Septin Filament Formation Is Essential in Budding Yeast

Division of Biochemistry and Molecular Biology, Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720, USA.
Developmental Cell (Impact Factor: 9.71). 04/2011; 20(4):540-9. DOI: 10.1016/j.devcel.2011.02.004
Source: PubMed


Septins are GTP-binding proteins that form ordered, rod-like multimeric complexes and polymerize into filaments, but how such supramolecular structure is related to septin function was unclear. In Saccharomyces cerevisiae, four septins form an apolar hetero-octamer (Cdc11-Cdc12-Cdc3-Cdc10-Cdc10-Cdc3-Cdc12-Cdc11) that associates end-to-end to form filaments. We show that septin filament assembly displays previously unanticipated plasticity. Cells lacking Cdc10 or Cdc11 are able to divide because the now-exposed subunits (Cdc3 or Cdc12, respectively) retain an ability to homodimerize via their so-called G interface, thereby allowing for filament assembly. In such cdc10Δ and cdc11Δ cells, the remaining septins, like wild-type complexes, localize to the cortex at the bud neck and compartmentalize nonseptin factors, consistent with a diffusion barrier composed of continuous filaments in intimate contact with the plasma membrane. Conversely, Cdc10 or Cdc11 mutants that cannot self-associate, but "cap" Cdc3 or Cdc12, respectively, prevent filament formation, block cortical localization, and kill cells.

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Available from: Michael Mcmurray, Jul 25, 2014
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    • "Mammalian septin-4 specifically binds phosphatidylinositol (4,5)-bisphosphate (PI(4,5)P 2 ; Zhang et al., 1999). In yeast, PI(4,5)P 2 is enriched in membrane areas of polarized growth and the bud neck (Garrenton et al., 2010) and stimulates formation and organization of septin filaments, which are in turn essential for cell viability (Bertin et al., 2010; McMurray et al., 2011). Indeed, in S. cerevisiae, septins are required for cytokinesis by tethering to the division site (i.e., the bud neck) most proteins involved in this process, including components of the contractile actomyosin ring (reviewed in Oh and Bi, 2010; Weirich et al., 2008). "
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    ABSTRACT: In many cell types septins assemble into filaments and rings at the neck of cellular appendages and/or at the cleavage furrow to help compartmentalize the plasma membrane and support cytokinesis. How septin ring assembly is coordinated with membrane remodelling and controlled by mechanical stress at these sites is however unclear.Through a genetic screen we uncovered an unanticipated link between the conserved Rho1 GTPase and its effector protein kinase C (Pkc1) with septin ring stability in yeast. Both Rho1 and Pkc1 stabilize the septin ring, at least partly through phosphorylation of the membrane-associated F-BAR protein Syp1, which colocalizes asymmetrically with the septin ring at the bud neck. Syp1 is displaced from the bud neck upon Pkc1-dependent phosphorylation at two serines, thereby impacting the rigidity of the new-forming septin ring. We propose that Rho1 and Pkc1 coordinate septin ring assembly with membrane and cell wall remodelling partly by controlling Syp1 residence at the bud neck. © 2015 by The American Society for Cell Biology.
    Full-text · Article · Jul 2015 · Molecular biology of the cell
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    • "Previous studies have demonstrated the presence of septin heterooctamers in fungi and heterohexamers in mammals [13], [14], [16], [17], [30]. Our results show that similar heteropolymer units are formed in A. nidulans by core septins AspACdc11, AspBCdc3, AspCCdc12 and AspDCdc10 throughout early development and that AspE is not a member of these heteropolymers. "
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    ABSTRACT: Septins are important components of the cytoskeleton that are highly conserved in eukaryotes and play major roles in cytokinesis, patterning, and many developmental processes. Septins form heteropolymers which assemble into higher-order structures including rings, filaments, and gauzes. In contrast to actin filaments and microtubules, the molecular mechanism by which septins assemble is not well-understood. Here, we report that in the filamentous fungus Aspergillus nidulans, four core septins form heteropolymeric complexes. AspE, a fifth septin lacking in unicellular yeasts, interacts with only one of the core septins, and only during multicellular growth. AspE is required for proper localization of three of the core septins, and requires this same subset of core septins for its own unique cortical localization. The ΔaspE mutant lacks developmentally-specific septin higher-order structures and shows reduced spore production and slow growth with low temperatures and osmotic stress. Our results show that at least two distinct septin heteropolymer populations co-exist in A. nidulans, and that while AspE is not a subunit of either heteropolymer, it is required for assembly of septin higher-order structures found in multicellular development.
    Full-text · Article · Mar 2014 · PLoS ONE
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    • "In S. cerevisiae, four septins oligomerize to form an octameric septin complex (Bertin et al. 2008). In the absence of one septin, the remaining three septins can still form a less optimal hexameric complex that is sufficient for cytokinesis (McMurray et al. 2011). Many human septins have complex tissue-specific expression patterns, such that many tissues contain multiple septin genes from the same subgroup (Cao et al. 2007). "
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    ABSTRACT: Septins are cytoskeletal proteins that form hetero-oligomeric complexes and function in many biological processes, including cytokinesis. Drosophila melanogaster has five septin genes. Sep5, which is the most recently evolved septin gene in Drosophila, is a retrogene copy of Sep2. Sep5 mutants appear wild type, whereas Sep2 mutant females are semisterile. Their ovaries have egg chambers containing abnormal numbers of nurse cells. The egg chamber phenotype is rescued to wild type by expressing a Sep2 cDNA, but it is only partially rescued by expressing a Sep5 cDNA, showing that these paralogs have diverged in function at the protein level. Sep2 Sep5 double mutants have an early pupal lethal phenotype and lack imaginal discs, suggesting that these genes have redundant functions during imaginal cell proliferation.
    Full-text · Article · Dec 2013 · Genome
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