title: A theoretical model of cytokinesis implicates feedback between membrane curvature and cytoskeletal organization in asymmetric cytokinetic furrowing.
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 theCaenorhabditis eleganszygote, 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.
authors.affiliation: Institute for Research in Immunology and Cancer, Université de Montréal, Montréal, QC H3T 1J4, Canada.
authors.forename: Jonas F
authors.initials: JF
authors.lastname: Dorn
authors.affiliation: Institute for Research in Immunology and Cancer, Université de Montréal, Montréal, QC H3T 1J4, Canada.
authors.forename: Li
authors.initials: L
authors.lastname: Zhang
authors.affiliation: Institute for Research in Immunology and Cancer, Université de Montréal, Montréal, QC H3T 1J4, Canada.
authors.forename: Tan-Trao
authors.initials: TT
authors.lastname: Phi
authors.affiliation: Institut Jacques Monod, 75205 Paris cedex 13, France.
authors.forename: Benjamin
authors.initials: B
authors.lastname: Lacroix
authors.affiliation: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599.
authors.forename: Paul S
authors.initials: PS
authors.lastname: Maddox
authors.affiliation: Biochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20814 jian.liu@nih.gov asm@unc.edu.
authors.forename: Jian
authors.initials: J
authors.lastname: Liu
authors.affiliation: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599 jian.liu@nih.gov asm@unc.edu.
authors.forename: Amy Shaub
authors.initials: AS
authors.lastname: Maddox
mesh_terms: D008841:Actin Cytoskeleton / Q000378:metabolism; D000818:Animals; D017173:Caenorhabditis elegans / Q000166:cytology*; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism; D002462:Cell Membrane; D048749:Cytokinesis / Q000502:physiology; D003599:Cytoskeleton / Q000378:metabolism; D025461:Feedback, Physiological; D008840:Microfilament Proteins / Q000378:metabolism; D008954:Models, Biological; D024462:Myosin Type II / Q000378:metabolism
chemical_list: C502566:ANI-1 protein, C elegans; D029742:Caenorhabditis elegans Proteins; D008840:Microfilament Proteins; D024462:Myosin Type II