Dynamic instability — A common denominator in prokaryotic and eukaryotic DNA segregation and cell division

Fuesler, John; Li, Sophia Hsin-Jung

doi:10.2478/s11658-012-0026-3

Cited by 9 publications

(8 citation statements)

References 18 publications

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“…In eukaryotic cells, several proteins, including the actin-binding proteins cofilin and profilin, collaborate to maintain a high concentration of monomeric actin, orders of magnitude higher than the critical concentration for polymerization. In bacteria, the dynamic instability of unattached ParM filaments maintains the concentration of monomeric ParM approximately fourfold above the critical concentration of filaments attached to segrosomes (9,14). If assembly of AlfA filaments drives plasmid movement, then how, in the absence of dynamic instability, is the concentration of monomeric AlfA maintained at a level sufficient to drive the growth of segrosome-attached filaments?…”

mentioning

confidence: 99%

Accessory factors promote AlfA-dependent plasmid segregation by regulating filament nucleation, disassembly, and bundling

Polka

Kollman

Mullins

2014

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

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In bacteria, some plasmids are partitioned to daughter cells by assembly of actin-like proteins (ALPs). The best understood ALP, ParM, has a core set of biochemical properties that contributes to its function, including dynamic instability, spontaneous nucleation, and bidirectional elongation. AlfA, an ALP that pushes plasmids apart in Bacillus, relies on a different set of underlying properties to segregate DNA. AlfA elongates unidirectionally and is not dynamically unstable; its assembly and disassembly are regulated by a cofactor, AlfB. Free AlfB breaks up AlfA bundles and promotes filament turnover. However, when AlfB is bound to the centromeric DNA sequence, parN, it forms a segrosome complex that nucleates and stabilizes AlfA filaments. When reconstituted in vitro, this system creates polarized, motile comet tails that associate by antiparallel filament bundling to form bipolar, DNAsegregating spindles.DNA segregation | bacterial cytoskeleton | Bacillus subtilis | reconstitution T he first filament-forming actin-like protein (ALP) was identified in bacteria in 2001 (1), and subsequent work identified more than 30 additional classes of ALPs in eubacteria and archaea (2). These proteins are involved in a variety of cellular processes, including assembly of the cell wall (1, 3-5), positioning of organelles (6), anchoring of cytokinesis machinery (7), and segregation of DNA (8). Most DNA-segregating ALPs participate in type II plasmid partitioning systems, which consist of three components: (i) a centromeric DNA sequence; (ii) a DNAbinding protein that interacts with the centromeric sequence to form a segrosome complex; and (iii) a polymer-forming ALP, whose self-assembly moves the segrosome through the cytoplasm (SI Appendix, Fig. S1). In the best understood type II segregation system, bidirectional polymerization of the ALP, ParM, pushes pairs of plasmids to opposite poles of rod-shaped cells. Extensive studies, both in vivo and in vitro, have produced detailed models of ParM-mediated DNA segregation (9, 10), but it is unclear to what extent these models can be generalized to describe other ALP-dependent DNA segregation systems.To better understand the diversity of molecular mechanisms underlying plasmid segregation, we studied a type II plasmid partitioning system encoded by the alf operon from the Bacillus subtilis plasmid pLS32 (11). The alf operon was first identified based on its ability to maintain plasmids through the process of sporulation, presumably by actively pushing a plasmid into the forespore at one end of the cell. In addition, the alf operon confers approximately eightfold greater stability to plasmids in rapidly dividing cells. The alf operon itself contains a centromeric sequence, parN, with three short, repeated sequences, and it encodes both an ALP, AlfA, and a DNA-binding protein, AlfB. The AlfA protein shares 15% sequence identity with ParM (2), whereas AlfB shares only 8% identity with ParR and has no significant BLAST hits (expect value < 1). In addition to sequence differences, AlfA...

