamics and Mechanics

Elizabeth M. Reichl, Yixin Ren, Mary K. Morphew, Michael Delannoy, Janet C. Effler, Kristine D. Girard, Srikanth Divi, Pablo A Iglesias, Scot C Kuo, Douglas Robinson

Research output: Contribution to journalArticle

Abstract

Introduction: Contractile networks are fundamental to many cellular functions, particularly cytokinesis and cell motility. Contractile networks depend on myosin-II mechanochemistry to generate sliding force on the actin polymers. However, to be contractile, the networks must also be crosslinked by crosslinking proteins, and to change the shape of the cell, the network must be linked to the plasma membrane. Discerning how this integrated network operates is essential for understanding cytokinesis contractility and shape control. Here, we analyzed the cytoskeletal network that drives furrow ingression in Dictyostelium. Results: We establish that the actin polymers are assembled into a meshwork and that myosin-II does not assemble into a discrete ring in the Dictyostelium cleavage furrow of adherent cells. We show that myosin-II generates regional mechanics by increasing cleavage furrow stiffness and slows furrow ingression during late cytokinesis as compared to myoII nulls. Actin crosslinkers dynacortin and fimbrin similarly slow furrow ingression and contribute to cell mechanics in a myosin-II-dependent manner. By using FRAP, we show that the actin crosslinkers have slower kinetics in the cleavage furrow cortex than in the pole, that their kinetics differ between wild-type and myoII null cells, and that the protein dynamics of each crosslinker correlate with its impact on cortical mechanics. Conclusions: These observations suggest that myosin-II along with actin crosslinkers establish local cortical tension and elasticity, allowing for contractility independent of a circumferential cytoskeletal array. Furthermore, myosin-II and actin crosslinkers may influence each other as they modulate the dynamics and mechanics of cell-shape change.

Original languageEnglish (US)
Pages (from-to)471-480
Number of pages10
JournalCurrent Biology
Volume18
Issue number7
DOIs
StatePublished - Apr 8 2008

Fingerprint

Myosin Type II
Cytokinesis
cytokinesis
Myosins
myosin
furrows
Mechanics
mechanics
actin
Actins
Dictyostelium
Cell Shape
cells
polymers
Polymers
kinetics
Null Lymphocytes
Kinetics
Elasticity
Cell membranes

Keywords

  • CELLBIO
  • CELLCYCLE

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)

Cite this

Interactions between Myosin and Actin Crosslinkers Control Cytokinesis Contractility Dynamics and Mechanics. / Reichl, Elizabeth M.; Ren, Yixin; Morphew, Mary K.; Delannoy, Michael; Effler, Janet C.; Girard, Kristine D.; Divi, Srikanth; Iglesias, Pablo A; Kuo, Scot C; Robinson, Douglas.

In: Current Biology, Vol. 18, No. 7, 08.04.2008, p. 471-480.

Research output: Contribution to journalArticle

Reichl, Elizabeth M. ; Ren, Yixin ; Morphew, Mary K. ; Delannoy, Michael ; Effler, Janet C. ; Girard, Kristine D. ; Divi, Srikanth ; Iglesias, Pablo A ; Kuo, Scot C ; Robinson, Douglas. / Interactions between Myosin and Actin Crosslinkers Control Cytokinesis Contractility Dynamics and Mechanics. In: Current Biology. 2008 ; Vol. 18, No. 7. pp. 471-480.
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AU - Effler, Janet C.

AU - Girard, Kristine D.

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N2 - Introduction: Contractile networks are fundamental to many cellular functions, particularly cytokinesis and cell motility. Contractile networks depend on myosin-II mechanochemistry to generate sliding force on the actin polymers. However, to be contractile, the networks must also be crosslinked by crosslinking proteins, and to change the shape of the cell, the network must be linked to the plasma membrane. Discerning how this integrated network operates is essential for understanding cytokinesis contractility and shape control. Here, we analyzed the cytoskeletal network that drives furrow ingression in Dictyostelium. Results: We establish that the actin polymers are assembled into a meshwork and that myosin-II does not assemble into a discrete ring in the Dictyostelium cleavage furrow of adherent cells. We show that myosin-II generates regional mechanics by increasing cleavage furrow stiffness and slows furrow ingression during late cytokinesis as compared to myoII nulls. Actin crosslinkers dynacortin and fimbrin similarly slow furrow ingression and contribute to cell mechanics in a myosin-II-dependent manner. By using FRAP, we show that the actin crosslinkers have slower kinetics in the cleavage furrow cortex than in the pole, that their kinetics differ between wild-type and myoII null cells, and that the protein dynamics of each crosslinker correlate with its impact on cortical mechanics. Conclusions: These observations suggest that myosin-II along with actin crosslinkers establish local cortical tension and elasticity, allowing for contractility independent of a circumferential cytoskeletal array. Furthermore, myosin-II and actin crosslinkers may influence each other as they modulate the dynamics and mechanics of cell-shape change.

AB - Introduction: Contractile networks are fundamental to many cellular functions, particularly cytokinesis and cell motility. Contractile networks depend on myosin-II mechanochemistry to generate sliding force on the actin polymers. However, to be contractile, the networks must also be crosslinked by crosslinking proteins, and to change the shape of the cell, the network must be linked to the plasma membrane. Discerning how this integrated network operates is essential for understanding cytokinesis contractility and shape control. Here, we analyzed the cytoskeletal network that drives furrow ingression in Dictyostelium. Results: We establish that the actin polymers are assembled into a meshwork and that myosin-II does not assemble into a discrete ring in the Dictyostelium cleavage furrow of adherent cells. We show that myosin-II generates regional mechanics by increasing cleavage furrow stiffness and slows furrow ingression during late cytokinesis as compared to myoII nulls. Actin crosslinkers dynacortin and fimbrin similarly slow furrow ingression and contribute to cell mechanics in a myosin-II-dependent manner. By using FRAP, we show that the actin crosslinkers have slower kinetics in the cleavage furrow cortex than in the pole, that their kinetics differ between wild-type and myoII null cells, and that the protein dynamics of each crosslinker correlate with its impact on cortical mechanics. Conclusions: These observations suggest that myosin-II along with actin crosslinkers establish local cortical tension and elasticity, allowing for contractility independent of a circumferential cytoskeletal array. Furthermore, myosin-II and actin crosslinkers may influence each other as they modulate the dynamics and mechanics of cell-shape change.

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