The Schizosaccharomyces pombe septation initiation network (SIN) is required for spore formation in meiosis

Krapp, Andrea; Collin, Philippe; Cokoja, Adisa; Dischinger, Sandra; Cano, Elena

doi:10.1242/jcs.03025

Cited by 36 publications

(54 citation statements)

References 46 publications

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“…Thus, Mug27 is expressed during the nuclear divisions of meiosis alone and also localizes at the SPB. Sid4 is the most upstream component of the SIN, which regulates spore formation (Krapp et al, 2006). Like other SIN proteins, Sid4 does not exhibit the characteristic crescent shape that many SPB antigens adopt during the late stages of meiosis when the outer spindle plaque is remodeled to promote spore formation (Krapp et al, 2006) (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…myosin ring, and in meiosis, when they regulate spore formation (reviewed by Wolfe and Gould, 2005;Krapp et al, 2004;Krapp et al, 2006). The core components of the SIN are three protein kinases (Cdc7, Sid1 and Sid2) and their associated regulatory and/or targeting subunits (Spg1, Cdc14 and Mob1), which assemble at the SPB on a scaffold composed of Sid4 and Cdc11.…”

Section: Introductionmentioning

confidence: 99%

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Mug27 is a meiosis-specific protein kinase that functions in fission yeast meiosis II and sporulation

Ohtaka

Okuzaki

Nishimura

2008

Journal of Cell Science

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Several meiosis-specific proteins of Schizosaccharomyces pombe play essential roles in meiotic progression. We report here that a novel meiosis-specific protein kinase, Mug27 (also known as Ppk35), is required for proper spore formation. This kinase is expressed by the mug27+ gene, which is abruptly transcribed after horsetail movement. This transcription is maintained until the second meiotic division. Green fluorescent protein (GFP)-tagged Mug27 appears at the start of prometaphase I, localizes to the spindle pole body (SPB) and then translocates to the forespore membrane (FSM) at late anaphase II. In the mug27Δ strain, smaller spores are produced compared with those of the mug27+ strain. Moreover, spore viability was reduced by half or more compared with that of the mug27+ strain. The protein-kinase activity of Mug27 appears to be important for its function: the putative kinase-dead Mug27 mutant had similar phenotypes to mug27Δ. Our results here indicate that the Mug27 kinase localizes at the SPB and regulates FSM formation and sporulation.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Mug27 is a meiosis-specific protein kinase that functions in fission yeast meiosis II and sporulation

Ohtaka

Okuzaki

Nishimura

2008

Journal of Cell Science

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“…The SIN has recently been shown to be required for sporulation in S. pombe (Krapp et al 2006). Interestingly, mutants lacking SIN function proceed through meiosis with normal kinetics but display abnormal forespore membranes, the S. pombe equivalent of the PSM, which fail to package nuclei and form mature spores.…”

Section: Discussionmentioning

confidence: 99%

Cdc15 Is Required for Spore Morphogenesis Independently of Cdc14 in Saccharomyces cerevisiae

et al. 2007

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In Saccharomyces cerevisiae exit from mitosis requires the Cdc14 phosphatase to reverse CDK-mediated phosphorylation. Cdc14 is released from the nucleolus by the Cdc14 early anaphase release (FEAR) and mitotic exit network (MEN) pathways. In meiosis, the FEAR pathway is essential for exit from anaphase I. The MEN component Cdc15 is required for the formation of mature spores. To analyze the role of Cdc15 during sporulation, a conditional mutant in which CDC15 expression was controlled by the CLB2 promoter was used. Cdc15-depleted cells proceeded normally through the meiotic divisions but were unable to properly disassemble meiosis II spindles. The morphology of the prospore membrane was aberrant and failed to capture the nuclear lobes. Cdc15 was not required for Cdc14 release from the nucleoli, but it was essential to maintain Cdc14 released and for its nucleo-cytoplasmic transport. However, cells carrying a CDC14 allele with defects in nuclear export (Cdc14-DNES) were able to disassemble the spindle and to complete spore formation, suggesting that the Cdc14 nuclear export defect was not the cause of the phenotypes observed in cdc15 mutants. MEIOSIS is a specialized cell division that produces the haploid cells needed for sexual reproduction, and the completion of meiosis is normally coupled to differentiation programs that produce gametes. In Saccharomyces cerevisiae, sporulation is initiated when diploid cells are grown in the absence of nitrogen and the presence of a nonfermentable carbon source such as acetate (Esposito and Klapholtz 1981). When triggered to enter the sporulation program, cells exit the mitotic cycle from the G1 phase. This is followed by one round of S phase and two meiotic divisions that generate four haploid nuclei, which are packaged into individual spores. As a consequence of this process, four haploid gametes (spores) are formed in the cytoplasm of the mother cell (ascus) (reviewed by Neiman 2005). At the onset of meiosis II, the spindle pole body (SPB) is modified by the incorporation of several meiosis-specific proteins, which together make up the meiosis II outer plaque (Knop and Strasser 2000;Bajgier et al. 2001;Nickas et al. 2003). This change in composition converts the function of the cytoplasmic face of the SPB from microtubule nucleation to membrane nucleation. The process of spore construction requires the de novo assembly of two cellular structures, the prospore membrane (PSM) that is generated around the daughter nuclei to create prospores and a protective spore wall that surrounds the prospores. Once the meiosis II outer plaque of the SPB has been assembled, it becomes a site for the docking and coalescence of secretory vesicles to form flattened double-membrane sheets termed PSMs (Moens 1971;Neiman 1998). These nascent PSMs expand during meiosis II, and at the time of nuclear division each PSM completely engulfs the nuclear lobe to which it is anchored via the SPB. At the completion of meiosis II, each PSM fuses with itself so that each daughter nucleus (and assoc...

