Septin clearance from the division site triggers cytokinesis in budding yeast

In many eukaryotic cells cytokinesis involves a contractile actomyosin ring (CAR) that drives cleavage furrow ingression. What triggers CAR constriction at a precise time of the cell cycle and how constriction is coupled to chromosome segregation are fundamental questions. In the budding yeast Sacch...

Full description

Saved in:
Bibliographic Details
Main Authors: Davide Tamborrini, Simonetta Piatti
Format: Article
Language:English
Published: Shared Science Publishers OG 2019-05-01
Series:Microbial Cell
Subjects:
Online Access:http://microbialcell.com/researcharticles/2019a-tamborrini-microbial-cell/
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850228352478085120
author Davide Tamborrini
Simonetta Piatti
author_facet Davide Tamborrini
Simonetta Piatti
author_sort Davide Tamborrini
collection DOAJ
description In many eukaryotic cells cytokinesis involves a contractile actomyosin ring (CAR) that drives cleavage furrow ingression. What triggers CAR constriction at a precise time of the cell cycle and how constriction is coupled to chromosome segregation are fundamental questions. In the budding yeast Saccharomyces cerevisiae, CAR assembly strictly requires a rigid septin collar that forms at the bud neck early during the cell cycle. At the time of cytokinesis, a sudden remodelling of the septin collar occurs, leading to its splitting into two separate rings that sandwich the CAR. We have shown that septin displacement during splitting is an essential prerequisite for CAR constriction [Tamborrini et al., Nat Commun. 9(1):4308]. Thus, cytokinesis in budding yeast is a two-step mechanism: during the first step, the septin collar organizes the assembly of the cytokinetic machinery at the right place while restraining CAR-driven membrane ingression; during the second step, a confined eviction of septins from the division site during septin ring splitting triggers CAR constriction. Our data further indicate that septin ring splitting is prompted by the Mitotic Exit Network (MEN), and in particular by its downstream phosphatase Cdc14, independently of its mitotic exit function. Surprisingly, MEN signalling at spindle pole bodies (SPBs) is critical for septin ring splitting and cytokinesis. Ubiquitination of the MEN anchor at SPBs by the Dma1/2 ubiquitin ligase attenuates MEN signalling and could have a decisive role in coupling cytokinesis to chromosome and organelle segregation. Altogether, our data emphasize the importance of septin ring splitting, which has been mysterious so far, and highlight a novel mechanism to prevent CAR constriction and cytokinesis in unpropitious conditions.
format Article
id doaj-art-eacea95dccc14c33b84d5d80cc662681
institution OA Journals
issn 2311-2638
language English
publishDate 2019-05-01
publisher Shared Science Publishers OG
record_format Article
series Microbial Cell
spelling doaj-art-eacea95dccc14c33b84d5d80cc6626812025-08-20T02:04:33ZengShared Science Publishers OGMicrobial Cell2311-26382019-05-016629529810.15698/mic2019.06.681Septin clearance from the division site triggers cytokinesis in budding yeastDavide Tamborrini0Simonetta Piatti1Centre de Recherche en Biologie Cellulaire de Montpellier 1919 Route de Mende, 34293 Montpellier, France.Centre de Recherche en Biologie Cellulaire de Montpellier 1919 Route de Mende, 34293 Montpellier, France.In many eukaryotic cells cytokinesis involves a contractile actomyosin ring (CAR) that drives cleavage furrow ingression. What triggers CAR constriction at a precise time of the cell cycle and how constriction is coupled to chromosome segregation are fundamental questions. In the budding yeast Saccharomyces cerevisiae, CAR assembly strictly requires a rigid septin collar that forms at the bud neck early during the cell cycle. At the time of cytokinesis, a sudden remodelling of the septin collar occurs, leading to its splitting into two separate rings that sandwich the CAR. We have shown that septin displacement during splitting is an essential prerequisite for CAR constriction [Tamborrini et al., Nat Commun. 9(1):4308]. Thus, cytokinesis in budding yeast is a two-step mechanism: during the first step, the septin collar organizes the assembly of the cytokinetic machinery at the right place while restraining CAR-driven membrane ingression; during the second step, a confined eviction of septins from the division site during septin ring splitting triggers CAR constriction. Our data further indicate that septin ring splitting is prompted by the Mitotic Exit Network (MEN), and in particular by its downstream phosphatase Cdc14, independently of its mitotic exit function. Surprisingly, MEN signalling at spindle pole bodies (SPBs) is critical for septin ring splitting and cytokinesis. Ubiquitination of the MEN anchor at SPBs by the Dma1/2 ubiquitin ligase attenuates MEN signalling and could have a decisive role in coupling cytokinesis to chromosome and organelle segregation. Altogether, our data emphasize the importance of septin ring splitting, which has been mysterious so far, and highlight a novel mechanism to prevent CAR constriction and cytokinesis in unpropitious conditions.http://microbialcell.com/researcharticles/2019a-tamborrini-microbial-cell/septinscytokinesisactomyosin ringMitotic Exit Network
spellingShingle Davide Tamborrini
Simonetta Piatti
Septin clearance from the division site triggers cytokinesis in budding yeast
Microbial Cell
septins
cytokinesis
actomyosin ring
Mitotic Exit Network
title Septin clearance from the division site triggers cytokinesis in budding yeast
title_full Septin clearance from the division site triggers cytokinesis in budding yeast
title_fullStr Septin clearance from the division site triggers cytokinesis in budding yeast
title_full_unstemmed Septin clearance from the division site triggers cytokinesis in budding yeast
title_short Septin clearance from the division site triggers cytokinesis in budding yeast
title_sort septin clearance from the division site triggers cytokinesis in budding yeast
topic septins
cytokinesis
actomyosin ring
Mitotic Exit Network
url http://microbialcell.com/researcharticles/2019a-tamborrini-microbial-cell/
work_keys_str_mv AT davidetamborrini septinclearancefromthedivisionsitetriggerscytokinesisinbuddingyeast
AT simonettapiatti septinclearancefromthedivisionsitetriggerscytokinesisinbuddingyeast