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mentioning

confidence: 99%

Accessory factors promote AlfA-dependent plasmid segregation by regulating filament nucleation, disassembly, and bundling

Polka

Kollman

Mullins

2014

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

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“…Biological membranes and cytoskeleton are examples of such aggregates whose stability depends on the aqueous solubility of all their components [4,[24][25][26][27]. Cellular matrix of fibrous structures is continuously rearranged by workings of molecular machines and a combination of polymerization and dissociation processes [28][29][30]. The delicate hydrophilic/hydrophobic balance of this extensive supramolecular threedimensional structure depends on both its molecular composition and properties of the aqueous phase (pH, ionic strength and ionic composition) [31,32].…”

Section: Transformation Of Structurementioning

confidence: 99%

“…An ensemble of macromolecules should be able, given proper environmental conditions, to spontaneously acquire the functional organization. Macromolecular ensembles in biological systems are in a state of dynamic instability [16,27,30,31]. In order to preserve the spatial arrangement and density of macromolecules, the available volume needs to be restricted by an impermeable barrier -the biological membrane, which defines the cell volume [11,75,83,84].…”

Section: The Functioning Of a Molecular Machinementioning

confidence: 99%

Molecular machines – a new dimension of biological sciences

Głogocka

Przybyło

Langner

2015

Cellular and Molecular Biology Letters

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Biological systems are characterized by directional and precisely controlled flow of matter and information along with the maintenance of their structural patterns. This is possible thanks to sequential transformations of information, energy and structure carried out by molecular machines. The new perception of biological systems, including their mechanical aspects, requires the implementation of tools and approaches previously developed for engineering sciences. In this review paper, a biological system is presented in a new perspective as an ensemble of coordinated molecular devices functioning in the limited space confined by the biological membrane. The working of a molecular machine is presented using the example of F0F1 ATPase, and the general conditions necessary for the coordination of a large number of functional units are described.

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“…The cytoskeleton is a key regulator and central organizer of many eukaryotic cellular processes including cell shape determination (morphogenesis), cell polarity, DNA segregation, cell division, phagocytosis, movement, and macromolecular trafficking [Fuesler and Li, 2012]. Most cytoskeletal elements known from eukaryotic cell studies appear to be present in bacteria, where they perform vital tasks relevant to many aspects of cell physiology (Table 1).…”

Section: The Bacterial Cytoskeletonmentioning

confidence: 99%

Microcompartments and Protein Machines in Prokaryotes

Saier

2013

Microb Physiol

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The prokaryotic cell was once thought of as a ‘bag of enzymes' with little or no intracellular compartmentalization. In this view, most reactions essential for life occurred as a consequence of random molecular collisions involving substrates, cofactors and cytoplasmic enzymes. Our current conception of a prokaryote is far from this view. We now consider a bacterium or an archaeon as a highly structured, nonrandom collection of functional membrane-embedded and proteinaceous molecular machines, each of which serves a specialized function. In this article we shall present an overview of such microcompartments including (1) the bacterial cytoskeleton and the apparati allowing DNA segregation during cell division; (2) energy transduction apparati involving light-driven proton pumping and ion gradient-driven ATP synthesis; (3) prokaryotic motility and taxis machines that mediate cell movements in response to gradients of chemicals and physical forces; (4) machines of protein folding, secretion and degradation; (5) metabolosomes carrying out specific chemical reactions; (6) 24-hour clocks allowing bacteria to coordinate their metabolic activities with the daily solar cycle, and (7) proteinaceous membrane compartmentalized structures such as sulfur granules and gas vacuoles. Membrane-bound prokaryotic organelles were considered in a recent Journal of Molecular Microbiology and Biotechnology written symposium concerned with membranous compartmentalization in bacteria [J Mol Microbiol Biotechnol 2013;23:1-192]. By contrast, in this symposium, we focus on proteinaceous microcompartments. These two symposia, taken together, provide the interested reader with an objective view of the remarkable complexity of what was once thought of as a simple noncompartmentalized cell.

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Dynamic instability — A common denominator in prokaryotic and eukaryotic DNA segregation and cell division

Cited by 9 publications

References 18 publications

Accessory factors promote AlfA-dependent plasmid segregation by regulating filament nucleation, disassembly, and bundling

Accessory factors promote AlfA-dependent plasmid segregation by regulating filament nucleation, disassembly, and bundling

Molecular machines – a new dimension of biological sciences

Microcompartments and Protein Machines in Prokaryotes

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