Literature DB >> 24859756

Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation.

Hoong Chuin Lim1, Ivan Vladimirovich Surovtsev2, Bruno Gabriel Beltran3, Fang Huang4, Jörg Bewersdorf5, Christine Jacobs-Wagner6.   

Abstract

The widely conserved ParABS system plays a major role in bacterial chromosome segregation. How the components of this system work together to generate translocation force and directional motion remains uncertain. Here, we combine biochemical approaches, quantitative imaging and mathematical modeling to examine the mechanism by which ParA drives the translocation of the ParB/parS partition complex in Caulobacter crescentus. Our experiments, together with simulations grounded on experimentally-determined biochemical and cellular parameters, suggest a novel 'DNA-relay' mechanism in which the chromosome plays a mechanical function. In this model, DNA-bound ParA-ATP dimers serve as transient tethers that harness the elastic dynamics of the chromosome to relay the partition complex from one DNA region to another across a ParA-ATP dimer gradient. Since ParA-like proteins are implicated in the partitioning of various cytoplasmic cargos, the conservation of their DNA-binding activity suggests that the DNA-relay mechanism may be a general form of intracellular transport in bacteria.DOI: http://dx.doi.org/10.7554/eLife.02758.001.
Copyright © 2014, Lim et al.

Entities:  

Keywords:  Caulobacter crescentus; DNA partitioning; Par system; chromosome dynamics; intracellular transport

Mesh:

Substances:

Year:  2014        PMID: 24859756      PMCID: PMC4067530          DOI: 10.7554/eLife.02758

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  101 in total

1.  Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication.

Authors:  Patrick H Viollier; Martin Thanbichler; Patrick T McGrath; Lisandra West; Maliwan Meewan; Harley H McAdams; Lucy Shapiro
Journal:  Proc Natl Acad Sci U S A       Date:  2004-06-03       Impact factor: 11.205

2.  Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA.

Authors:  Heath Murray; Jeff Errington
Journal:  Cell       Date:  2008-10-03       Impact factor: 41.582

3.  Sample drift correction in 3D fluorescence photoactivation localization microscopy.

Authors:  Michael J Mlodzianoski; John M Schreiner; Steven P Callahan; Katarina Smolková; Andrea Dlasková; Jitka Santorová; Petr Ježek; Joerg Bewersdorf
Journal:  Opt Express       Date:  2011-08-01       Impact factor: 3.894

4.  Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells.

Authors:  M Evinger; N Agabian
Journal:  J Bacteriol       Date:  1977-10       Impact factor: 3.490

5.  spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis.

Authors:  K Ireton; N W Gunther; A D Grossman
Journal:  J Bacteriol       Date:  1994-09       Impact factor: 3.490

6.  Cell cycle-dependent polar localization of chromosome partitioning proteins in Caulobacter crescentus.

Authors:  D A Mohl; J W Gober
Journal:  Cell       Date:  1997-03-07       Impact factor: 41.582

7.  F plasmid partition depends on interaction of SopA with non-specific DNA.

Authors:  Jean-Philippe Castaing; Jean-Yves Bouet; David Lane
Journal:  Mol Microbiol       Date:  2008-09-30       Impact factor: 3.501

8.  ATP control of dynamic P1 ParA-DNA interactions: a key role for the nucleoid in plasmid partition.

Authors:  Anthony G Vecchiarelli; Yong-Woon Han; Xin Tan; Michiyo Mizuuchi; Rodolfo Ghirlando; Christian Biertümpfel; Barbara E Funnell; Kiyoshi Mizuuchi
Journal:  Mol Microbiol       Date:  2010-07-27       Impact factor: 3.501

9.  Simultaneous multiple-emitter fitting for single molecule super-resolution imaging.

Authors:  Fang Huang; Samantha L Schwartz; Jason M Byars; Keith A Lidke
Journal:  Biomed Opt Express       Date:  2011-04-29       Impact factor: 3.732

10.  Mapping the driving forces of chromosome structure and segregation in Escherichia coli.

Authors:  Nathan J Kuwada; Keith C Cheveralls; Beth Traxler; Paul A Wiggins
Journal:  Nucleic Acids Res       Date:  2013-06-17       Impact factor: 16.971

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  88 in total

1.  Directed and persistent movement arises from mechanochemistry of the ParA/ParB system.

Authors:  Longhua Hu; Anthony G Vecchiarelli; Kiyoshi Mizuuchi; Keir C Neuman; Jian Liu
Journal:  Proc Natl Acad Sci U S A       Date:  2015-12-08       Impact factor: 11.205

2.  Can a Flux-Based Mechanism Explain Protein Cluster Positioning in a Three-Dimensional Cell Geometry?

Authors:  Matthias Kober; Silke Bergeler; Erwin Frey
Journal:  Biophys J       Date:  2019-07-04       Impact factor: 4.033

3.  XerD unloads bacterial SMC complexes at the replication terminus.

Authors:  Xheni Karaboja; Zhongqing Ren; Hugo B Brandão; Payel Paul; David Z Rudner; Xindan Wang
Journal:  Mol Cell       Date:  2021-01-19       Impact factor: 17.970

4.  DNA-relay mechanism is sufficient to explain ParA-dependent intracellular transport and patterning of single and multiple cargos.

Authors:  Ivan V Surovtsev; Manuel Campos; Christine Jacobs-Wagner
Journal:  Proc Natl Acad Sci U S A       Date:  2016-10-31       Impact factor: 11.205

5.  Physical modeling of chromosome segregation in escherichia coli reveals impact of force and DNA relaxation.

Authors:  Thomas J Lampo; Nathan J Kuwada; Paul A Wiggins; Andrew J Spakowitz
Journal:  Biophys J       Date:  2015-01-06       Impact factor: 4.033

Review 6.  Cytoskeletal Proteins in Caulobacter crescentus: Spatial Orchestrators of Cell Cycle Progression, Development, and Cell Shape.

Authors:  Kousik Sundararajan; Erin D Goley
Journal:  Subcell Biochem       Date:  2017

7.  Nucleoid Size Scaling and Intracellular Organization of Translation across Bacteria.

Authors:  William T Gray; Sander K Govers; Yingjie Xiang; Bradley R Parry; Manuel Campos; Sangjin Kim; Christine Jacobs-Wagner
Journal:  Cell       Date:  2019-05-30       Impact factor: 41.582

8.  Molecular Anatomy of ParA-ParA and ParA-ParB Interactions during Plasmid Partitioning.

Authors:  Andrea Volante; Juan C Alonso
Journal:  J Biol Chem       Date:  2015-06-08       Impact factor: 5.157

9.  Segregation of four Agrobacterium tumefaciens replicons during polar growth: PopZ and PodJ control segregation of essential replicons.

Authors:  J S Robalino-Espinosa; J R Zupan; A Chavez-Arroyo; P Zambryski
Journal:  Proc Natl Acad Sci U S A       Date:  2020-10-06       Impact factor: 11.205

Review 10.  Engineering spatiotemporal organization and dynamics in synthetic cells.

Authors:  Alessandro Groaz; Hossein Moghimianavval; Franco Tavella; Tobias W Giessen; Anthony G Vecchiarelli; Qiong Yang; Allen P Liu
Journal:  Wiley Interdiscip Rev Nanomed Nanobiotechnol       Date:  2020-11-21
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