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Cytokinesis-based constraints on polarized cell growth in fission yeast.

Bohnert KA, Gould KL - PLoS Genet. (2012)

Bottom Line: Intriguingly, such cells elongated constitutively at new ends unless cytokinesis was perturbed.We posit that such constraints facilitate invasive fungal growth, as cytokinesis mutants displaying bipolar growth defects formed numerous pseudohyphae.Collectively, these data highlight a role for previous cell cycles in defining a cell's capacity to polarize at specific sites, and they additionally provide insight into how a unicellular yeast can transition into a quasi-multicellular state.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute and Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.

ABSTRACT
The rod-shaped fission yeast Schizosaccharomyces pombe, which undergoes cycles of monopolar-to-bipolar tip growth, is an attractive organism for studying cell-cycle regulation of polarity establishment. While previous research has described factors mediating this process from interphase cell tips, we found that division site signaling also impacts the re-establishment of bipolar cell growth in the ensuing cell cycle. Complete loss or targeted disruption of the non-essential cytokinesis protein Fic1 at the division site, but not at interphase cell tips, resulted in many cells failing to grow at new ends created by cell division. This appeared due to faulty disassembly and abnormal persistence of the cell division machinery at new ends of fic1Δ cells. Moreover, additional mutants defective in the final stages of cytokinesis exhibited analogous growth polarity defects, supporting that robust completion of cell division contributes to new end-growth competency. To test this model, we genetically manipulated S. pombe cells to undergo new end take-off immediately after cell division. Intriguingly, such cells elongated constitutively at new ends unless cytokinesis was perturbed. Thus, cell division imposes constraints that partially override positive controls on growth. We posit that such constraints facilitate invasive fungal growth, as cytokinesis mutants displaying bipolar growth defects formed numerous pseudohyphae. Collectively, these data highlight a role for previous cell cycles in defining a cell's capacity to polarize at specific sites, and they additionally provide insight into how a unicellular yeast can transition into a quasi-multicellular state.

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Model of Fic1's involvement in cytokinesis and the establishment of bipolar growth in S.pombe. During cytokinesis, Fic1 serves as a scaffold for SH3 proteins, including Cdc15, at the cytokinetic ring. In the absence of Fic1, its interactions, or a parallel pathway, the completion of cell division is perturbed, and the cell division machinery persists at the previous division site. Failure to robustly complete cytokinesis impedes new end growth, even if NETO signaling is prematurely activated. Cytokinesis-based constraints on new end growth polarity aid in the transition into invasive fungal growth.
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pgen-1003004-g010: Model of Fic1's involvement in cytokinesis and the establishment of bipolar growth in S.pombe. During cytokinesis, Fic1 serves as a scaffold for SH3 proteins, including Cdc15, at the cytokinetic ring. In the absence of Fic1, its interactions, or a parallel pathway, the completion of cell division is perturbed, and the cell division machinery persists at the previous division site. Failure to robustly complete cytokinesis impedes new end growth, even if NETO signaling is prematurely activated. Cytokinesis-based constraints on new end growth polarity aid in the transition into invasive fungal growth.

Mentions: In this study, we have shown how cytokinesis and cell polarity crosstalk to regulate fission yeast morphogenesis. Our data support a model (Figure 10) in which Fic1 acts as an adaptor at the CR, where it guides proper completion of cytokinesis and thereby affects division site remodeling. Loss of Fic1, its interactions, or parallel pathways results in delayed growth at new ends, even upon constitutive activation of NETO signaling. Impaired bipolar cell growth resulting from defective cytokinesis in turn enhances S. pombe invasiveness.


Cytokinesis-based constraints on polarized cell growth in fission yeast.

Bohnert KA, Gould KL - PLoS Genet. (2012)

Model of Fic1's involvement in cytokinesis and the establishment of bipolar growth in S.pombe. During cytokinesis, Fic1 serves as a scaffold for SH3 proteins, including Cdc15, at the cytokinetic ring. In the absence of Fic1, its interactions, or a parallel pathway, the completion of cell division is perturbed, and the cell division machinery persists at the previous division site. Failure to robustly complete cytokinesis impedes new end growth, even if NETO signaling is prematurely activated. Cytokinesis-based constraints on new end growth polarity aid in the transition into invasive fungal growth.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3475658&req=5

pgen-1003004-g010: Model of Fic1's involvement in cytokinesis and the establishment of bipolar growth in S.pombe. During cytokinesis, Fic1 serves as a scaffold for SH3 proteins, including Cdc15, at the cytokinetic ring. In the absence of Fic1, its interactions, or a parallel pathway, the completion of cell division is perturbed, and the cell division machinery persists at the previous division site. Failure to robustly complete cytokinesis impedes new end growth, even if NETO signaling is prematurely activated. Cytokinesis-based constraints on new end growth polarity aid in the transition into invasive fungal growth.
Mentions: In this study, we have shown how cytokinesis and cell polarity crosstalk to regulate fission yeast morphogenesis. Our data support a model (Figure 10) in which Fic1 acts as an adaptor at the CR, where it guides proper completion of cytokinesis and thereby affects division site remodeling. Loss of Fic1, its interactions, or parallel pathways results in delayed growth at new ends, even upon constitutive activation of NETO signaling. Impaired bipolar cell growth resulting from defective cytokinesis in turn enhances S. pombe invasiveness.

Bottom Line: Intriguingly, such cells elongated constitutively at new ends unless cytokinesis was perturbed.We posit that such constraints facilitate invasive fungal growth, as cytokinesis mutants displaying bipolar growth defects formed numerous pseudohyphae.Collectively, these data highlight a role for previous cell cycles in defining a cell's capacity to polarize at specific sites, and they additionally provide insight into how a unicellular yeast can transition into a quasi-multicellular state.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute and Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.

ABSTRACT
The rod-shaped fission yeast Schizosaccharomyces pombe, which undergoes cycles of monopolar-to-bipolar tip growth, is an attractive organism for studying cell-cycle regulation of polarity establishment. While previous research has described factors mediating this process from interphase cell tips, we found that division site signaling also impacts the re-establishment of bipolar cell growth in the ensuing cell cycle. Complete loss or targeted disruption of the non-essential cytokinesis protein Fic1 at the division site, but not at interphase cell tips, resulted in many cells failing to grow at new ends created by cell division. This appeared due to faulty disassembly and abnormal persistence of the cell division machinery at new ends of fic1Δ cells. Moreover, additional mutants defective in the final stages of cytokinesis exhibited analogous growth polarity defects, supporting that robust completion of cell division contributes to new end-growth competency. To test this model, we genetically manipulated S. pombe cells to undergo new end take-off immediately after cell division. Intriguingly, such cells elongated constitutively at new ends unless cytokinesis was perturbed. Thus, cell division imposes constraints that partially override positive controls on growth. We posit that such constraints facilitate invasive fungal growth, as cytokinesis mutants displaying bipolar growth defects formed numerous pseudohyphae. Collectively, these data highlight a role for previous cell cycles in defining a cell's capacity to polarize at specific sites, and they additionally provide insight into how a unicellular yeast can transition into a quasi-multicellular state.

Show MeSH
Related in: MedlinePlus