Analysis of the cps1 gene provides evidence for a septation checkpoint in Schizosaccharomyces pombe

Goff, Xavier Le; Woollard, Alison; Simanis, Viesturs

doi:10.1007/s004380051071

Cited by 118 publications

(157 citation statements)

References 46 publications

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“…Previous studies have shown that structural defects in the actomyosin ring are monitored via a checkpoint mechanism that involves the protein phosphatase Clp1p/Flp1p and the SIN (Le Goff et al, 1999;Liu et al, 1999Liu et al, , 2000Cueille et al, 2001;Trautmann et al, 2001;Mishra et al, 2004). We have shown that clp1⌬ displays an additive deleterious effect in combination with pdk1⌬, consistent with the idea that pdk1⌬ cells assemble structurally defective rings and that their maximal viability depends on Clp1p function.…”

Section: Discussionsupporting

confidence: 88%

“…In particular, it is interesting to note that Sid2p is related to members of the AGC family of kinases (Sparks et al, 1999;Tamaskovic et al, 2003) which are known to be regulated by PDK1 family members (Belham et al, 1999). However, the finding that SIN proteins participate in correcting defects associated with the cell division apparatus (Le Goff et al, 1999;Liu et al, 1999;Mishra et al, 2004) might provide an alternate explanation to the observed synthetic lethality between pdk1⌬ and SIN mutants.…”

Section: Discussionmentioning

confidence: 99%

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Roles of Pdk1p, a Fission Yeast Protein Related to Phosphoinositide-dependent Protein Kinase, in the Regulation of Mitosis and Cytokinesis

Bimbó

Liu

Balasubramanian

2005

MBoC

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Proteins related to the phosphoinositide-dependent protein kinase family have been identified in the majority of eukaryotes. Although much is known about upstream mechanisms that regulate the PDK1-family of kinases in metazoans, how these kinases regulate cell growth and division remains unclear. Here, we characterize a fission yeast protein related to members of this family, which we have termed Pdk1p. Pdk1p localizes to the spindle pole body and the actomyosin ring in early mitotic cells. Cells deleted for pdk1 display multiple defects in mitosis and cytokinesis, all of which are exacerbated when the function of fission yeast polo kinase, Plo1p, is partially compromised. We conclude that Pdk1p functions in concert with Plo1p to regulate multiple processes such as the establishment of a bipolar mitotic spindle, transition to anaphase, placement of the actomyosin ring and proper execution of cytokinesis. We also present evidence that the effects of Pdk1p on cytokinesis are likely mediated via the fission yeast anillin-related protein, Mid1p, and the septation initiation network. INTRODUCTIONThe segregation of chromosomes during mitosis and the physical division of cells during cytokinesis represent two irreversible events in the cell cycle. Not surprisingly, mitosis and cytokinesis are tightly regulated in the cell cycle in such a way that mitosis is initiated only upon completion of DNA synthesis and cytokinesis is executed only after completion of mitosis.The fission yeast Schizosaccharomyces pombe has been used extensively for the study of mitosis and cytokinesis, due to the structural and molecular conservation of these events in fission yeast and metazoans (Nurse 1990;Gould and Simanis, 1997;Feierbach and Chang, 2001). S. pombe has three chromosomes that condense during mitosis and are separated along an intranuclear mitotic spindle (Yanagida, 1998). After chromosome segregation, S. pombe cells divide through the use of an actomyosin-based contractile ring. Gene products important for mitotic entry, mitotic progression, and cytokinesis have been identified from a number of genetic screens, as well as from reverse genetic approaches (Nurse et al., 1976;Hirano et al., 1986;Chang et al., 1996;Balasubramanian et al., 1998). Central to the regulation of mitosis and cytokinesis are the S. pombe polo-related protein kinase Plo1p (Ohkura et al., 1995;Bähler et al., 1998;Mulvihill et al., 1999) and members of the septation initiation network (SIN), a signaling pathway comprised of three protein kinases (Cdc7p, Sid1p, and Sid2p) and a GTPase (Spg1p) Rajagopalan et al., 2003). Members of the polo-kinase family are conserved across all eukaryotes (Nigg, 1998). In addition, several components of the SIN are highly conserved, including an analogous signaling complex in the budding yeast referred to as the mitotic exit network (Bardin and Amon, 2001;McCollum and Gould, 2001;Simanis, 2003). The fission yeast Plo1p-kinase and SIN components localize to the spindle pole body and coordinate mitotic events with cytokinesis .To...

