Open Questions about the Roles of DnaA, Related Proteins, and Hyperstructure Dynamics in the Cell Cycle

Kohiyama, Masamichi; Herrick, John; Norris, Vic

doi:10.3390/life13091890

Cited by 4 publications

(3 citation statements)

References 178 publications

(230 reference statements)

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“…This implies properties like the permeability of the nucleoid to macromolecules involved in transcription and translation. As described by Kohiyama et al [64] the replication bubble starts with a DnaA-based hyperstructure that integrates the many proteins involved in metabolic and regulatory pathways necessary for the initiation of replication. Here, however, only the structural aspects of the nascent chromosome arms and their behavior during segregation are considered.…”

Section: Replichore Movement To Opposite Halves Of the Nucleoidmentioning

confidence: 99%

Compaction and Segregation of DNA in Escherichia coli

Woldringh

2024

Preprint

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Theoretical and experimental approaches have been applied to study the polymer physics under-lying compaction of DNA in the bacterial nucleoid. Knowledge of the compaction mechanism is necessary to obtain a mechanistic understanding of the process of segregation of replicating chromosome arms (replichores) during the cell cycle. In the first part of this review light microscope observations are discussed that have demonstrated that the nucleoid has a lower refractive index and thus a lower density than the cytoplasm. A polymer-physical explanation for this phenomenon was given by the theory of Theo Odijk pro-posed in 1998. By assuming a phase separation between nucleoid and cytoplasm and by imposing equality of osmotic pressure and chemical potential between the two phases, a minimal energy situation is obtained in which soluble proteins are depleted from the nucleoid, thus explaining its lower density. The theory is compared with recent views for DNA compaction that are based on mere exclusion of polyribosomes from the nucleoid or on the transcriptional activity of the cell. These new views raise the question of whether they can still explain the lower refractive index or density of the nucleoid. In the second part of this review the question is discussed how DNA segregation occurs in Esche-richia coli, in the absence of the so-called active ParABS system, present in the majority of bacteria. How is entanglement prevented of nascent chromosome arms, generated at the origin in the pa-rental network of the E. coli nucleoid? The observations of the groups of Sherratt and Hansen in 2006, that the four nascent chromosome arms synthesized in the initial replication bubble, segre-gate to opposite halves of the sister nucleoids implies that extensive intermingling of daughter strands does not occur. Based on the hypothesis that leading and lagging replichores synthesized in the replication bubble, fold into micro-domains that do not intermingle, a passive "four-excluding-arms model" for segregation is proposed. This model implies that the key for seg-regation already lies in the structure of the replication bubble at the very start of DNA replication; it explains the different patterns of chromosome arms as well as the segregation distances between replicated loci as experimentally observed.

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Section: Replichore Movement To Opposite Halves Of the Nucleoidmentioning

confidence: 99%

Compaction and Segregation of DNA in Escherichia coli

Woldringh

2024

Preprint

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“…Or does segregation occur in a relatively homogeneous nucleoid, where small soluble proteins are depleted to some extent from the nucleoid, as proposed by Odijk ([ 5 ]; see also [ 35 ])? As described by Kohiyama et al [ 67 ], the replication bubble starts with a DnaA-based hyperstructure that integrates the many proteins involved in the necessary metabolic and regulatory pathways for the initiation of replication. Here, however, only the structural aspects of the nascent chromosome arms and their behavior during segregation are considered.…”

Section: Segregation and Movement Of Chromosome Arms (Replichores)mentioning

confidence: 99%

Compaction and Segregation of DNA in Escherichia coli

Woldringh

2024

Life

View full text Add to dashboard Cite

Theoretical and experimental approaches have been applied to study the polymer physics underlying the compaction of DNA in the bacterial nucleoid. Knowledge of the compaction mechanism is necessary to obtain a mechanistic understanding of the segregation process of replicating chromosome arms (replichores) during the cell cycle. The first part of this review discusses light microscope observations demonstrating that the nucleoid has a lower refractive index and thus, a lower density than the cytoplasm. A polymer physics explanation for this phenomenon was given by a theory discussed at length in this review. By assuming a phase separation between the nucleoid and the cytoplasm and by imposing equal osmotic pressure and chemical potential between the two phases, a minimal energy situation is obtained, in which soluble proteins are depleted from the nucleoid, thus explaining its lower density. This theory is compared to recent views on DNA compaction that are based on the exclusion of polyribosomes from the nucleoid or on the transcriptional activity of the cell. These new views prompt the question of whether they can still explain the lower refractive index or density of the nucleoid. In the second part of this review, we discuss the question of how DNA segregation occurs in Escherichia coli in the absence of the so-called active ParABS system, which is present in the majority of bacteria. How is the entanglement of nascent chromosome arms generated at the origin in the parental DNA network of the E. coli nucleoid prevented? Microscopic observations of the position of fluorescently-labeled genetic loci have indicated that the four nascent chromosome arms synthesized in the initial replication bubble segregate to opposite halves of the sister nucleoids. This implies that extensive intermingling of daughter strands does not occur. Based on the hypothesis that leading and lagging replichores synthesized in the replication bubble fold into microdomains that do not intermingle, a passive four-excluding-arms model for segregation is proposed. This model suggests that the key for segregation already exists in the structure of the replication bubble at the very start of DNA replication; it explains the different patterns of chromosome arms as well as the segregation distances between replicated loci, as experimentally observed.

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“…Kohiyama [10] tries, in his words, "to throw a cobblestone in the pond" (from the French 'jeter un pavé dans la mare'). He and his colleagues revisit the DnaA story from the point of view of hyperstructures; they propose the existence of a physico-chemical clock that simultaneously triggers the initiation of chromosome replication and of cell division.…”

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confidence: 99%