A DNA architectural protein couples cellular physiology and DNA topology in <i>Escherichia coli</i>

Schneider, Robert; Travers, Andrew; Kutateladze, Tamara; Muskhelishvili, Georgi

doi:10.1046/j.1365-2958.1999.01656.x

Cited by 155 publications

(145 citation statements)

References 59 publications

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“…Consistent with this structure, the absence of FIS can be compensated by increased negative superhelicity leading to the hypothesis that FIS acts as a topological homeostat, stabilizing the local writhe conducive for untwisting of the GC-rich stable RNA promoters (Rochman et al 2002;Muskhelishvili and Travers 2003). At the same time, FIS was found to repress the expression of the genes encoding DNA gyrase (Schneider et al 1999). Thus, in this case, a major DNA architectural protein coordinates the global and local structure of the DNA.…”

Section: Fis-rna Polymerase Complexmentioning

confidence: 73%

The regulatory role of DNA supercoiling in nucleoprotein complex assembly and genetic activity

Muskhelishvili

Travers

2016

Biophys Rev

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We argue that dynamic changes in DNA supercoiling in vivo determine both how DNA is packaged and how it is accessed for transcription and for other manipulations such as recombination. In both bacteria and eukaryotes, the principal generators of DNA superhelicity are DNA translocases, supplemented in bacteria by DNA gyrase. By generating gradients of superhelicity upstream and downstream of their site of activity, translocases enable the differential binding of proteins which preferentially interact with respectively more untwisted or more writhed DNA. Such preferences enable, in principle, the sequential binding of different classes of protein and so constitute an essential driver of chromatin organization.Keywords DNA supercoiling . DNA translocases . Chromatin organization . Superhelicity gradients . DNA untwisting . DNAwrithing Dynamic changes of DNA supercoiling act as a driving force behind the alterations of genetic activity and DNA compaction both in eukaryotes and prokaryotes. Both these processes involve formation of spatially organized nucleoprotein structures by DNA architectural proteins. Whereas in eukaryotes the paradigmal example is the histone octamer, in prokaryotes a similar function is attributed to a small class of highly abundant nucleoid-associated proteins. We argue that, depending on the primary sequence organization, the changes of superhelicity elicit various alterations of local DNA geometry, while these, in turn, facilitate the assembly of distinct nucleoprotein structures pertinent to genetic function. Genome-wide conversion of the superhelical energy into various three-dimensional DNA structures thus acts as an analogue code coordinating the energy supply with the genetic expression of the chromosome.Recent studies make it increasingly clear that the DNA double helix carries at least two types of encoded information and that these include the well-known genetic code and the structural information determining the form and physical properties of the double helix itself. Since both these information types are inscribed in the same DNA sequence, and yet one is discrete whereas the other is continuous, they have been respectively dubbed the digital and analog DNA codes (Marr et al. 2008;Travers et al. 2012;Muskhelishvili and Travers 2013). The potential of the DNA to adopt distinct configurations is strongly modulated by DNA supercoiling, which is increasingly recognized as one of the major forces coordinating the cellular DNA transactions in both prokaryotes (including Archaea) and eukaryotes.DNA supercoiling can be generated by the simple application of torque to the double helix (Strick et al. 1998) but, importantly, because the DNA molecule itself possesses chirality-it is, after all, a right-handed double helix-the local structures stabilized by changes in superhelical density depend on both the sign and strength of the applied torque. For example, both positive and negative torque (respectively overand underwinding of the double helix) can change the intrinsic coiling of ...

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Section: Fis-rna Polymerase Complexmentioning

confidence: 73%

The regulatory role of DNA supercoiling in nucleoprotein complex assembly and genetic activity

Muskhelishvili

Travers

2016

Biophys Rev

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“…This activity might play an important role in governing the global dynamics of chromatin reshaping in bacteria. Fis was, however, also identified as a pleiotropic regulator of gene expression [Bosch et al, 1990;Schneider et al, 1999;Hirvonen et al, 2001;Kelly et al, 2004] and site-specific recombination [Koch and Kahmann, 1986;Thompson et al, 1987]. It is thought to act as a topological homeostat that modulates local supercoiling in selected promoter regions in order to maintain conditions that are favorable for transcription.…”

