Assembly Mechanism of the Contractile Ring for Cytokinesis by Fission Yeast

Vavylonis, Dimitrios; Wu, Jian-Qiu; Sheng, Hao; O’Shaughnessy, Ben; Pollard, Thomas D.

doi:10.1126/science.1151086

Cited by 361 publications

(638 citation statements)

References 19 publications

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“…Later, cortical nodes coalesce during the 'lateral condensation' process to form a ring structure. 8,[12][13][14] Concomitantly, F-actin cables are formed in parallel in the cell centre and are packed as a ring. A homogeneous ring structure is achieved by the incorporation of the FER/CIP4 homology (FCH) domain protein Cdc15.…”

Section: Introductionmentioning

confidence: 99%

Role of the protein kinase Kin1 and nuclear centering in actomyosin ring formation in fission yeast

Cadou¹,

Carbona²,

Couturier³

et al. 2009

Cell Cycle

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Cytokinesis is the last step of the cell cycle, producing two daughter cells inheriting equal genetic information. This process involves the assembly of an actomyosin ring during mitosis. In the fission yeast Schizosaccharomyces pombe, cytokinesis occurs at the geometric cell centre, a position which is defined by the interphase nucleus and the anilin-related Mid1 protein. The pom1Δ, tea1Δ and tea4Δ mutants are defective in restricting Mid1 as a band around the nucleus and misplace the division site. We previously reported that inhibition of the protein kinase Kin1 promoted failure of cytokinesis in pom1Δ and tea1Δ cells but the mechanism involving Kin1 remained elusive. Here we investigated the contribution of Kin1 in cytokinesis. We show that Kin1-GFP has a dynamic cell cycle regulated distribution. Like pom1Δ and tea1Δ, tea4Δ exhibits a strong genetic interaction with kin1Δ. Using a conditional repressible kin1 allele that only alters interphase nuclear centering, we observed that Kin1 downregulation severely compromised actomyosin ring formation and septum synthesis in tea4Δ cells. In addition, nuclear displacement induced either by overexpression of a putative catalytically inactive Kin1 mutant, by chemically mediated microtubule depolymerization or by mutation in the par1Δ gene impaired cytokinesis in tea4Δ but not tea4 + cells. We propose that nuclear mispositioning exacerbates the tea4Δ, pom1Δ and tea1Δ cell division phenotype. Our work reveal that nuclear centering becomes essential when Pom1/Tea1/Tea4 function is compromised and that Kin1 expression level is a key regulatory element in this situation. Our results suggest the existence of distinct overlapping control mechanisms to ensure efficient cell division.

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Section: Introductionmentioning

confidence: 99%

Role of the protein kinase Kin1 and nuclear centering in actomyosin ring formation in fission yeast

Cadou¹,

Carbona²,

Couturier³

et al. 2009

Cell Cycle

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“…Two major models have been proposed. The Search, Capture, Pull, and Release (SCPR) n 772Rincon and Paoletti CYTOSKELETON model proposes that actin filaments nucleated by Cdc12 from each node search for nearby nodes, in which Myo2 captures actin filaments and produces the force necessary to pull nodes together, resulting in the condensation into a ring structure [Wu et al, 2006;Vavylonis et al, 2008;Ojkic et al, 2011]. The alternate Cdc12 Spot-Leading Cable model proposes that a major Cdc12 spot moves toward the cell middle and nucleates an actin leading cable beneath the plasma membrane and perpendicular to the long axis of the cell, which eventually gives rise to the contractile ring [Chang, 1999;Kamasaki et al, 2007].…”

