Mechanics and regulation of cytokinesis in budding yeast

Bhavsar-Jog, Yogini P.; Bi, Erfei

doi:10.1016/j.semcdb.2016.12.010

Cited by 46 publications

(108 citation statements)

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“…As CAR constricts, a primary septum flanked by secondary septa is formed behind the CAR, and after closure of the CAR, the primary septum is degraded by the glucanases Eng1p and Agn1p, which are delivered to the septum in a septin-dependent manner [13,14]. The primary septum mainly comprises linear b (1,3) glucans that are synthesized by the glucan synthase Bgs1p while the secondary septum contains linear b(1,3) glucans, branched b(1,3) glucans (synthesized by Bgs4p), and a (1,3) glucans (synthesized by Ags1p) [25]. It remains unknown if septins function to regulate these glucan synthases.…”

Section: Introductionmentioning

confidence: 99%

Septins regulate the equatorial dynamics of the separation initiation network kinase Sid2p and glucan synthases to ensure proper cytokinesis

et al. 2018

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Septins generally function as scaffolds and as cortical barriers to restrict the diffusion of membrane proteins. In the fission yeast Schizosaccharomyces pombe, septins form a ring structure at the septum after spindle breakdown during the constriction of the contractile actomyosin ring (CAR) and serve as a scaffold to recruit glucanases to mediate ultimate daughter cell separation. Despite this, it remains unclear if septins play any significant roles before the cell separation during cytokinesis. Employing live cell microscopy, we carefully examined SIN (Septation Initiation Network) signaling and glucan synthases, two key factors ensuring proper function of the CAR. In the absence of the core septin component Spn1p, the formation of a compact CAR is advanced and the CAR constriction rate is slightly but significantly decreased. Moreover, the SIN kinase Sid2p and the glucan synthases Bgs1p and Ags1p form an equatorial ring quite prematurely, but their maintenance at the equatorial region is diminished spn1Δ cells. These findings suggest that septins act as key players in an accurate establishment and the maintenance of CAR by orchestrating the equatorial dynamics of Sid2p and glucan synthases. Hence, this work demonstrates that, in addition to their function during ultimate cell septation, septins have important roles in regulating earlier cytokinetic events, including CAR assembly and constriction, SIN signaling, and the cortical dynamics of the glucan synthases.

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Section: Introductionmentioning

confidence: 99%

Septins regulate the equatorial dynamics of the separation initiation network kinase Sid2p and glucan synthases to ensure proper cytokinesis

et al. 2018

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“…This remodeling is spatiotemporally coordinated with a cytoskeletal structure pertaining to a kingdom of life, for example, the FtsZ ring in bacteria [15], the phragmoplast in plants [16], and the actomyosin ring in fungi and animals [17, 18]. While the cytoskeletal structures have been analyzed extensively, the mechanisms of ECM remodeling remain poorly understood.…”

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confidence: 99%

“…While the cytoskeletal structures have been analyzed extensively, the mechanisms of ECM remodeling remain poorly understood. In the budding yeast Saccharomyces cerevisiae , the ECM remodeling refers to sequential formations of the primary and secondary septa that are catalyzed by chitin synthase-II (Chs2) and chitin synthase-III (the catalytic subunit Chs3 and its activator Chs4), respectively [18, 19]. Surprisingly, both Chs2 and Chs3 are delivered to the division site at the onset of cytokinesis [6, 20].…”

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confidence: 99%

Hof1 and Chs4 Interact via F-BAR Domain and Sel1-like Repeats to Control Extracellular Matrix Deposition during Cytokinesis