Section: Mechansims Of Nucleoid Organizationmentioning

confidence: 99%

The bacterial nucleoid: A highly organized and dynamic structure

Thanbichler

Wang

Shapiro

2005

J of Cellular Biochemistry

122

101

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Recent advances in bacterial cell biology have revealed unanticipated structural and functional complexity, reminiscent of eukaryotic cells. Particular progress has been made in understanding the structure, replication, and segregation of the bacterial chromosome. It emerged that multiple mechanisms cooperate to establish a dynamic assembly of supercoiled domains, which are stacked in consecutive order to adopt a defined higher-level organization. The position of genetic loci on the chromosome is thereby linearly correlated with their position in the cell. SMC complexes and histone-like proteins continuously remodel the nucleoid to reconcile chromatin compaction with DNA replication and gene regulation. Moreover, active transport processes ensure the efficient segregation of sister chromosomes and the faithful restoration of nucleoid organization while DNA replication and condensation are in progress.

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“…Thus, factor for inversion stimulation (FIS), a NAP abundant during the early exponential phase (18), regulates expression not only of the superhelicity determinants DNA gyrase subunits A and B (gyrA and gyrB) and topoisomerase I (topA) (19)(20)(21) but also other NAP-encoding genes including hns, α subunit of histone-like protein from E. coli strain U93 (hupA), and DNA binding protein from starved cells (dps) (22)(23)(24) and components of the transcription machinery such as σ 38 subunit of RNA polymerase rpoS (25). Similarly mutations affecting the selectivity of RNAP influence NAP production (26)(27)(28).…”

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confidence: 99%

Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle

Sobetzko

Travers²,

Muskhelishvili³

2011

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

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203

261

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In Escherichia coli crosstalk between DNA supercoiling, nucleoid-associated proteins and major RNA polymerase σ initiation factors regulates growth phase-dependent gene transcription. We show that the highly conserved spatial ordering of relevant genes along the chromosomal replichores largely corresponds both to their temporal expression patterns during growth and to an inferred gradient of DNA superhelical density from the origin to the terminus. Genes implicated in similar functions are related mainly in trans across the chromosomal replichores, whereas DNA-binding transcriptional regulators interact predominantly with targets in cis along the replichores. We also demonstrate that macrodomains (the individual structural partitions of the chromosome) are regulated differently. We infer that spatial and temporal variation of DNA superhelicity during the growth cycle coordinates oxygen and nutrient availability with global chromosome structure, thus providing a mechanistic insight into how the organization of a complete bacterial chromosome encodes a spatiotemporal program integrating DNA replication and global gene expression. In Escherichia coli cells the physiological transitions induced by the changing growth environment are accompanied by changes in DNA superhelical density (1-3), nucleoid structure (4-6), and the promoter selectivity of the RNA polymerase (RNAP) holoenzyme (3, 7). During the growth cycle both the relative and absolute concentrations of the abundant nucleoid-associated proteins (NAPs ; Table S1) change substantially and correspondingly generate bacterial chromatin of variable composition (8, 9). The NAPs stabilize distinct supercoil structures (10-12) selectively favoring particular RNAP holoenzymes (13-15). These variable nucleoprotein complexes modulate DNA topology during the growth cycle (Fig. 1A), optimizing the channeling of supercoil energy into appropriate metabolic pathways (16,17).The expression of the genes determining superhelical density, polymerase selectivity, and nucleoid structure is coordinated by cross-regulation. Thus, factor for inversion stimulation (FIS), a NAP abundant during the early exponential phase (18), regulates expression not only of the superhelicity determinants DNA gyrase subunits A and B (gyrA and gyrB) and topoisomerase I (topA) (19-21) but also other NAP-encoding genes including hns, α subunit of histone-like protein from E. coli strain U93 (hupA), and DNA binding protein from starved cells (dps) (22-24) and components of the transcription machinery such as σ 38 subunit of RNA polymerase rpoS (25). Similarly mutations affecting the selectivity of RNAP influence NAP production (26-28). Again, mutations in the genes controlling DNA superhelicity affect the production of both NAPs and the basal transcription machinery (27,29). This pattern of integrated control constitutes a heterarchical network coordinating chromosome structure with cellular metabolism (27,28,30). A further pointer to this integrated network is the observed selection of mutations in fis...

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A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli

Cited by 155 publications

References 59 publications

The regulatory role of DNA supercoiling in nucleoprotein complex assembly and genetic activity

The regulatory role of DNA supercoiling in nucleoprotein complex assembly and genetic activity

The bacterial nucleoid: A highly organized and dynamic structure

Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle

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