Subunit-dependent modulation of septin assembly: Budding yeast septin Shs1 promotes ring and gauze formation

Garcia, Galo; Bertin, Aurelie; Li, Zhu; Song, Yi; McMurray, Michael A.; Thorner, Jeremy; Nogales, Eva

doi:10.1083/jcb.201107123

Title: Subunit-dependent modulation of septin assembly: Budding yeast septin Shs1 promotes ring and gauze formation

Journal Article · Mon Dec 05 00:00:00 EST 2011 · Journal of Cell Biology

DOI:https://doi.org/10.1083/jcb.201107123· OSTI ID:1625162

Garcia, Galo ^[1]; Bertin, Aurelie ^[1]; Li, Zhu ^[1]; Song, Yi ^[1]; McMurray, Michael A. ^[1]; Thorner, Jeremy ^[1]; Nogales, Eva ^[2]

Univ. of California, Berkeley, CA (United States).Dept. of Molecular and Cell Biology. Division of Biochemistry and Molecular Biology
Univ. of California, Berkeley, CA (United States).Dept. of Molecular and Cell Biology. Division of Biochemistry and Molecular Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Science Division; Howard Hughes Medical Inst., Chevy Chase, MD (United States)

Septins are conserved guanosine triphosphate–binding cytoskeletal proteins involved in membrane remodeling. In budding yeast, five mitotic septins (Cdc3, Cdc10, Cdc11, Cdc12, and Shs1), which are essential for cytokinesis, transition during bud growth from a patch to a collar, which splits into two rings in cytokinesis and is disassembled before the next cell cycle. Cdc3, Cdc10, Cdc11, and Cdc12 form an apolar octameric rod with Cdc11 at each tip, which polymerizes into straight paired filaments. We show that Shs1 substitutes for Cdc11, resulting in octameric rods that do not polymerize into filaments but associate laterally, forming curved bundles that close into rings. In vivo, half of shs1Δ mutant cells exhibit incomplete collars and disrupted neck filaments. Importantly, different phosphomimetic mutations in Shs1 can either prevent ring formation or promote formation of a gauzelike meshwork. These results show that a single alternative terminal subunit is sufficient to confer a distinctive higher-order septin ultrastructure that can be further regulated by phosphorylation.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH)