Schreiter

Okada

et al. 2017

Current Biology

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SUMMARY Localized extracellular matrix (ECM) remodeling is thought to stabilize the cleavage furrow and maintain cell shape during cytokinesis [1–14]. This remodeling is spatiotemporally coordinated with a cytoskeletal structure pertaining to a kingdom of life, for example, the FtsZ ring in bacteria [15], the phragmoplast in plants [16], and the actomyosin ring in fungi and animals [17, 18]. While the cytoskeletal structures have been analyzed extensively, the mechanisms of ECM remodeling remain poorly understood. In the budding yeast Saccharomyces cerevisiae, the ECM remodeling refers to sequential formations of the primary and secondary septa that are catalyzed by chitin synthase-II (Chs2) and chitin synthase-III (the catalytic subunit Chs3 and its activator Chs4), respectively [18, 19]. Surprisingly, both Chs2 and Chs3 are delivered to the division site at the onset of cytokinesis [6, 20]. What keeps Chs3 inactive until secondary septum formation remains unknown. Here, we show that Hof1 binds to the Sel1-like repeats (SLR) of Chs4 via its F-BAR domain, and inhibits Chs3-mediated chitin synthesis during cytokinesis. In addition, Hof1 is required for rapid accumulation as well as efficient removal of Chs4 at the division site. This study uncovers a mechanism by which Hof1 controls timely activation of Chs3 during cytokinesis, and defines a novel interaction and function for the conserved F-BAR domain and SLR that are otherwise known for their abilities to bind membrane lipids [21, 22] and scaffold protein complex formation [23].

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“…Fundamental aspects of cytokinesis are conserved between yeast and animal cells (Balasubramanian et al, 2004;Bhavsar-Jog and Bi, 2017;Glotzer, 2016). Both yeast and metazoan cells undergo cytokinesis through a sequence of coordinated steps that include AMR contraction, membrane ingression, localized secretion, extracellular matrix (ECM) remodeling, and abscission.…”

Section: How Broadly Conserved Is the Eco Pathway?mentioning

confidence: 99%

A cell separation checkpoint that enforces the proper order of late cytokinetic events

Brace¹,

Doerfler²,

Weiss³

2018

Preprint

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List of Abbreviations:Actomyosin ring (AMR); Primary septum (PS); Secondary septum (SS); Cyclin dependent kinase (CDK); Auxin inducible degron (AID); Immunoprecipitation (IP); Mitotic Exit Network (MEN); Regulation of Ace2 and Morphogenesis network (RAM) SummaryEukaryotic cell division requires sequence dependency relationships in which late processes commence only after early ones are appropriately completed. We have discovered a system that blocks late events of cytokinesis until early ones are successfully accomplished. In budding yeast, cytokinetic actomyosin ring contraction and membrane ingression are coupled with deposition of an extracellular septum that is destroyed immediately after its completion by secreted enzymes. We find this secretion event is linked to septum completion and forestalled when the process is slowed. Delay of septum destruction requires Fir1, an intrinsically disordered protein localized to the cytokinesis site that is degraded upon septum completion but stabilized when septation is aberrant. Fir1 appears to protect cytokinesis in part by inhibiting a separation-specific exocytosis function of the NDR/LATS kinase Cbk1, a key component of a "hippo" signaling pathway that induces mother-daughter separation. We term this system "enforcement of cytokinesis order" (ECO), a checkpoint ensuring proper temporal sequence of mechanistically incompatible processes of cytokinesis.Eukaryotic cells undergo dramatic reorganization at the end of mitosis, producing two cells from one through the processes of cytokinesis. This division requires execution of mechanistically diverse events in an unvarying and often rapid sequence, in which late processes are not initiated until early ones are effectively completed. Specification of the division site and assembly of cytokinetic structures precedes the mechanical and regulatory events of actomyosin ring (AMR) constriction and membrane ingression; this is followed by disassembly of cytokinetic machinery, cessation of cytokinetic membrane trafficking, and abscission of the divided cells (

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Mechanics and regulation of cytokinesis in budding yeast

Cited by 46 publications

References 182 publications

Septins regulate the equatorial dynamics of the separation initiation network kinase Sid2p and glucan synthases to ensure proper cytokinesis

Septins regulate the equatorial dynamics of the separation initiation network kinase Sid2p and glucan synthases to ensure proper cytokinesis

Hof1 and Chs4 Interact via F-BAR Domain and Sel1-like Repeats to Control Extracellular Matrix Deposition during Cytokinesis

A cell separation checkpoint that enforces the proper order of late cytokinetic events

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