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“…It is tightly regulated through the mitotic cell cycle to assure proper coordination of mitosis and cytokinesis, and during meiosis, where it is essential for spore formation (Krapp et al 2006). Signaling requires the activity of three protein kinases, each of which has a regulatory subunit (kinase regulator); Cdc7p-Spg1p (Fankhauser and Simanis 1994;Schmidt et al 1997;Mehta and Gould 2006), Sid1p-Cdc14p (Fankhauser and Simanis 1993;Guertin et al 2000;Guertin and McCollum 2001), and Sid2p-Mob1p (Sparks et al 1999;Hou et al 2000;Salimova et al 2000).…”

Section: Septation Initiation Networkmentioning

confidence: 99%

“…To analyze F-actin patches, the crn1-GFP allele (Pelham and Chang 2001) was crossed into the strains of interest; exponentially growing cultures were fixed by addition of paraformaldehyde to 3.7% (w/v from 37% w/v solution). GFP-atb2, expressed from the atb2 promoter and integrated at leu1 (Krapp et al 2006), was crossed into the strains and living cells were imaged using a Plan-S-Apo 60· N.A. 1.42 objective lens mounted on a Perkin-Elmer spinning disk confocal microscope.…”

Section: Microscopymentioning

confidence: 99%

Characterization of ypa1 and ypa2, the Schizosaccharomyces pombe Orthologs of the Peptidyl Proyl Isomerases That Activate PP2A, Reveals a Role for Ypa2p in the Regulation of Cytokinesis

Goyal

2012

Genetics

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The Schizosaccharomyces pombe septation initiation network (SIN) regulates cytokinesis. Cdc7p is the first kinase in the core SIN; we have screened genetically for SIN regulators by isolating cold-sensitive suppressors of cdc7-24. Our screen yielded a mutant in SPAC1782.05, one of the two fission yeast orthologs of mammalian phosphotyrosyl phosphatase activator. We have characterized this gene and its ortholog SPAC4F10.04, which we have named ypa2 and ypa1, respectively. We find that Ypa2p is the major form of protein phosphatase type 2A activator in S. pombe. A double ypa1-D ypa2-D null mutant is inviable, indicating that the two gene products have at least one essential overlapping function. Individually, the ypa1 and ypa2 genes are essential for survival only at low temperatures. The ypa2-D mutant divides at a reduced cell size and displays aberrant cell morphology and cytokinesis. Genetic analysis implicates Ypa2p as an inhibitor of the septation initiation network. We also isolated a cold-sensitive allele of ppa2, the major protein phosphatase type 2A catalytic subunit, implicating this enzyme as a regulator of the septation initiation network. SCHIZOSACCHAROMYCES pombe cells take the form of a cylinder capped by hemispherical ends. During interphase, cells grow mainly at their tips. Cell elongation ceases after mitotic commitment, and the cytoskeleton is reorganized in preparation for nuclear and cell division (reviewed by McCully and Robinow 1971;Mitchison and Nurse 1985;Marks et al. 1986;Hagan and Hyams 1988;Hagan 1998). The cell divides by fission after forming a septum in the middle of the cell. The site of division is defined at the onset of mitosis (Daga and Chang 2005), by the formation of an actomyosin contractile ring (CAR), whose assembly continues throughout mitosis (Wu et al. 2003;Pollard 2008;Pollard and Wu 2010). At the end of anaphase, the CAR is thought to guide synthesis of the multilayered division septum (reviewed by (Ishiguro 1998;Sipiczki 2007). Septation Initiation NetworkThe S. pombe septation initiation network (SIN) is a network of protein kinases that is essential for cytokinesis in the mitotic cycle; reviewed by (Gould and Simanis 1997;Simanis 2003;Wolfe and Gould 2005;Goyal et al. 2011). It is tightly regulated through the mitotic cell cycle to assure proper coordination of mitosis and cytokinesis, and during meiosis, where it is essential for spore formation (Krapp et al. 2006). Signaling requires the activity of three protein kinases, each of which has a regulatory subunit (kinase regulator); Cdc7p-Spg1p (Fankhauser and Simanis 1994;Schmidt et al. 1997;Mehta and Gould 2006), Sid1p-Cdc14p (Fankhauser and Simanis 1993;Guertin et al. 2000;Guertin and McCollum 2001), and Sid2p-Mob1p (Sparks et al. 1999;Hou et al. 2000;Salimova et al. 2000). SIN signaling is modulated by the nucleotide status of the GTPase Spg1p (Schmidt et al. 1997;Sohrmann et al. 1998), which is determined by the balance of spontaneous nucleotide exchange, a putative GEF, Etd1p Garcia-Cortes and McCollu...

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The Schizosaccharomyces pombe septation initiation network (SIN) is required for spore formation in meiosis

Cited by 36 publications

References 46 publications

Mug27 is a meiosis-specific protein kinase that functions in fission yeast meiosis II and sporulation

Mug27 is a meiosis-specific protein kinase that functions in fission yeast meiosis II and sporulation

Cdc15 Is Required for Spore Morphogenesis Independently of Cdc14 in Saccharomyces cerevisiae

Characterization of ypa1 and ypa2, the Schizosaccharomyces pombe Orthologs of the Peptidyl Proyl Isomerases That Activate PP2A, Reveals a Role for Ypa2p in the Regulation of Cytokinesis

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