mentioning

confidence: 99%

Mid1/anillin and the spatial regulation of cytokinesis in fission yeast

Rincón

Paoletti

2012

Cytoskeleton

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Cell division is a critical and irreversible step in the cell cycle. The strategies that cells follow to regulate the position of the division plane must take into account the global geometry of the cell as well as position of the genetic material to ensure its accurate segregation into daughter cells of a given cell shape and size. Along the years, research on Schizosaccharomyces pombe, a wellrecognized model organism for cell division studies has allowed a detailed molecular understanding of the spatial mechanisms regulating cytokinesis. Division plane position in this unicellular rod-shaped organism, which divides by the assembly and constriction of a medially placed actomyosin ring, largely depends on the anillinlike protein Mid1. Therefore, the major pathways controlling the position of the division plane converge on Mid1. In this review, we make an overview of the studies that have deciphered how Mid1 localization and scaffolding activities are controlled over the cell cycle to ensure the symmetrical division of fission yeast cells. These studies have revealed new mechanisms generating spatial information based on nuclear shuttling of the division plane factor Mid1 and on the establishment of cortical inhibitory gradients of the cell polarity kinase Pom1. V C 2012 Wiley Periodicals, Inc Key Words: cytokinesis, fission yeast, contractile ring, Mid1, cell division Introduction C ytokinesis is the final step of cell division that physically separates the daughter cells at the end of the cell cycle. It is a universal process, essential for cell proliferation, for the survival of unicellular organisms or for the development of multicellular organisms, whose major features have been well conserved along evolution. As an irreversible event, cytokinesis is under tight spatial and temporal regulation. Defective cytokinesis can indeed alter cell geometry or size, perturb cellular organization within tissues or prevent the accurate transmission of the genetic material, producing aneuploid cells, which can affect the survival of unicellular species or favor cancer and tumor progression in animal species.Cytokinesis is first strictly coordinated with mitotic progression in order to successfully fulfill chromosome segregation. Checkpoint mechanisms monitoring the function of the mitotic apparatus can halt cells in metaphase, which prevents cytokinesis until actual chromosome segregation in anaphase.Second, spatial regulatory pathways define the position of the division plane according to the position of the nucleus at mitotic entry, or of the mitotic apparatus, perpendicular to the axis of chromosome segregation. This ensures the efficient segregation of the genetic material and allows to control the geometry of the daughter cells in response to morphogenetic programs. Cell division can indeed be symmetric or asymmetric to allow the generation of daughter cells of different sizes. Orientation of the division plane is also modulated to properly position the daughter cells inside embryos or tissues and to permit the asymm...

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“…In the mature ring, the actin filaments average 600 nm in length and show interdigitation. Live-imaging studies with fluorescent proteins revealed that the contractile ring assembles from a series of cortical nodes that contain myosin motors and simultaneously nucleate actin assembly (Vavylonis et al 2008). These nodes assemble into rings by means of a pathway that will be discussed in detail below.…”

Section: Accessory Structures In Fission and Budding Yeastmentioning

confidence: 99%

“…These two types of nodes fuse in late G 2 in the cell center, and some type 1 node components dissipate from these hybrid, cytokinetic nodes during M phase ( . These nodes then undergo a wellcharacterized ring assembly process that will be discussed below (Vavylonis et al 2008). Mid1 likely induces local concentration of contractile ring components, as artificial targeting of several ring components to nodes can largely restore cytokinesis in mid1 mutant cells (Tao et al 2014).…”

Section: Contractile Ring Positioning In Fission Yeastmentioning

confidence: 99%

“…The aforementioned nodes that contain myosin and formin nucleate actin filaments that are captured by neighboring nodes and pulled together (Vavylonis et al 2008). The barbed end of the growing actin filament is anchored by the nucleating formin at the donor node, and the pointed end of the filament is captured by myosin at the acceptor node (Laporte et al 2011).…”

Section: Contractile Ring Assembly In Fission Yeastmentioning

confidence: 99%

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Cytokinesis in Metazoa and Fungi

Glotzer

2016

Cold Spring Harb Perspect Biol

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SUMMARYCell division-cytokinesis-involves large-scale rearrangements of the entire cell. Primarily driven by cytoskeletal proteins, cytokinesis also depends on topological rearrangements of the plasma membrane, which are coordinated with nuclear division in both space and time. Despite the fundamental nature of the process, different types of eukaryotic cells show variations in both the structural mechanisms of cytokinesis and the regulatory controls. In animal cells and fungi, a contractile actomyosin-based structure plays a central, albeit flexible, role. Here, the underlying molecular mechanisms are summarized and integrated and common themes are highlighted.

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Assembly Mechanism of the Contractile Ring for Cytokinesis by Fission Yeast

Cited by 361 publications

References 19 publications

Role of the protein kinase Kin1 and nuclear centering in actomyosin ring formation in fission yeast

Role of the protein kinase Kin1 and nuclear centering in actomyosin ring formation in fission yeast

Mid1/anillin and the spatial regulation of cytokinesis in fission yeast

Cytokinesis in Metazoa and Fungi

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