Grant/Contract Number:: AC02-05CH11231; GM86603; GM21841

OSTI ID:: 1625162

Journal Information:: Journal of Cell Biology, Vol. 195, Issue 6; ISSN 0021-9525

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Cytoskeleton: Cirque du Septins Gladfelter, Amy S. Current Biology, Vol. 24, Issue 11 https://doi.org/10.1016/j.cub.2014.04.030	journal	June 2014
Daughter Cell Identity Emerges from the Interplay of Cdc42, Septins, and Exocytosis Okada, Satoshi; Leda, Marcin; Hanna, Julia Developmental Cell, Vol. 26, Issue 2 https://doi.org/10.1016/j.devcel.2013.06.015	journal	July 2013
Architecture and dynamic remodelling of the septin cytoskeleton during the cell cycle Ong, Katy; Wloka, Carsten; Okada, Satoshi Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6698	journal	December 2014
Synergistic role of nucleotides and lipids for the self-assembly of Shs1 septin oligomers Taveneau, Cyntia; Blanc, Rémi; Péhau-Arnaudet, Gérard Biochemical Journal, Vol. 477, Issue 14 https://doi.org/10.1042/bcj20200199	journal	July 2020
Distinct segregation patterns of yeast cell-peripheral proteins uncovered by a method for protein segregatome analysis Sugiyama, Shinju; Tanaka, Motomasa Proceedings of the National Academy of Sciences, Vol. 116, Issue 18 https://doi.org/10.1073/pnas.1819715116	journal	April 2019
SUMOylation of human septins is critical for septin filament bundling and cytokinesis Ribet, David; Boscaini, Serena; Cauvin, Clothilde Journal of Cell Biology, Vol. 216, Issue 12 https://doi.org/10.1083/jcb.201703096	journal	October 2017
Septin ring size scaling and dynamics require the coiled-coil region of Shs1p Meseroll, Rebecca A.; Howard, Louisa; Gladfelter, Amy S. Molecular Biology of the Cell, Vol. 23, Issue 17 https://doi.org/10.1091/mbc.e12-03-0207	journal	September 2012
Regulation of the formin Bnr1 by septins anda MARK/Par1-family septin-associated kinase Buttery, Shawnna M.; Kono, Keiko; Stokasimov, Ema Molecular Biology of the Cell, Vol. 23, Issue 20 https://doi.org/10.1091/mbc.e12-05-0395	journal	October 2012
Aim44p regulates phosphorylation of Hof1p to promote contractile ring closure during cytokinesis in budding yeast Wolken, Dana M. Alessi; McInnes, Joseph; Pon, Liza A. Molecular Biology of the Cell, Vol. 25, Issue 6 https://doi.org/10.1091/mbc.e13-06-0317	journal	March 2014
Cell type–specific expression of SEPT3-homology subgroup members controls the subunit number of heteromeric septin complexes Sellin, Mikael E.; Stenmark, Sonja; Gullberg, Martin Molecular Biology of the Cell, Vol. 25, Issue 10 https://doi.org/10.1091/mbc.e13-09-0553	journal	May 2014
Detection of protein–protein interactions at the septin collar inSaccharomyces cerevisiaeusing a tripartite split-GFP system Finnigan, Gregory C.; Duvalyan, Angela; Liao, Elizabeth N. Molecular Biology of the Cell, Vol. 27, Issue 17 https://doi.org/10.1091/mbc.e16-05-0337	journal	September 2016
Interplay of septin amphipathic helices in sensing membrane-curvature and filament bundling Woods, Benjamin L.; Cannon, Kevin S.; Gladfelter, Amy S. Molecular Biology of the Cell https://doi.org/10.1101/2020.05.12.090787	journal	May 2020
Choanoflagellate transfection illuminates their cell biology and the ancestry of animal septins Booth, David S.; Szmidt-Middleton, Heather; , Nicole King Molecular Biology of the Cell https://doi.org/10.1101/343111	journal	August 2018
The Long and Viscous Road: Uncovering Nuclear Diffusion Barriers in Closed Mitosis Zavala, Eder; Marquez-Lago, Tatiana T. PLoS Computational Biology, Vol. 10, Issue 7 https://doi.org/10.1371/journal.pcbi.1003725	journal	July 2014
A Single Nucleotide Polymorphism Uncovers a Novel Function for the Transcription Factor Ace2 during Candida albicans Hyphal Development Calderón-Noreña, Diana M.; González-Novo, Alberto; Orellana-Muñoz, Sara PLOS Genetics, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pgen.1005152	journal	April 2015
Distinct Septin Heteropolymers Co-Exist during Multicellular Development in the Filamentous Fungus Aspergillus nidulans Hernández-Rodríguez, Yainitza; Masuo, Shunsuke; Johnson, Darryl PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0092819	journal	March 2014
Phosphorylation of Pnut in the Early Stages ofDrosophilaEmbryo Development Affects Association of the Septin Complex with the Membrane and Is Important for Viability Akhmetova, Katarina; Balasov, Maxim; Svitin, Anton G3 Genes\|Genomes\|Genetics, Vol. 8, Issue 1 https://doi.org/10.1534/g3.117.300186	journal	January 2018
Higher-Order Septin Assembly Is Driven by GTP-Promoted Conformational Changes: Evidence From Unbiased Mutational Analysis in Saccharomyces cerevisiae Weems, Andrew D.; Johnson, Courtney R.; Argueso, Juan Lucas Genetics, Vol. 196, Issue 3 https://doi.org/10.1534/genetics.114.161182	journal	January 2014
Septin-Associated Protein Kinases in the Yeast Saccharomyces cerevisiae Perez, Adam M.; Finnigan, Gregory C.; Roelants, Françoise M. Frontiers in Cell and Developmental Biology, Vol. 4 https://doi.org/10.3389/fcell.2016.00119	journal	November 2016
Septin Organization and Functions in Budding Yeast Glomb, Oliver; Gronemeyer, Thomas Frontiers in Cell and Developmental Biology, Vol. 4 https://doi.org/10.3389/fcell.2016.00123	journal	November 2016
Protein Kinase A-Mediated Septin7 Phosphorylation Disrupts Septin Filaments and Ciliogenesis Wang, Han-Yu; Lin, Chun-Hsiang; Shen, Yi-Ru Cells, Vol. 10, Issue 2 https://doi.org/10.3390/cells10020361	journal	February 2021
Mammalian SEPT9 isoforms direct microtubule-dependent arrangements of septin core heteromers E., Sellin, Mikael; Sonja, Stenmark,; Martin, Gullberg, ETH Zurich https://doi.org/10.3929/ethz-b-000064111	text	January 2012
The step-wise pathway of septin hetero-octamer assembly in budding yeast Weems, Andrew; McMurray, Michael eLife, Vol. 6 https://doi.org/10.7554/elife.23689	journal	May 2017

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