Faculty Opinions recommendation of Mitotic exit network controls the localization of Cdc14 to the spindle pole body in Saccharomyces cerevisiae.

ABSTRACTMeiosis in the budding yeast Saccharomyces cerevisiae is used to create haploid yeast spores from a diploid mother cell. During meiosis II, cytokinesis occurs by closure of the prospore membrane, a membrane that initiates at the spindle pole body and grows to surround each of the haploid meiotic products. Timely prospore membrane closure requires SPS1, which encodes a STE20-family GCKIII kinase. To identify genes that may activate SPS1, we utilized a histone phosphorylation defect of sps1 mutants to screen for genes with a similar phenotype and found that cdc15 shared this phenotype. CDC15 encodes a Hippo-like kinase that is part of the mitotic exit network. We find that Sps1 complexes with Cdc15, that Sps1 phosphorylation requires Cdc15, and that CDC15 is also required for timely prospore membrane closure. We also find that SPS1, like CDC15, is required for meiosis II spindle disassembly and sustained anaphase II release of Cdc14 in meiosis. However, the NDR-kinase complex encoded by DBF2/DBF20 MOB1 which functions downstream of CDC15 in mitotic cells, does not appear to play a role in spindle disassembly, timely prospore membrane closure, or sustained anaphase II Cdc14 release. Taken together, our results suggest that the mitotic exit network is rewired for exit from meiosis II, such that SPS1 replaces the NDR-kinase complex downstream of CDC15.

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A Noncanonical Hippo Pathway Regulates Spindle Disassembly and Cytokinesis During Meiosis in Saccharomyces cerevisiae

Genetics ◽

10.1534/genetics.120.303584 ◽

2020 ◽

Vol 216 (2) ◽

pp. 447-462

Author(s):

Scott M. Paulissen ◽

Cindy A. Hunt ◽

Brian C. Seitz ◽

Christian J. Slubowski ◽

Yao Yu ◽

...

Keyword(s):

Saccharomyces Cerevisiae ◽

Hippo Pathway ◽

Spindle Pole Body ◽

Spindle Pole ◽

Mitotic Exit ◽

Link Type ◽

Prospore Membrane ◽

Mitotic Exit Network ◽

Spindle Disassembly ◽

Ndr Kinase

Meiosis in the budding yeast Saccharomyces cerevisiae is used to create haploid yeast spores from a diploid mother cell. During meiosis II, cytokinesis occurs by closure of the prospore membrane, a membrane that initiates at the spindle pole body and grows to surround each of the haploid meiotic products. Timely prospore membrane closure requires SPS1, which encodes an STE20 family GCKIII kinase. To identify genes that may activate SPS1, we utilized a histone phosphorylation defect of sps1 mutants to screen for genes with a similar phenotype and found that cdc15 shared this phenotype. CDC15 encodes a Hippo-like kinase that is part of the mitotic exit network. We find that Sps1 complexes with Cdc15, that Sps1 phosphorylation requires Cdc15, and that CDC15 is also required for timely prospore membrane closure. We also find that SPS1, like CDC15, is required for meiosis II spindle disassembly and sustained anaphase II release of Cdc14 in meiosis. However, the NDR-kinase complex encoded by DBF2/DBF20MOB1 which functions downstream of CDC15 in mitotic cells, does not appear to play a role in spindle disassembly, timely prospore membrane closure, or sustained anaphase II Cdc14 release. Taken together, our results suggest that the mitotic exit network is rewired for exit from meiosis II, such that SPS1 replaces the NDR-kinase complex downstream of CDC15.

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Inactivation of Mitotic Kinase Triggers Translocation of MEN Components to Mother-Daughter Neck in Yeast

Molecular Biology of the Cell ◽

10.1091/mbc.e03-04-0238 ◽

2003 ◽

Vol 14 (11) ◽

pp. 4734-4743 ◽

Cited By ~ 31

Author(s):

Hong Hwa Lim ◽

Foong May Yeong ◽

Uttam Surana

Keyword(s):

