Septin rings act as template for myosin higher-order structures and inhibit redundant polarity establishment

Schneider, Carolin; Grois, Julia; Renz, Christian; Gronemeyer, Thomas; Johnsson, Nils

doi:10.1242/jcs.125302

Cited by 42 publications

(61 citation statements)

References 52 publications

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“…Based on microscopy alone (not growth or viability assays), this permanent tethering of C-terminally tagged Bni5 to intact Shs1 had only a minor deleterious effect on the timing of the execution of cytokinesis. The fact that, in our hands, both an Shs1-Bni5-eGFP and an Shs1-eGFP-Bni5 chimera supported robust growth, even in cdc10D cells where the rate of proliferation is already markedly slower than in wild-type cells, indicates that the detriment to maintaining (additional) Bni5 at the bud neck during cytokinesis is rather modest, despite the fact that, normally, native Bni5 is displaced from the septin ring prior to the onset of actomyosin ring ingression (Lee et al 2002;Fang et al 2010;Schneider et al 2013).…”

Section: Only the C-terminal Third Of Bni5 Is Required For Its Functionmentioning

confidence: 53%

“…Similar to one of the strategies we employed, one previous study examined the effect of fusing Bni5-mCherry to the C terminus of full-length Shs1 (Schneider et al 2013). Based on microscopy alone (not growth or viability assays), this permanent tethering of C-terminally tagged Bni5 to intact Shs1 had only a minor deleterious effect on the timing of the execution of cytokinesis.…”

Section: Only the C-terminal Third Of Bni5 Is Required For Its Functionmentioning

confidence: 99%

“…Cumulative evidence indicates that Bni5 is a septin-associated protein (Lee et al 2002) and that it has a role in localizing Myo1 to the bud neck prior to the onset of cytokinesis (Fang et al 2010;Schneider et al 2013). However, how Bni5 is recruited to the septin collar has been unclear.…”

Section: Loss Of Bni5 Phenocopies the Growth And Morphology Defects Omentioning

confidence: 99%

“…Thus, efficient subcellular recruitment to the septin collar alone is not sufficient for Bni5 function. It is important to point out that all previous studies to localize Bni5 used C-terminally tagged derivatives (Lee et al 2002;Nam et al 2007a;Fang et al 2010;Renz et al 2013;Schneider et al 2013).…”

Section: Only the C-terminal Third Of Bni5 Is Required For Its Functionmentioning

confidence: 99%

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The Carboxy-Terminal Tails of Septins Cdc11 and Shs1 Recruit Myosin-II Binding Factor Bni5 to the Bud Neck in Saccharomyces cerevisiae

