Literature DB >> 26831086

Defining the rate-limiting processes of bacterial cytokinesis.

Carla Coltharp1, Jackson Buss1, Trevor M Plumer1, Jie Xiao2.   

Abstract

Bacterial cytokinesis is accomplished by the essential 'divisome' machinery. The most widely conserved divisome component, FtsZ, is a tubulin homolog that polymerizes into the 'FtsZ-ring' ('Z-ring'). Previous in vitro studies suggest that Z-ring contraction serves as a major constrictive force generator to limit the progression of cytokinesis. Here, we applied quantitative superresolution imaging to examine whether and how Z-ring contraction limits the rate of septum closure during cytokinesis in Escherichia coli cells. Surprisingly, septum closure rate was robust to substantial changes in all Z-ring properties proposed to be coupled to force generation: FtsZ's GTPase activity, Z-ring density, and the timing of Z-ring assembly and disassembly. Instead, the rate was limited by the activity of an essential cell wall synthesis enzyme and further modulated by a physical divisome-chromosome coupling. These results challenge a Z-ring-centric view of bacterial cytokinesis and identify cell wall synthesis and chromosome segregation as limiting processes of cytokinesis.

Entities:  

Keywords:  FtsZ; cell wall synthesis; cytokinesis; force generation; superresolution

Mesh:

Substances:

Year:  2016        PMID: 26831086      PMCID: PMC4776500          DOI: 10.1073/pnas.1514296113

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  119 in total

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Authors:  D M Raskin; P A de Boer
Journal:  J Bacteriol       Date:  1999-10       Impact factor: 3.490

2.  Conformational changes of FtsZ reported by tryptophan mutants.

Authors:  Yaodong Chen; Harold P Erickson
Journal:  Biochemistry       Date:  2011-05-03       Impact factor: 3.162

3.  Modeling the physics of FtsZ assembly and force generation.

Authors:  Harold P Erickson
Journal:  Proc Natl Acad Sci U S A       Date:  2009-05-28       Impact factor: 11.205

4.  Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure.

Authors:  Gleb Shtengel; James A Galbraith; Catherine G Galbraith; Jennifer Lippincott-Schwartz; Jennifer M Gillette; Suliana Manley; Rachid Sougrat; Clare M Waterman; Pakorn Kanchanawong; Michael W Davidson; Richard D Fetter; Harald F Hess
Journal:  Proc Natl Acad Sci U S A       Date:  2009-02-06       Impact factor: 11.205

5.  Force generation by a dynamic Z-ring in Escherichia coli cell division.

Authors:  Jun F Allard; Eric N Cytrynbaum
Journal:  Proc Natl Acad Sci U S A       Date:  2008-12-29       Impact factor: 11.205

Review 6.  Bacterial cell division: assembly, maintenance and disassembly of the Z ring.

Authors:  David W Adams; Jeff Errington
Journal:  Nat Rev Microbiol       Date:  2009-09       Impact factor: 60.633

7.  FtsK is a bifunctional protein involved in cell division and chromosome localization in Escherichia coli.

Authors:  G Liu; G C Draper; W D Donachie
Journal:  Mol Microbiol       Date:  1998-08       Impact factor: 3.501

8.  The balance between different peptidoglycan precursors determines whether Escherichia coli cells will elongate or divide.

Authors:  K J Begg; A Takasuga; D H Edwards; S J Dewar; B G Spratt; H Adachi; T Ohta; H Matsuzawa; W D Donachie
Journal:  J Bacteriol       Date:  1990-12       Impact factor: 3.490

9.  Estimating Z-ring radius and contraction in dividing Escherichia coli.

Authors:  Johan Strömqvist; Karl Skoog; Daniel O Daley; Jerker Widengren; Gunnar von Heijne
Journal:  Mol Microbiol       Date:  2010-02-10       Impact factor: 3.501

10.  ZapE is a novel cell division protein interacting with FtsZ and modulating the Z-ring dynamics.

Authors:  Benoit S Marteyn; Gouzel Karimova; Andrew K Fenton; Anastasia D Gazi; Nicholas West; Lhousseine Touqui; Marie-Christine Prevost; Jean-Michel Betton; Oemer Poyraz; Daniel Ladant; Kenn Gerdes; Philippe J Sansonetti; Christoph M Tang
Journal:  mBio       Date:  2014-03-04       Impact factor: 7.867

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  72 in total

1.  Mechanistic Origin of Cell-Size Control and Homeostasis in Bacteria.

Authors:  Fangwei Si; Guillaume Le Treut; John T Sauls; Stephen Vadia; Petra Anne Levin; Suckjoon Jun
Journal:  Curr Biol       Date:  2019-05-16       Impact factor: 10.834

Review 2.  At the Heart of Bacterial Cytokinesis: The Z Ring.

Authors:  Shishen Du; Joe Lutkenhaus
Journal:  Trends Microbiol       Date:  2019-06-03       Impact factor: 17.079

3.  Short FtsZ filaments can drive asymmetric cell envelope constriction at the onset of bacterial cytokinesis.

Authors:  Qing Yao; Andrew I Jewett; Yi-Wei Chang; Catherine M Oikonomou; Morgan Beeby; Cristina V Iancu; Ariane Briegel; Debnath Ghosal; Grant J Jensen
Journal:  EMBO J       Date:  2017-04-24       Impact factor: 11.598

4.  Probing for Binding Regions of the FtsZ Protein Surface through Site-Directed Insertions: Discovery of Fully Functional FtsZ-Fluorescent Proteins.

Authors:  Desmond A Moore; Zakiya N Whatley; Chandra P Joshi; Masaki Osawa; Harold P Erickson
Journal:  J Bacteriol       Date:  2016-12-13       Impact factor: 3.490

5.  FtsZ Constriction Force - Curved Protofilaments Bending Membranes.

Authors:  Harold P Erickson; Masaki Osawa
Journal:  Subcell Biochem       Date:  2017

Review 6.  The bacterial divisome: more than a ring?

Authors:  Bill Söderström; Daniel O Daley
Journal:  Curr Genet       Date:  2016-07-08       Impact factor: 3.886

7.  ZipA and FtsA* stabilize FtsZ-GDP miniring structures.

Authors:  Yaodong Chen; Haiyan Huang; Masaki Osawa; Harold P Erickson
Journal:  Sci Rep       Date:  2017-06-16       Impact factor: 4.379

Review 8.  Bacterial cell division at a glance.

Authors:  Christopher R Mahone; Erin D Goley
Journal:  J Cell Sci       Date:  2020-04-08       Impact factor: 5.285

9.  An essential Staphylococcus aureus cell division protein directly regulates FtsZ dynamics.

Authors:  Prahathees J Eswara; Robert S Brzozowski; Marissa G Viola; Gianni Graham; Catherine Spanoudis; Catherine Trebino; Jyoti Jha; Joseph I Aubee; Karl M Thompson; Jodi L Camberg; Kumaran S Ramamurthi
Journal:  Elife       Date:  2018-10-02       Impact factor: 8.140

Review 10.  Redefining the roles of the FtsZ-ring in bacterial cytokinesis.

Authors:  Jie Xiao; Erin D Goley
Journal:  Curr Opin Microbiol       Date:  2016-09-10       Impact factor: 7.934

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