Chromosome Segregation ◽

Spindle Pole Body ◽

Spindle Pole ◽

Mitotic Exit ◽

Mitotic Kinase ◽

Division Site ◽

Pole Body ◽

Spindle Pole Bodies ◽

Mitotic Exit Network ◽

Mutant Cells

Chromosome segregation, mitotic exit, and cytokinesis are executed in this order during mitosis. Although a scheme coordinating sister chromatid separation and initiation of mitotic exit has been proposed, the mechanism that temporally links the onset of cytokinesis to mitotic exit is not known. Exit from mitosis is regulated by the mitotic exit network (MEN), which includes a GTPase (Tem1) and various kinases (Cdc15, Cdc5, Dbf2, and Dbf20). Here, we show that Dbf2 and Dbf20 functions are necessary for the execution of cytokinesis. Relocalization of these proteins from spindle pole bodies to mother daughter neck seems to be necessary for this role because cdc15-2 mutant cells, though capable of exiting mitosis at semipermissive temperature, are unable to localize Dbf2 (and Dbf20) to the “neck” and fail to undergo cytokinesis. These cells can assemble and constrict the actomyosin ring normally but are incapable of forming a septum, suggesting that MEN components are critical for the initiation of septum formation. Interestingly, the spindle pole body to neck translocation of Dbf2 and Dbf20 is triggered by the inactivation of mitotic kinase. The requirement of kinase inactivation for translocation of MEN components to the division site thus provides a mechanism that renders mitotic exit a prerequisite for cytokinesis.

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Mutual regulation of cyclin-dependent kinase and the mitotic exit network

The Journal of Cell Biology ◽

10.1083/jcb.200911128 ◽

2010 ◽

Vol 188 (3) ◽

pp. 351-368 ◽

Cited By ~ 52

Author(s):

Cornelia König ◽

Hiromi Maekawa ◽

Elmar Schiebel

Keyword(s):

Spindle Pole Body ◽

Spindle Pole ◽

Mitotic Exit ◽

Cyclin Dependent Kinase ◽

Spatial Regulation ◽

Daughter Cells ◽

Pole Body ◽

Mitotic Exit Network ◽

Mutual Regulation ◽

Early Anaphase

The mitotic exit network (MEN) is a spindle pole body (SPB)–associated, GTPase-driven signaling cascade that controls mitotic exit. The inhibitory Bfa1–Bub2 GTPase-activating protein (GAP) only associates with the daughter SPB (dSPB), raising the question as to how the MEN is regulated on the mother SPB (mSPB). Here, we show mutual regulation of cyclin-dependent kinase 1 (Cdk1) and the MEN. In early anaphase Cdk1 becomes recruited to the mSPB depending on the activity of the MEN kinase Cdc15. Conversely, Cdk1 negatively regulates binding of Cdc15 to the mSPB. In addition, Cdk1 phosphorylates the Mob1 protein to inhibit the activity of Dbf2–Mob1 kinase that regulates Cdc14 phosphatase. Our data revise the understanding of the spatial regulation of the MEN. Although MEN activity in the daughter cells is controlled by Bfa1–Bub2, Cdk1 inhibits MEN activity at the mSPB. Consistent with this model, only triple mutants that lack BUB2 and the Cdk1 phosphorylation sites in Mob1 and Cdc15 show mitotic exit defects.

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Regulation of the Bfa1p–Bub2p complex at spindle pole bodies by the cell cycle phosphatase Cdc14p

The Journal of Cell Biology ◽

10.1083/jcb.200112085 ◽

2002 ◽

Vol 157 (3) ◽

pp. 367-379 ◽

Cited By ~ 81

Author(s):

Gislene Pereira ◽

Claire Manson ◽

Joan Grindlay ◽

Elmar Schiebel

Keyword(s):

Spindle Pole Body ◽

Spindle Pole ◽

Mitotic Exit ◽

Gtpase Activating Protein ◽

Signal Transduction Cascade ◽

Pole Body ◽

Spindle Pole Bodies ◽

Short Period ◽

Mitotic Exit Network ◽

Early Anaphase

The budding yeast mitotic exit network (MEN) is a GTPase-driven signal transduction cascade that controls the release of the phosphatase Cdc14p from the nucleolus in anaphase and thereby drives mitotic exit. We show that Cdc14p is partially released from the nucleolus in early anaphase independent of the action of the MEN components Cdc15p, Dbf2p, and Tem1p. Upon release, Cdc14p binds to the spindle pole body (SPB) via association with the Bfa1p–Bub2p GTPase activating protein complex, which is known to regulate the activity of the G protein Tem1p. Cdc14p also interacts with this GTPase. The association of the MEN component Mob1p with the SPB acts as a marker of MEN activation. The simultaneous binding of Cdc14p and Mob1p to the SPB in early anaphase suggests that Cdc14p initially activates the MEN. In a second, later step, which coincides with mitotic exit, Cdc14p reactivates the Bfa1p–Bub2p complex by dephosphorylating Bfa1p. This inactivates the MEN and displaces Mob1p from SPBs. These data indicate that Cdc14p activates the MEN in early anaphase but later inactivates it through Bfa1p dephosphorylation and so restricts MEN activity to a short period in anaphase.