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Roles of Pdk1p, a Fission Yeast Protein Related to Phosphoinositide-dependent Protein Kinase, in the Regulation of Mitosis and Cytokinesis

Bimbó

Liu

Balasubramanian

2005

MBoC

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“…However, because these studies are done at temperatures where there is still some residual SIN function, it is unclear whether the SIN is required for bulk septum synthesis. Although at high restrictive temperatures SIN mutants do not make septa, it is not clear if this is an indirect effect due to the disappearance of the actomyosin ring, which is required for localization of septum-synthesizing enzymes (Le Goff et al 1999;Liu et al 1999;Cortes et al 2002), making this issue difficult to resolve.…”

Section: Discussionmentioning

confidence: 99%

“…Recently, several enzymes involved in synthesis of 1,3-b-glucan and 1,3-a-glucan have been identified, and all of them are large integral membrane proteins. As 1,3-b-glucan synthase subunits, Cps1p/Bgs1p and Bgs4p are required for assembly of 1,3-b-glucan and thus of the primary septum (Le Goff et al 1999;Liu et al 1999;Cortes et al 2002Cortes et al , 2005. The enzyme complex involved in 1,3-b-glucan synthesis requires not only synthase subunits but also regulatory 1 subunit(s).…”

mentioning

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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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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“…The SIN triggers actomyosin ring contraction coordinated with the synthesis of the primary and secondary septa that will form the new cell wall (Krapp et al 2004;Wolfe and Gould 2005). The small GTPase Rho1 is known to promote cell-wall formation at the division site by stimulation of Cps1p/ Drc1 1,3-b-glucan synthase (Le Goff et al 1999), but the mechanism remains unclear.…”

Section: T He Fission Yeast Schizosaccharomyces Pombe Is a Lead-mentioning

confidence: 99%

Antagonistic Roles of PP2A-Pab1 and Etd1 in the Control of Cytokinesis in Fission Yeast

et al. 2010

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In Schizosaccharomyces pombe, Etd1 is a positive regulator of the septation initiation network (SIN), a conserved GTPase-regulated kinase cascade that triggers cytokinesis. Here we show that a mutation in the pab1 gene, which encodes the B-regulatory subunit of the protein phosphatase 2A (PP2A), suppresses mutations in the etd1 gene. Etd1 is required for the function of the GTPase Spg1, a key regulator of SIN signaling. Interestingly, the loss of Pab1 function restored the activity of Spg1 in Etd1-deficient cells. This result suggests that PP2A-Pab1-mediated dephosphorylation inhibits Spg1, thus antagonizing Etd1 function. The loss of pab1 function also rescues the lethality of mutants of other genes in the SIN cascade such as mob1, sid1, and cdc11. Two-hybrid assays indicate that Pab1 physically interacts with Mob1, Sid1, Sid2, and Cdc11, suggesting that the phosphatase 2A B-subunit is a component of the SIN complex. Together, our results indicate that PP2A-Pab1 plays a novel role in cytokinesis, regulating SIN activity at different levels. Pab1 is also required to activate polarized cell growth. Thus, PP2A-Pab1 may be involved in coordinating polar growth and cytokinesis.

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Analysis of the cps1 gene provides evidence for a septation checkpoint in Schizosaccharomyces pombe

Cited by 118 publications

References 46 publications

Roles of Pdk1p, a Fission Yeast Protein Related to Phosphoinositide-dependent Protein Kinase, in the Regulation of Mitosis and Cytokinesis

Roles of Pdk1p, a Fission Yeast Protein Related to Phosphoinositide-dependent Protein Kinase, in the Regulation of Mitosis and Cytokinesis

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

Antagonistic Roles of PP2A-Pab1 and Etd1 in the Control of Cytokinesis in Fission Yeast

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