Distinct roles of Rho1, Cdc42, and Cyk3 in septum formation and abscission during yeast cytokinesis

Onishi, Masayuki; Ko, Nolan; Nishihama, Ryuichi; Pringle, John R.

doi:10.1083/jcb.201302001

Cited by 66 publications

(116 citation statements)

References 105 publications

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“…1, top). In contrast to the budding yeast Saccharomyces cerevisiae, where the SS appears to be assembled after the PS is completed (38), fission yeast septum grows by simultaneous synthesis of both the PS and the SS (8,10). After septum completion, the septum thickness increases in a maturation process involving an additional round of SS synthesis.…”

Section: Septum Composition and Structurementioning

confidence: 99%

The Cell Biology of Fission Yeast Septation

Cortés

Ramos

Osumi

et al. 2016

Microbiol Mol Biol Rev

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SUMMARYIn animal cells, cytokinesis requires the formation of a cleavage furrow that divides the cell into two daughter cells. Furrow formation is achieved by constriction of an actomyosin ring that invaginates the plasma membrane. However, fungal cells contain a rigid extracellular cell wall surrounding the plasma membrane; thus, fungal cytokinesis also requires the formation of a special septum wall structure between the dividing cells. The septum biosynthesis must be strictly coordinated with the deposition of new plasma membrane material and actomyosin ring closure and must occur in such a way that no breach in the cell wall occurs at any time. Because of the high turgor pressure in the fungal cell, even a minor local defect might lead to cell lysis and death. Here we review our knowledge of the septum structure in the fission yeastSchizosaccharomyces pombeand of the recent advances in our understanding of the relationship between septum biosynthesis and actomyosin ring constriction and how the two collaborate to build a cross-walled septum able to support the high turgor pressure of the cell. In addition, we discuss the importance of the septum biosynthesis for the steady ingression of the cleavage furrow.

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Section: Septum Composition and Structurementioning

confidence: 99%

The Cell Biology of Fission Yeast Septation

Cortés

Ramos

Osumi

et al. 2016

Microbiol Mol Biol Rev

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“…Specifically, failure to inactivate Cdc42 leads to failed cell abscission in budding yeast and HeLa cells, and prevents cellularization in Drosophila embryos (Atkins et al, 2013;Crawford et al, 1998;Dutartre et al, 1996;Onishi et al, 2013). The mechanism by which Cdc42 is inactivated prior to cell abscission has not been investigated in fission yeast.…”

Section: Crosstalk Between Gef1 and Scd1 During Cytokinesismentioning

confidence: 99%

A novel interplay between GEFs orchestrates Cdc42 activity during cell polarity and cytokinesis

Hercyk

Rich

Das

2018

Preprint

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Cdc42, a conserved regulator of cell polarity, is activated by two GEFs, Gef1 and Scd1, in fission yeast. While gef1 and scd1 mutants exhibit distinct phenotypes, how they do so is unclear given that they activate the same GTPase. Using the GEF localization pattern during cytokinesis as a paradigm, we report a novel interplay between Gef1 and Scd1 that spatially modulates Cdc42. We find that Gef1 promotes Scd1 localization to the division site during cytokinesis and to the new end during polarized growth through the recruitment of the scaffold Scd2 via a Cdc42 feedforward pathway. Gef1-mediated Scd1 recruitment at the new end enables the transition from monopolar to bipolar growth. Reciprocally, Scd1 restricts Gef1 localization to prevent ectopic Cdc42 activation during cytokinesis to promote cell separation and during interphase to maintain cell shape. Our findings reveal an elegant regulatory pattern in which Gef1 establishes new sites of Scd1-mediated Cdc42 activity, while Scd1 restricts Gef1 to functional sites. We propose that crosstalk between GEFs is a conserved mechanism that orchestrates Cdc42 activation during complex cellular processes.Summary StatementCdc42 GEFs Gef1 and Scd1 crosstalk to fine-tune Cdc42 activity. This crosstalk promotes bipolar growth and maintains cell shape in fission yeast.

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“…The deletions of MYO1 or CYK3 are tolerated in wild-type cells but are synthetic lethal to each other and to a deletion of HOF1 (Korinek et al, 2000;Vallen et al, 2000). Dcyk3 cells display defects in primary septum formation and thus depend on a functional AMR for survival (Meitinger et al, 2010;Onishi et al, 2013) (Fig. 5C, complex 1).…”

Section: Mutations In Iqg1p That Disrupt Its Interaction With Hof1pmentioning

confidence: 99%

“…By contrast, the deletion of CHS2 affects not only septum formation but also AMR contraction and plasma membrane ingression (VerPlank and Li, 2005). Both the formation of the primary and secondary septum are important for the final abscission of the daughter cell at the end of cytokinesis (Barr and Gruneberg, 2007;Onishi et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…One of the unresolved issues concerns the existence and composition of a central element of cytokinesis that is proposed to link and coordinate AMR contraction with septum synthesis in yeast or with extracellular matrix remodeling in the case of animal cells (Bi and Park, 2012;Onishi et al, 2013). Iqg1p was tentatively assigned this important regulatory role in yeast (Bi and Park, 2012;Onishi et al, 2013). Starting from a systematic split-ubiquitin screen, we characterize a newly identified interaction between Iqg1p and Hof1p in a mechanistic detail that allows addressing it as a bridge between AMR contraction, membrane ingression and septum synthesis during cytokinesis.…”

Section: Introductionmentioning

confidence: 99%

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Stepwise and cooperative assembly of a cytokinetic core complex in yeast Saccharomyces cerevisiae

Tian

Johnsson

2014

Journal of Cell Science

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Actomyosin ring (AMR) contraction and the synthesis of an extracellular septum are interdependent pathways that mediate cytokinesis in the yeast Saccharomyces cerevisiae and other eukaryotes. How these interdependent pathways are physically connected is central for understanding cytokinesis. The yeast IQGAP (Iqg1p) belongs to the conserved AMR. The F-BAR-domaincontaining protein Hof1p is a member of a complex that stimulates cell wall synthesis. We report here on the stepwise formation of a physical connection between both proteins. The C-terminal IQrepeats of Iqg1p first bind to the essential myosin light chain before both proteins assemble with Hof1p into the Mlc1p-Iqg1p-Hof1p (MIH) bridge. Mutations in Iqg1p that disrupt the MIH complex alter Hof1p targeting to the AMR and impair AMR contraction. Epistasis analyses of two IQG1 alleles that are incompatible with formation of the MIH complex support the existence and functional significance of a large cytokinetic core complex. We propose that the MIH complex acts as hinge between the AMR and the proteins involved in cell wall synthesis and membrane attachment.

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Distinct roles of Rho1, Cdc42, and Cyk3 in septum formation and abscission during yeast cytokinesis

Abstract: Rho1 inactivation by Cyk3 promotes primary septum formation and cleavage-furrow ingression, whereas Rho1 activation or Cdc42 inactivation promotes secondary septum formation and abscission.

Cited by 66 publications

References 105 publications

The Cell Biology of Fission Yeast Septation

The Cell Biology of Fission Yeast Septation

A novel interplay between GEFs orchestrates Cdc42 activity during cell polarity and cytokinesis

Stepwise and cooperative assembly of a cytokinetic core complex in yeast Saccharomyces cerevisiae

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