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The Mitotic Exit Network Regulates Spindle Pole Body Selection During Sporulation ofSaccharomyces cerevisiae

Genetics ◽

10.1534/genetics.116.194522 ◽

2017 ◽

Vol 206 (2) ◽

pp. 919-937 ◽

Cited By ~ 10

Author(s):

Christian Renicke ◽

Ann-Katrin Allmann ◽

Anne Pia Lutz ◽

Thomas Heimerl ◽

Christof Taxis

Keyword(s):

Spindle Pole Body ◽

Spindle Pole ◽

Mitotic Exit ◽

Pole Body ◽

Mitotic Exit Network

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Spindle pole bodies function as signal amplifiers in the Mitotic Exit Network

Molecular Biology of the Cell ◽

10.1091/mbc.e19-10-0584 ◽

2020 ◽

Vol 31 (9) ◽

pp. 906-916 ◽

Cited By ~ 1

Author(s):

Ian W. Campbell ◽

Xiaoxue Zhou ◽

Angelika Amon

Keyword(s):

Signal Transduction ◽

Daughter Cell ◽

Spindle Pole Body ◽

Spindle Pole ◽

Mitotic Exit ◽

Signal Transduction Cascade ◽

Pole Body ◽

Spindle Pole Bodies ◽

Mitotic Exit Network ◽

Kinase Cascade

The signal transduction cascade, known as the mitotic exit network (MEN), detects nuclear position by scaffolding its GTPase onto the spindle pole body that moves into the daughter cell during anaphase. Propagating the MEN kinase cascade onto two spindle pole bodies amplifies MEN signaling, resulting in a timely exit from mitosis.

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Mutations affecting spindle pole body and mitotic exit network function are synthetically lethal with a deletion of the nucleoporin NUP1 in S. cerevisiae

Current Genetics ◽

10.1007/s00294-007-0168-4 ◽

2007 ◽

Vol 53 (2) ◽

pp. 95-105 ◽

Cited By ~ 4

Author(s):

Nicola C. Harper ◽

Nicole T. Al-Greene ◽

Munira A. Basrai ◽

Kenneth D. Belanger

Keyword(s):

Spindle Pole Body ◽

Spindle Pole ◽

Mitotic Exit ◽

Network Function ◽

Pole Body ◽

Mitotic Exit Network ◽

Synthetically Lethal

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Ady3p Links Spindle Pole Body Function to Spore Wall Synthesis in Saccharomyces cerevisiae

Genetics ◽

10.1093/genetics/160.4.1439 ◽

2002 ◽

Vol 160 (4) ◽

pp. 1439-1450

Author(s):

Mark E Nickas ◽

Aaron M Neiman

Keyword(s):

Saccharomyces Cerevisiae ◽

De Novo ◽

Spindle Pole Body ◽

Leading Edge ◽

Spindle Pole ◽

Spore Wall ◽

Pole Body ◽

Prospore Membrane ◽

Sporulation Efficiency ◽

Spore Walls

Abstract Spore formation in Saccharomyces cerevisiae requires the de novo synthesis of prospore membranes and spore walls. Ady3p has been identified as an interaction partner for Mpc70p/Spo21p, a meiosis-specific component of the outer plaque of the spindle pole body (SPB) that is required for prospore membrane formation, and for Don1p, which forms a ring-like structure at the leading edge of the prospore membrane during meiosis II. ADY3 expression has been shown to be induced in midsporulation. We report here that Ady3p interacts with additional components of the outer and central plaques of the SPB in the two-hybrid assay. Cells that lack ADY3 display a decrease in sporulation efficiency, and most ady3Δ/ady3Δ asci that do form contain fewer than four spores. The sporulation defect in ady3Δ/ady3Δ cells is due to a failure to synthesize spore wall polymers. Ady3p forms ring-like structures around meiosis II spindles that colocalize with those formed by Don1p, and Don1p rings are absent during meiosis II in ady3Δ/ady3Δ cells. In mpc70Δ/mpc70Δ cells, Ady3p remains associated with SPBs during meiosis II. Our results suggest that Ady3p mediates assembly of the Don1p-containing structure at the leading edge of the prospore membrane via interaction with components of the SPB and that this structure is involved in spore wall formation.

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