A theoretical model of cytokinesis implicates feedback between membrane curvature and cytoskeletal organization in asymmetric cytokinetic furrowing

Jonas F. Dorn, Li Zhang, Tan Trao Phi, Benjamin Lacroix, Paul S. Maddox, Jian Liu, Amy Shaub Maddox

Research output: Contribution to journalArticle

Abstract

During cytokinesis, the cell undergoes a dramatic shape change as it divides into two daughter cells. Cell shape changes in cytokinesis are driven by a cortical ring rich in actin filaments and nonmuscle myosin II. The ring closes via actomyosin contraction coupled with actin depolymerization. Of interest, ring closure and hence the furrow ingression are nonconcentric (asymmetric) within the division plane across Metazoa. This nonconcentricity can occur and persist even without preexisting asymmetric cues, such as spindle placement or cellular adhesions. Cell-autonomous asymmetry is not explained by current models. We combined quantitative high-resolution live-cell microscopy with theoretical modeling to explore the mechanistic basis for asymmetric cytokinesis in the Caenorhabditis elegans zygote, with the goal of uncovering basic principles of ring closure. Our theoretical model suggests that feedback among membrane curvature, cytoskeletal alignment, and contractility is responsible for asymmetric cytokinetic furrowing. It also accurately predicts experimental perturbations of conserved ring proteins. The model further suggests that curvature-mediated filament alignment speeds up furrow closure while promoting energy efficiency. Collectively our work underscores the importance of membrane-cytoskeletal anchoring and suggests conserved molecular mechanisms for this activity.

Original languageEnglish (US)
Pages (from-to)1286-1299
Number of pages14
JournalMolecular Biology of the Cell
Volume27
Issue number8
DOIs
StatePublished - Apr 15 2016
Externally publishedYes

Fingerprint

Cytokinesis
Theoretical Models
Membranes
Myosin Type II
Actomyosin
Cell Shape
Zygote
Caenorhabditis elegans
Actin Cytoskeleton
Cues
Actins
Microscopy
Efficiency
Proteins

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

A theoretical model of cytokinesis implicates feedback between membrane curvature and cytoskeletal organization in asymmetric cytokinetic furrowing. / Dorn, Jonas F.; Zhang, Li; Phi, Tan Trao; Lacroix, Benjamin; Maddox, Paul S.; Liu, Jian; Maddox, Amy Shaub.

In: Molecular Biology of the Cell, Vol. 27, No. 8, 15.04.2016, p. 1286-1299.

Research output: Contribution to journalArticle

Dorn, Jonas F. ; Zhang, Li ; Phi, Tan Trao ; Lacroix, Benjamin ; Maddox, Paul S. ; Liu, Jian ; Maddox, Amy Shaub. / A theoretical model of cytokinesis implicates feedback between membrane curvature and cytoskeletal organization in asymmetric cytokinetic furrowing. In: Molecular Biology of the Cell. 2016 ; Vol. 27, No. 8. pp. 1286-1299.
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