Biphasic expression of rnrB in Dictyostelium discoideum suggests a direct relationship between cell cycle control and cell differentiation

MacWilliams, Harry K.; Deichsel, Heike; Gaudet, Pascale; Bonfils, Claire; Tsang, Adrian

doi:10.1046/j.1432-0436.2001.067001012.x

Cited by 14 publications

(17 citation statements)

References 106 publications

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“…In mammalian cells, de novo dNTP biosynthesis components, such as ribonucleotide reductase, are induced at G1-S, satisfying dNTP demand (Magnusson et al, 2003). Dictyostelium ribonucleotide reductase is expressed during growth, repressed during starvation then strongly re-induced after aggregation in prespore cells (MacWilliams et al, 2001;Tsang et al, 1996), 1655 RESEARCH ARTICLE Cell cycle and Dictyostelium development coincident with the widespread S phase we observed. BrdU is only incorporated via salvage pathways, perhaps making mitochondrial incorporation resilient, even if BrdU were out-competed in nuclei by de novo synthesised dTTP.…”

Section: Research Articlementioning

confidence: 67%

Live imaging of theDictyosteliumcell cycle reveals widespread S phase during development, a G2 bias in spore differentiation and a premitotic checkpoint

Muramoto

Chubb

2008

Development

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The regulation of the Dictyostelium cell cycle has remained ambiguous owing to difficulties in long-term imaging of motile cells and a lack of markers for defining cell cycle phases. There is controversy over whether cells replicate their DNA during development, and whether spores are in G1 or G2 of the cell cycle. We have introduced a live-cell S-phase marker into Dictyostelium cells that allows us to precisely define cycle phase. We show that during multicellular development, a large proportion of cells undergo nuclear DNA synthesis. Germinating spores enter S phase only after their first mitosis, indicating that spores are in G2. In addition, we demonstrate that Dictyostelium heterochromatin is copied late in S phase and replicates via accumulation of replication factors, rather than recruitment of DNA to pre-existing factories. Analysis of variability in cycle times indicates that regulation of the cycle manifests at a single random transition in G2, and we present the first identified checkpoint in Dictyostelium, which operates at the G2-M transition in response to DNA damage.

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Section: Research Articlementioning

confidence: 67%

Live imaging of theDictyosteliumcell cycle reveals widespread S phase during development, a G2 bias in spore differentiation and a premitotic checkpoint

Muramoto

Chubb

2008

Development

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“…Several studies have suggested that cells starved late in G2 phase become prespore cells, and cells starved early in G2, M or S phase become prestalk cells (McDonald and Durston, 1984;Weijer et al, 1984a;Ohmori and Maeda, 1987;Gomer and Firtel, 1987;Maeda et al, 1989;Zimmerman and Weijer, 1993;Wood et al, 1996). Cells that exit the cell cycle at different times in could be biased towards a particular cell fate by known cell-cycle regulated signals such as Ca 2+ , or cytosolic pH (Clay et al, 1995;Gross et al, 1983;Leach et al, 1973;Maeda and Maeda, 1974;Saran et al, 1994;Thompson and Kay, 2000;MacWilliams et al, 2001). It is tempting to speculate that some condition imposed by the initial arrest impinges on the regulation of tissue specific mitosis later in development.…”

Section: Discussionmentioning

confidence: 99%

“…Maeda and colleagues have proposed that cells exit the cell cycle at a particular point late in the G2 phase called the 'putative shift' (PS) point and those cells that must traverse G2 under starvation conditions for the longest time in order to arrive at the PS point will have a propensity to differentiate as prestalk cells (Maeda et al, 1989;Maeda, 1993;Araki et al, 1997;Maeda, 1997). Alternatively, it has been suggested that cells either exit the cell cycle early in G2, biasing them to differentiate as prestalk cells, or cells exit the cell cycle late in G2, biasing them to differentiate as prespore cells (MacWilliams et al, 2001). There is general agreement that all cells pause in G2 during the first half of development.…”

