Fission yeast Clp1p phosphatase regulates G2/M transition and coordination of cytokinesis with cell cycle progression

Trautmann, Susanne; Wolfe, Benjamin; Jorgensen, Paul; Tyers, Mike; Gould, Kathleen L.; McCollum, Dannel

doi:10.1016/s0960-9822(01)00268-8

Cited by 186 publications

(331 citation statements)

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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%

“…This could result from improper assembly/function of the actomyosin ring or from defective SIN signaling. Mishra et al (2004) recently reported that a checkpoint mechanism that depends on the protein phosphatase Clp1p/Flp1p (Cueille et al, 2001;Trautmann et al, 2001), and SIN allows for completion of cytokinesis and increased viability in response to minor damage to the cell division apparatus. Several viable mutants partially defective in the cell division apparatus depend on Clp1p for their viability.…”

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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%

mentioning

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, this phosphomutant cannot induce the assembly of full contractile rings [Roberts-Galbraith et al, 2010]. Another interesting point is that Cdc15 dephosphorylation is partly dependent on the phosphatase Clp1, a known effector of the SIN pathway [Cueille et al, 2001;Trautmann et al, 2001;Chen et al, 2008]. Clp1 localization at the contractile ring depends on Mid1 (see Fig.…”

Section: Mechanisms Of Contractile Ring Assemblymentioning

confidence: 99%

Mid1/anillin and the spatial regulation of cytokinesis in fission yeast

Rincón

Paoletti

2012

Cytoskeleton

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Cell division is a critical and irreversible step in the cell cycle. The strategies that cells follow to regulate the position of the division plane must take into account the global geometry of the cell as well as position of the genetic material to ensure its accurate segregation into daughter cells of a given cell shape and size. Along the years, research on Schizosaccharomyces pombe, a wellrecognized model organism for cell division studies has allowed a detailed molecular understanding of the spatial mechanisms regulating cytokinesis. Division plane position in this unicellular rod-shaped organism, which divides by the assembly and constriction of a medially placed actomyosin ring, largely depends on the anillinlike protein Mid1. Therefore, the major pathways controlling the position of the division plane converge on Mid1. In this review, we make an overview of the studies that have deciphered how Mid1 localization and scaffolding activities are controlled over the cell cycle to ensure the symmetrical division of fission yeast cells. These studies have revealed new mechanisms generating spatial information based on nuclear shuttling of the division plane factor Mid1 and on the establishment of cortical inhibitory gradients of the cell polarity kinase Pom1. V C 2012 Wiley Periodicals, Inc Key Words: cytokinesis, fission yeast, contractile ring, Mid1, cell division Introduction C ytokinesis is the final step of cell division that physically separates the daughter cells at the end of the cell cycle. It is a universal process, essential for cell proliferation, for the survival of unicellular organisms or for the development of multicellular organisms, whose major features have been well conserved along evolution. As an irreversible event, cytokinesis is under tight spatial and temporal regulation. Defective cytokinesis can indeed alter cell geometry or size, perturb cellular organization within tissues or prevent the accurate transmission of the genetic material, producing aneuploid cells, which can affect the survival of unicellular species or favor cancer and tumor progression in animal species.Cytokinesis is first strictly coordinated with mitotic progression in order to successfully fulfill chromosome segregation. Checkpoint mechanisms monitoring the function of the mitotic apparatus can halt cells in metaphase, which prevents cytokinesis until actual chromosome segregation in anaphase.Second, spatial regulatory pathways define the position of the division plane according to the position of the nucleus at mitotic entry, or of the mitotic apparatus, perpendicular to the axis of chromosome segregation. This ensures the efficient segregation of the genetic material and allows to control the geometry of the daughter cells in response to morphogenetic programs. Cell division can indeed be symmetric or asymmetric to allow the generation of daughter cells of different sizes. Orientation of the division plane is also modulated to properly position the daughter cells inside embryos or tissues and to permit the asymm...

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“…elegans and Homo sapiens on the basis of sequence similarity to the budding yeast Saccharomyces cerevisiae protein (Li et al, 1997;Cueille et al, 2001;Trautmann et al, 2001;Gruneberg et al, 2002). (All) Cdc14 proteins characterised to date are dual-specificity protein phosphatases that share a core of approximately 300 amino acids towards the amino terminus that includes a strictly conserved protein-phosphatase domain motif (Gray et al, 2003).…”

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confidence: 99%

A role for the Cdc14-family phosphatase Flp1p at the end of the cell cycle in controlling the rapid degradation of the mitotic inducer Cdc25p in fission yeast

Esteban

Blanco

Cueille³

et al. 2004

Journal of Cell Science

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The Schizosaccaromyces pombe protein Flp1p belongs to a conserved family of serine-threonine-phosphatases. The founding member of this family, Saccharomyces cerevisiae Cdc14p, is required for inactivation of mitotic CDKs and reversal of CDK mediated phosphorylation at the end of mitosis, thereby bringing about the M-G1 transition. Initial studies of Flp1p suggest that it may play a different role to Cdc14p. Here we show that Flp1p is required for rapid degradation of the mitotic inducer Cdc25p at the end of mitosis, and that Cdc25p is a substrate of Flp1p in vitro. Down-regulation of Cdc25p activity by Flp1p may ensure a prompt inactivation of mitotic CDK complexes to trigger cell division. Our results suggest a regulatory mechanism, and a universal role, for Cdc14p like proteins in coordination of cytokinesis with other cell cycle events.

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Fission yeast Clp1p phosphatase regulates G2/M transition and coordination of cytokinesis with cell cycle progression

Cited by 186 publications

References 33 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

Mid1/anillin and the spatial regulation of cytokinesis in fission yeast

A role for the Cdc14-family phosphatase Flp1p at the end of the cell cycle in controlling the rapid degradation of the mitotic inducer Cdc25p in fission yeast

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