Cell wall remodeling at the fission yeast cell division site requires the Rho-GEF Rgf3p

Morrell‐Falvey, Jennifer L.; Ren, Liping; Feoktistova, Anna; Haese, Greg Den; Gould, Kathleen L.

doi:10.1242/jcs.02664

Cited by 56 publications

(122 citation statements)

References 59 publications

(90 reference statements)

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“…Interestingly, depletion of Rho1p or mutation of one of its exchange factors, Rgf3, caused a cell lysis phenotype (Arellano et al 1997;Tajadura et al 2004;Morrell-Falvey et al 2005;Mutoh et al 2005) that is extremely similar to that which we observed in the sid2-250 mutant cells at low restrictive temperatures. We decided to examine whether enhancing 1,3-bd-glucan synthesis by slightly overexpressing Rho1p can rescue the lysis phenotype in sid2-250 mutant cells.…”

Section: Resultssupporting

confidence: 75%

“…In addition, the lysis of cells caused by switching off Rgf3p can be rescued by sorbitol, while Rho1p-depleted cells cannot, suggesting that Rgf3p controls a subset of the functions of Rho1p in cell wall biosynthesis (Arellano et al 1997;Tajadura et al 2004;Morrell-Falvey et al 2005;Mutoh et al 2005). More interestingly, both Rho1p and Rgf3p localize at the septum (Arellano et al 1997;Tajadura et al 2004;Morrell-Falvey et al 2005;Mutoh et al 2005), strongly suggesting that they are involved in cell wall biosynthesis at the septum. Thus, it is an intriguing possibility that the SIN targets Rho1 as one of its downstream effectors; this could be achieved by activating Rgf3, which is a specific Rho1 GEF for its function in cell wall biosynthesis (Tajadura et al 2004).…”

Section: Discussionmentioning

confidence: 99%

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A Role for the Septation Initiation Network in Septum Assembly Revealed by Genetic Analysis of sid2-250 Suppressors

et al. 2006

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In the fission yeast Schizosaccharomyces pombe the septation initiation network (SIN) is required for stabilization of the actomyosin ring in late mitosis as well as for ring constriction and septum deposition. In a genetic screen for suppressors of the SIN mutant sid2-250, we isolated a mutation, ace2-35, in the transcription factor Ace2p. Both ace2D and ace2-35 show defects in cell separation, and both can rescue the growth defects of some SIN mutants at low restrictive temperatures, where the SIN single mutants lyse at the time of cytokinesis. By detailed analysis of the formation and constriction of the actomyosin ring and septum in the sid2-250 mutant at low restrictive temperatures, we show that the lysis phenotype of the sid2-250 mutant is likely due to a weak cell wall and septum combined with enzymatic activity of septumdegrading enzymes. Consistent with the recent findings that Ace2p controls transcription of genes involved in cell separation, we show that disruption of some of these genes can also rescue sid2-250 mutants. Consistent with SIN mutants having defects in septum formation, many SIN mutants can be rescued at the low restrictive temperature by the osmotic stabilizer sorbitol. The small GTPase Rho1 is known to promote cell wall formation, and we find that Rho1p expressed from a multi-copy plasmid can also rescue sid2-250 at the low restrictive temperature. Together these results suggest that the SIN has a role in promoting proper cell wall formation at the division septa.

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Section: Resultssupporting

confidence: 75%

Section: Discussionmentioning

confidence: 99%

A Role for the Septation Initiation Network in Septum Assembly Revealed by Genetic Analysis of sid2-250 Suppressors

et al. 2006

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“…Overexpression of rgf1 + , encoding the main Rho1-GEF (García et al 2006), rescued the growth of rho1-596 mutant cells, but overexpression of rgf3 + , encoding the cytokinesis specific Rho1-GEF (Tajadura et al 2004;Morrell-Falvey et al 2005;Mutoh et al 2005), did not ( Figure S1A). These results suggest that rho1-596 growth defects are not restricted to cytokinesis.…”

Section: Rho1-596 Is a Thermosensitive Strain With Severe Cell Wall Dmentioning

confidence: 99%

Negative Functional Interaction Between Cell Integrity MAPK Pathway and Rho1 GTPase in Fission Yeast