Section: Introductionmentioning

confidence: 99%

Tissue-specific G1-phase cell-cycle arrest prior to terminal differentiation inDictyostelium

2004

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The cell cycle status of developing Dictyostelium cells remains unresolved because previous studies have led to conflicting interpretations. We propose a new model of cell cycle events during development. We observe mitosis of about 50% of the cells between 12 and 18 hours of development. Cellular DNA content profiles obtained by flow cytometry and quantification of extra-chromosomal and chromosomal DNA suggest that the daughter cells have half the chromosomal DNA of vegetative cells. Furthermore, little chromosomal DNA synthesis occurs during development, indicating that no S phase occurs. The DNA content in cells sorted by fluorescent tissue-specific reporters indicates that prespore cells divide before prestalk cells and later encapsulate as G1-arrested spores. Consistent with this, germinating spores have one copy of their chromosomes, as judged by fluorescence in situ hybridization and they replicate their chromosomes before mitosis of the emergent amoebae. The DNA content of mature stalk cells suggests that they also attain a G1 state prior to terminal differentiation. As prestalk cells appear to be in G2 up to 22 hours of development, our data suggest that they divide just prior to stalk formation. Our results suggest tissue-specific regulation of G1 phase cell cycle arrest prior to terminal differentiation in Dictyostelium.

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“…6). Given a doubling time of 10-12 hours, a 30-minute M phase and a negligible G1 (Weijer et al, 1984), rblA is maximally expressed in the late G2 phase, when cells have a strong presporedifferentiation preference (Thompson and Kay, 2000;MacWilliams et al, 2001). We then diluted stationary-phase cells into normal or (Weijer et al, 1984), it appears that the spores are also G2 under our conditions.…”

Section: Research Articlementioning

confidence: 96%

“…'Pathway preferences' may result from differences in the composition of the growth medium or in stage of the growth curve when harvested. Preferences may also be found among the cells of a single culture, and here they depend on the cell cycle position of individual amebae at the moment when development begins (reviewed by MacWilliams et al, 2001). Preferences are not absolute but relative, so that cells can be placed in a linear hierarchy from most stalk-preferring to most spore-preferring (Leach et al, 1973;Fortunato et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

A retinoblastoma ortholog controls stalk/spore preference inDictyostelium

MacWilliams¹,

Doquang

Pedrola

et al. 2006

Development

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We describe rblA, the Dictyostelium ortholog of the retinoblastoma susceptibility gene Rb. In the growth phase, rblA expression is correlated with several factors that lead to 'preference' for the spore pathway. During multicellular development, expression increases 200-fold in differentiating spores. rblA-null strains differentiate stalk cells and spores normally, but in chimeras with wild type, the mutant shows a strong preference for the stalk pathway. rblA-null cells are hypersensitive to the stalk morphogen DIF, suggesting that rblA normally suppresses the DIF response in cells destined for the spore pathway. rblA overexpression during growth leads to G1 arrest, but as growing Dictyostelium are overwhelmingly in G2 phase, rblA does not seem to be important in the normal cell cycle. rblA-null cells show reduced cell size and a premature growth-development transition; the latter appears anomalous but may reflect selection pressures acting on social ameba.

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Biphasic expression of rnrB in Dictyostelium discoideum suggests a direct relationship between cell cycle control and cell differentiation

Cited by 14 publications

References 106 publications

Live imaging of theDictyosteliumcell cycle reveals widespread S phase during development, a G2 bias in spore differentiation and a premitotic checkpoint

Live imaging of theDictyosteliumcell cycle reveals widespread S phase during development, a G2 bias in spore differentiation and a premitotic checkpoint

Tissue-specific G1-phase cell-cycle arrest prior to terminal differentiation inDictyostelium

A retinoblastoma ortholog controls stalk/spore preference inDictyostelium

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