Finnigan¹,

Booth²,

Duvalyan³

et al. 2015

Genetics

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Septins are a conserved family of GTP-binding proteins that form heterooctameric complexes that assemble into higher-order structures. In yeast, septin superstructure at the bud neck serves as a barrier to separate a daughter cell from its mother and as a scaffold to recruit the proteins that execute cytokinesis. However, how septins recruit specific factors has not been well characterized. In the accompanying article in this issue, , we demonstrated that the C-terminal extensions (CTEs) of the alternative terminal subunits of septin heterooctamers, Cdc11 and Shs1, share a role required for optimal septin function in vivo. Here we describe our use of unbiased genetic approaches (both selection of dosage suppressors and analysis of synthetic interactions) that pinpointed Bni5 as a protein that interacts with the CTEs of Cdc11 and Shs1. Furthermore, we used three independent methods-construction of chimeric proteins, noncovalent tethering mediated by a GFP-targeted nanobody, and imaging by fluorescence microscopy-to confirm that a physiologically important function of the CTEs of Cdc11 and Shs1 is optimizing recruitment of Bni5 and thereby ensuring efficient localization at the bud neck of Myo1, the type II myosin of the actomyosin contractile ring. KEYWORDS yeast; cytokinesis; complexes; filaments; mutants S EPTIN-based structures in metazoans are frequently found at the boundaries between cellular compartments (Saarikangas and Barral 2011;Trimble and Grinstein 2015). The tissue specificity with which septin genes are expressed, and/or their mRNAs undergo alternative splicing, is consistent with specific septins and septin isoforms playing distinct roles in particular developmental and physiological processes (Roeseler et al. 2009;Hall and Russell 2012;Dolat et al. 2014). A prominent septin-containing structure is located at the bottom of the neck of each small membranous protrusion (dendritic spine) that projects from the dendrites that extend from the cell body of a neuron (Tada et al. 2007;Ewers et al. 2014), indicating some role in neurogenesis. A discrete septincontaining structure, dubbed the annulus, separates the head and midpiece from the flagellum in mature mammalian sperm and is required for sperm motility (Sugino et al. 2008;Toure et al. 2011). Similarly, septin function has been implicated in the amoeboid motility of T cells by promoting membrane retraction (Tooley et al. 2009;Gilden et al. 2012). Septincontaining structures are found at the base of the primary (nonmotile) cilium and at discrete regions along the axoneme, suggesting roles in ciliogenesis and in the signaling functions of this sensory organelle (Hu et al. 2010;Ghossoub et al. 2013;Sharma et al. 2013). Septin "cages" assemble around intracellular bacterial pathogens or the vacuolar inclusions that contain them, but whether caging serves as a first line of defense against their spread (Mostowy et al. 2010), or is exploited by the microbes to promote their spread (Volceanov et al. 2014), has not been resolved. In all the instanc...

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Section: Only the C-terminal Third Of Bni5 Is Required For Its Functionmentioning

confidence: 53%

Section: Only the C-terminal Third Of Bni5 Is Required For Its Functionmentioning

confidence: 99%

Section: Loss Of Bni5 Phenocopies the Growth And Morphology Defects Omentioning

confidence: 99%

Section: Only the C-terminal Third Of Bni5 Is Required For Its Functionmentioning

confidence: 99%

See 2 more Smart Citations

The Carboxy-Terminal Tails of Septins Cdc11 and Shs1 Recruit Myosin-II Binding Factor Bni5 to the Bud Neck in Saccharomyces cerevisiae

Finnigan¹,

Booth²,

Duvalyan³

et al. 2015

Genetics

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“…To confirm aspects of the Iqg1p-Hof1p interaction in vivo, we fused IQ9-11-CHERRY to the t-SNARE Sso1p (Schneider et al, 2013). The Sso1 moiety in the IQ9-11-CHERRY-Sso1p fusion caused the relocation of IQ9-11 homogenously to the plasma membrane (Fig.…”

Section: Mutations In Iqg1p That Disrupt Its Interaction With Hof1pmentioning

confidence: 99%

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

Tian

Johnsson

2014

Journal of Cell Science

Self Cite

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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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Architecture, remodeling, and functions of the septin cytoskeleton

Marquardt

Chen

2018

Cytoskeleton

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The septin family of proteins has fascinated cell biologists for decades due to the elaborate architecture they adopt in different eukaryotic cells. Whether they exist as rings, collars, or gauzes in different cell types and at different times in the cell cycle illustrates a complex series of regulation in structure. While the organization of different septin structures at the cortex of different cell types during the cell cycle has been described to various degrees, the exact structure and regulation at the filament level are still largely unknown. Recent advances in fluorescent and electron microscopy, as well as work in septin biochemistry, have allowed new insights into the aspects of septin architecture, remodeling, and function in many cell types. This mini-review highlights many of the recent findings with an emphasis on the budding yeast model.

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Septin rings act as template for myosin higher-order structures and inhibit redundant polarity establishment

Cited by 42 publications

References 52 publications

The Carboxy-Terminal Tails of Septins Cdc11 and Shs1 Recruit Myosin-II Binding Factor Bni5 to the Bud Neck in Saccharomyces cerevisiae

The Carboxy-Terminal Tails of Septins Cdc11 and Shs1 Recruit Myosin-II Binding Factor Bni5 to the Bud Neck in Saccharomyces cerevisiae

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

Architecture, remodeling, and functions of the septin cytoskeleton

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