et al. 2013

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Rho1 GTPase is the main activator of cell wall glucan biosynthesis and regulates actin cytoskeleton in fungi, including Schizosaccharomyces pombe. We have obtained a fission yeast thermosensitive mutant strain carrying the rho1-596 allele, which displays reduced Rho1 GTPase activity. This strain has severe cell wall defects and a thermosensitive growth, which is partially suppressed by osmotic stabilization. In a global screening for rho1-596 multicopy suppresors the pmp1 + gene was identified. Pmp1 is a dual specificity phosphatase that negatively regulates the Pmk1 mitogen-activated protein kinase (MAPK) cell integrity pathway. Accordingly, elimination of Pmk1 MAPK partially rescued rho1-596 thermosensitivity, corroborating the unexpected antagonistic functional relationship of these genes. We found that rho1-596 cells displayed increased basal activation of the cell integrity MAPK pathway and therefore were hypersensitive to MgCl 2 and FK506. Moreover, the absence of calcineurin was lethal for rho1-596. We found a higher level of calcineurin activity in rho1-596 than in wild-type cells, and overexpression of constitutively active calcineurin partially rescued rho1-596 thermosensitivity. All together our results suggest that loss of Rho1 function causes an increase in the cell integrity MAPK activity, which is detrimental to the cells and turns calcineurin activity essential. RHO GTPases are conserved proteins that regulate the actin cytoskeleton organization in all eukaryots (Heasman and Ridley 2008). Additionally, in yeast and other fungi, these GTPases provide the coordinated regulation of cell wall biosynthesis and actin organization, which is required to maintain cell integrity and polarized growth (Levin 2005;Park and Bi 2007;Perez and Cansado 2010). The Schizosaccharomyces pombe genome contains six genes coding Rho GTPases. Among them, rho1 + is essential (Arellano et al. 1996). Rho1 function is mediated by its interaction with at least three different targets: the b(1,3)-glucan synthase (Arellano et al. 1996), which is responsible for the synthesis of the major cell wall component, and the kinases Pck1 and Pck2 Sayers et al. 2000). Through both kinases, Rho1 also regulates the cell wall synthesis. Rho2 also interacts with Pck2 and, therefore, both GTPases regulate the a-D-glucan synthesis through Pck2 (Katayama et al. 1999;Calonge et al. 2000). Lack of Rho1 is lethal, and this phenotype is not suppressed by osmotic stabilization (Arellano et al. 1997), suggesting that defective biosynthesis of the cell wall is not the unique cause of death. On the contrary, Rho2-less cells are viable, although they become slightly rounded and more sensitive to treatment with glucanases (Hirata et al. 1998). Rho2 and Pck2 participate in the activation of the cell integrity mitogen-activated protein kinase (MAPK) signaling pathway (Ma et al. 2006). This signaling cascade responds to different extracellular stress stimuli such as hyper-or hypotonic conditions, oxidative stress, cell wall damaging compounds, and g...

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“…The regulation of Rho1p in fission yeast involves at least three GEFs (Rgf1p, Rgf2p, and Rgf3p) and several putative GAPs (Rga1p,Rga5p,and Rga8p). rgf3 ϩ is an essential gene and the protein specifically activates Rho1p during cytokinesis (Tajadura et al, 2004;Morrell-Falvey et al, 2005;Mutoh et al, 2005). Rgf1p and Rgf2p are the closest relatives, and they provide a redundant function for the activation of Rho1p (Mutoh et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

The Rho1p Exchange Factor Rgf1p Signals Upstream from the Pmk1 Mitogen-activated Protein Kinase Pathway in Fission Yeast

Garcia

Tajadura²,

Sánchez

2009

MBoC

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The Schizosaccharomyces pombe exchange factor Rgf1p specifically regulates Rho1p during polarized growth. Rgf1p activates the ␤-glucan synthase (GS) complex containing the catalytic subunit Bgs4p and is involved in the activation of growth at the second end, a transition that requires actin reorganization. In this work, we investigated Rgf1p signaling and observed that Rgf1p acted upstream from the Pck2p-Pmk1p MAPK signaling pathway. We noted that Rgf1p and calcineurin play antagonistic roles in Cl ؊ homeostasis; rgf1⌬ cells showed the vic phenotype (viable in the presence of immunosuppressant and chlorine ion) and were unable to grow in the presence of high salt concentrations, both phenotypes being characteristic of knockouts of the MAPK components. In addition, mutations that perturb signaling through the MAPK pathway resulted in defective cell integrity (hypersensitivity to caspofungin and ␤-glucanase). Rgf1p acts by positively regulating a subset of stimuli toward the Pmk1p-cell integrity pathway. After osmotic shock and cell wall damage HA-tagged Pmk1p was phosphorylated in wild-type cells but not in rgf1⌬ cells. Finally, we provide evidence to show that Rgf1p regulates Pmk1p activation in a process that involves the activation of Rho1p and Pck2p, and we demonstrate that Rgf1p is unique in this signaling process, because Pmk1p activation was largely independent of the other two Rho1p-specific GEFs, Rgf2p and Rgf3p.

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Cell wall remodeling at the fission yeast cell division site requires the Rho-GEF Rgf3p

Cited by 56 publications

References 59 publications

A Role for the Septation Initiation Network in Septum Assembly Revealed by Genetic Analysis of sid2-250 Suppressors

A Role for the Septation Initiation Network in Septum Assembly Revealed by Genetic Analysis of sid2-250 Suppressors

Negative Functional Interaction Between Cell Integrity MAPK Pathway and Rho1 GTPase in Fission Yeast

The Rho1p Exchange Factor Rgf1p Signals Upstream from the Pmk1 Mitogen-activated Protein Kinase Pathway in Fission Yeast

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