Cell‐specific SpoIIIE assembly and DNA translocation polarity are dictated by chromosome orientation

Becker, Eric; Pogliano, Kit

doi:10.1111/j.1365-2958.2007.05992.x

Cited by 50 publications

(69 citation statements)

References 45 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Structural and fluorescence microscopy evidence suggests that during sporulation each chromosome arm is translocated through an independent SpoIIIE channel 17,23,36 . Our compartment-specific SpoIIIE-tagging experiments showed that during sporulation SpoIIIE is exclusively assembled on the mother-cell side of the septum, whereas SpoIIIE-Δγ is assembled on both sides with equal frequency.…”

Section: Discussionmentioning

confidence: 99%

“…The long pause durations required for reversing translocation direction by SpoIIIE-Δγ in our in vivo DNA translocation assay (~20 min) further suggest that the mechanism giving rise to translocation reversals is slow and may involve the reassembly of the forespore complex. Recent studies determined that the ability of SpoIIIE to hydrolyze ATP is required for the disassembly of the forespore SpoIIIE complex and that the orientation of the chromosome after septation determines the direction of DNA translocation 23 . Taken together, these results suggest that translocation by the forespore exporter leads to specific interactions between SpoIIIE-γ and nonpermissive SRS that lead to the inactivation and subsequent dissociation of the forespore complex (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Here we used a cell-specific GFP-tagging method to visualize SpoIIIE complexes assembled at the mother-cell or forespore side of the sporulation septum 23 . In this method, the leucine zipper domains of Jun and Fos (Jun LZ and Fos LZ ) 35 are used as specific tags to link SpoIIIE and GFP.…”

Section: Spoiiie-γ Regulates the Compartmental Localization Of Spoiiiementioning

confidence: 99%

“…To understand this sporulation defect triggered by the lack of SpoIIIE-γ, we used a time-lapse fluorescence microscopy technique 23 to characterize quantitatively the dynamics of chromosome translocation in vivo by SpoIIIE. Synchronized sporulating cultures were grown on agar pads and imaged at regular intervals by fluorescence microscopy.…”

Section: Spoiiie-γ Is Required For Directional Dna Translocation In Vivomentioning

confidence: 99%

“…The fact that SpoIIIE is expressed throughout vegetative growth implied the existence of another unidentified factor that regulates translocation polarity in the absence of cellular asymmetry 21,22 . Recent work showed that, in a racA soj-spo0J mutant background, the misorientation of the chromosome relative to the septum caused SpoIIIE to translocate the chromosome out of the forespore 23 . This result suggests that SpoIIIE directional DNA transfer may also be regulated by the polarity of the chromosome itself.…”

mentioning

confidence: 99%

See 4 more Smart Citations

Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis

Ptacin

Nollmann

Becker

et al. 2008

Nat Struct Mol Biol

Self Cite

165

View full text Add to dashboard Cite

In prokaryotes, the transfer of DNA between cellular compartments is essential for the segregation and exchange of genetic material. SpoIIIE and FtsK are AAA+ ATPases responsible for intercompartmental chromosome translocation in bacteria. Despite functional and sequence similarities, these motors were proposed to use drastically different mechanisms: SpoIIIE was suggested to be a unidirectional DNA transporter that exports DNA from the compartment in which it assembles, whereas FtsK was shown to establish translocation directionality by interacting with highly skewed chromosomal sequences. Here we use a combination of single-molecule, bioinformatics and in vivo fluorescence methodologies to study the properties of DNA translocation by SpoIIIE in vitro and in vivo. These data allow us to propose a sequence-directed DNA exporter model that reconciles previously proposed models for SpoIIIE and FtsK, constituting a unified model for directional DNA transport by the SpoIIIE/FtsK family of AAA+ ring ATPases.The segregation and exchange of genetic material are central to the processes of cell division and evolution. Although mechanisms of genetic transfer between cellular compartments are diverse, all require the movement of DNA across cellular membranes. A dramatic example of intercellular transmembrane DNA transport is the segregation of chromosomes during sporulation in Bacillus subtilis. During this process, newly replicated chromosomes are rearranged into an elongated structure, or axial filament, in which the origin of replication of each chromosome is tethered to opposite cell poles 1,2 . Next, the division plane is relocated to one pole, creating two asymmetric cellular compartments (the forespore and the mother cell) and trapping the origin-proximal 30% of one chromosome within the forespore 3,4 . The septally

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Spoiiie-γ Regulates the Compartmental Localization Of Spoiiiementioning

confidence: 99%

Section: Spoiiie-γ Is Required For Directional Dna Translocation In Vivomentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis

Ptacin

Nollmann

Becker

et al. 2008

Nat Struct Mol Biol

Self Cite

165

View full text Add to dashboard Cite

show abstract

The FtsK Family of DNA Pumps

Demarre

Galli

Barre

2012

Advances in Experimental Medicine and Biology

View full text Add to dashboard Cite

Interest for proteins of the FtsK family initially arose from their implication in many primordial processes in which DNA needs to be transported from one cell compartment to another in eubacteria. In the first section of this chapter, we address a list of the cellular functions of the different members of the FtsK family that have been so far studied. Soon after their discovery, interest for the FstK proteins spread because of their unique biochemical properties: most DNA transport systems rely on the assembly of complex multicomponent machines. In contrast, six FtsK proteins are sufficient to assemble into a fast and powerful DNA pump; the pump transports closed circular double stranded DNA molecules without any covalent-bond breakage nor topological alteration; transport is oriented despite the intrinsic symmetrical nature of the double stranded DNA helix and can occur across cell membranes. The different activities required for the oriented transport of DNA across cell compartments are achieved by three separate modules within the FtsK proteins: a DNA translocation module, an orientation module and an anchoring module. In the second part of this chapter, we review the structural and biochemical properties of these different modules.

show abstract

High Pressure Bioscience

Akasaka¹,

Matsuki²

2015

Subcellular Biochemistry

View full text Add to dashboard Cite

The book series SUBCELLULAR BIOCHEMISTRY is a renowned and well recognized forum for disseminating advances of emerging topics in Cell Biology and related subjects. All volumes are edited by established scientists and the individual chapters are written by experts on the relevant topic. The individual chapters of each volume are fully citable and indexed in Medline/Pubmed to ensure maximum visibility of the work.

show abstract

Cell‐specific SpoIIIE assembly and DNA translocation polarity are dictated by chromosome orientation

Cited by 50 publications

References 45 publications

Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis

Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis

The FtsK Family of DNA Pumps

High Pressure Bioscience

Contact Info

Product

Resources

About