Dual Role of DNA in Regulating ATP Hydrolysis by the SopA Partition Protein

Ah-Seng, Yoan; Lopez, Fréderic; Pasta, Franck; Lane, David; Bouet, Jean‐Yves

doi:10.1074/jbc.m109.044800

Cited by 78 publications

(109 citation statements)

References 38 publications

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“…Most recently, triple labeling of plasmids, ParA (from plasmid pB171), and the nucleoid in E. coli confirmed and extended the notion that plasmids move toward retracting ParA signals (143). Together, these data suggest a model in which ParA ATPase stimulation by ParB (4,12,96,140) depolymerizes ParA filaments at the ParB contact site and leads to concomitant pulling of attached plasmids (58,143). The assembly of ParA on a DNA substrate in vivo, rather than forming independent structures, makes the status of ParA as a bona fide cytoskeletal element a subject of controversy in the field.…”

Section: Deviant Walker A-motif Atpasesmentioning

confidence: 72%

The Bacterial Cytoskeleton

2010

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Bacteria, like eukaryotes, employ cytoskeletal elements to perform many functions, including cell morphogenesis, cell division, DNA partitioning, and cell motility. They not only possess counterparts of eukaryotic actin, tubulin, and intermediate filament proteins, but they also have cytoskeletal elements of their own. Unlike the rigid sequence and structural conservation often observed for eukaryotic cytoskeletal proteins, the bacterial counterparts can display considerable diversity in sequence and function across species. Their wide range of function highlights the flexibility of core cytoskeletal protein motifs, such that one type of cytoskeletal element can perform various functions, and one function can be performed by different types of cytoskeletal elements.

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Section: Deviant Walker A-motif Atpasesmentioning

confidence: 72%

The Bacterial Cytoskeleton

2010

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“…The ATPturnover rate of SopA in the presence of saturating DNA (0.01/min; ref. 21) is ∼200-fold slower than the rate of SopA release from DNA. Thus, DNA release is not obligatorily coupled to ATP hydrolysis.…”

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confidence: 99%

Cell-free study of F plasmid partition provides evidence for cargo transport by a diffusion-ratchet mechanism

Vecchiarelli

Hwang

Mizuuchi

2013

Proc. Natl. Acad. Sci. U.S.A.

138

185

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Increasingly diverse types of cargo are being found to be segregated and positioned by ParA-type ATPases. Several minimalistic systems described in bacteria are self-organizing and are known to affect the transport of plasmids, protein machineries, and chromosomal loci. One well-studied model is the F plasmid partition system, SopABC. In vivo, SopA ATPase forms dynamic patterns on the nucleoid in the presence of the ATPase stimulator, SopB, which binds to the sopC site on the plasmid, demarcating it as the cargo. To understand the relationship between nucleoid patterning and plasmid transport, we established a cell-free system to study plasmid partition reactions in a DNA-carpeted flowcell. We observed depletion zones of the partition ATPase on the DNA carpet surrounding partition complexes. The findings favor a diffusion-ratchet model for plasmid motion whereby partition complexes create an ATPase concentration gradient and then climb up this gradient toward higher concentrations of the ATPase. Here, we report on the dynamic properties of the Sop system on a DNA-carpet substrate, which further support the proposed diffusion-ratchet mechanism.bacterial chromosome segregation | ParA ATPase | plasmid segregation | spatial pattern organization | chromosome dynamics P roper DNA segregation ensures the faithful inheritance of genomic information for all life forms. In bacteria, this fundamental process is poorly understood. Low-copy bacterial genomes, including plasmids and chromosomes, encode active partition (Par) systems to ensure stability. Par systems are minimalistic in that only three dedicated components are required: a partition site on the DNA, a partition site-binding protein, and a nucleoside triphosphatase (NTPase). Par systems have been classified according to the type of NTPase involved: Walker-type (generically called "ParA"), actin-like, or tubulin-like (reviewed in ref. 1). Reconstitution of purified Par components of R1 plasmid in a cell-free system unveiled the mechanism involving an actin-like ATPase, ParM, in which elongating filaments of the ATPase push plasmids to opposite cell poles (2). Tubulin-like GTPases also appear to function as a filament (3). However, all chromosome-based and most plasmid-based systems use ParAs, and mounting evidence shows that ParA-like ATPases also are responsible for transporting large protein machineries (reviewed in ref. 4). However, the underlying mechanism for reactions of this category remains unresolved.The Sop system (stability of plasmid) of F plasmid is one of the first Par systems to be identified (5, 6) and is considered a paradigm for the study of ParA-mediated DNA segregation. The three plasmid-encoded system components are SopA (the ParAtype ATPase), SopB (or ParB in other systems; i.e., the partition site-binding protein), and sopC (or parS in other systems; i.e., the cis-acting partition site on the plasmid). The first task of a partition system is to identify its DNA cargo. SopB accomplishes this task by loading onto sopC and forming a partition c...

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“…The stability of plasmid (SOP) system of F plasmid is a canonical ParA-mediated cargo transport system. The ParA ATPase of F plasmid, SopA, is stimulated by SopB that assembles into a partition complex on the centromere-like locus, sopC, on the plasmid cargo (3,4). SopA binds DNA nonspecifically in the presence of ATP and colocalizes with the nucleoid in vivo (5,6).…”

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confidence: 99%

A propagating ATPase gradient drives transport of surface-confined cellular cargo

Vecchiarelli

Neuman

Mizuuchi

2014

Proc. Natl. Acad. Sci. U.S.A.

174

227

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Significance The process of DNA segregation is of central importance for all organisms. Although the basic mechanism of eukaryotic mitosis is relatively well established, the most common mechanism used for bacterial DNA segregation has been unclear. ParA ATPases form dynamic patterns on the bacterial nucleoid to spatially organize plasmids, chromosomes and other large cellular cargo, but the force-generating mechanism has been a source of controversy and debate. A dominant view proposes that ParA-mediated transport and cargo positioning occurs via a filament-based mechanism that resembles eukaryotic mitosis. Here, we present direct evidence against such models. Our cell-free reconstitution supports a non–filament-based mode of transport that may be as widely found in nature as filament-based mechanisms.

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Dual Role of DNA in Regulating ATP Hydrolysis by the SopA Partition Protein

Cited by 78 publications

References 38 publications

The Bacterial Cytoskeleton

The Bacterial Cytoskeleton

Cell-free study of F plasmid partition provides evidence for cargo transport by a diffusion-ratchet mechanism

A propagating ATPase gradient drives transport of surface-confined cellular cargo

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