Roles of the fission yeast UNC-13/Munc13 protein Ync13 in late stages of cytokinesis

Cytokinesis is a complicated yet conserved step of the cell-division cycle that requires the coordination of multiple proteins and cellular processes. Here we describe a previously uncharacterized protein, Ync13, and its roles during fission yeast cytokinesis. Ync13 is a member of the UNC-13/Munc13 protein family, whose animal homologues are essential priming factors for soluble N-ethylmaleimide-sensitive factor attachment protein receptor complex assembly during exocytosis in various cell types, but no roles in cytokinesis have been reported. We find that Ync13 binds to lipids in vitro and dynamically localizes to the plasma membrane at cell tips during interphase and at the division site during cytokinesis. Deletion of Ync13 leads to defective septation and exocytosis, uneven distribution of cell-wall enzymes and components of cell-wall integrity pathway along the division site and massive cell lysis during cell separation. Interestingly, loss of Ync13 compromises endocytic site selection at the division plane. Collectively, we find that Ync13 has a novel function as an UNC-13/Munc13 protein in coordinating exocytosis, endocytosis, and cell-wall integrity during fission yeast cytokinesis.

[1]  O. Ohara,et al.  Characterization of a large UNC13D gene duplication in a patient with familial hemophagocytic lymphohistiocytosis type 3. , 2018, Clinical immunology.

[2]  X. Lou.  Sensing Exocytosis and Triggering Endocytosis at Synapses: Synaptic Vesicle Exocytosis–Endocytosis Coupling , 2018, Front. Cell. Neurosci..

[3]  T. Maritzen,et al.  Coupling of exocytosis and endocytosis at the presynaptic active zone , 2017, Neuroscience Research.

[4]  A. Burns,et al.  Munc13 proteins control regulated exocytosis in mast cells , 2017, The Journal of Biological Chemistry.

[5]  J. Rizo,et al.  Simultaneous lipid and content mixing assays for in vitro reconstitution studies of synaptic vesicle fusion , 2017, Nature Protocols.

[6]  R. Pfuetzner,et al.  Molecular Mechanisms of Synaptic Vesicle Priming by Munc13 and Munc18 , 2017, Neuron.

[7]  T. Südhof,et al.  ELKS1 localizes the synaptic vesicle priming protein bMunc13-2 to a specific subset of active zones , 2017, The Journal of cell biology.

[8]  J. Long,et al.  Molecular Mechanisms for the Coupling of Endocytosis to Exocytosis in Neurons , 2017, Front. Mol. Neurosci..

[9]  D. Drubin,et al.  Selection and stabilization of endocytic sites by Ede1, a yeast functional homologue of human Eps15 , 2017, Molecular biology of the cell.

[10]  J. Rizo,et al.  Mechanistic insights into neurotransmitter release and presynaptic plasticity from the crystal structure of Munc13-1 C1C2BMUN , 2017, eLife.

[11]  A. Brunger,et al.  Conformational change of syntaxin linker region induced by Munc13s initiates SNARE complex formation in synaptic exocytosis , 2017, The EMBO journal.

[12]  P. Pérez,et al.  Overview of fission yeast septation , 2016, Cellular microbiology.

[13]  Jian-Qiu Wu,et al.  Roles of the novel coiled-coil protein Rng10 in septum formation during fission yeast cytokinesis , 2016, Molecular Biology of the Cell.

[14]  Jesper Johansen,et al.  Polarized Exocytosis Induces Compensatory Endocytosis by Sec4p-Regulated Cortical Actin Polymerization , 2016, PLoS biology.

[15]  J. Rizo,et al.  Functional synergy between the Munc13 C-terminal C1 and C2 domains , 2016, eLife.

[16]  M. Osumi,et al.  Fission yeast septation , 2016, Communicative & integrative biology.

[17]  Sergio A. Rincon,et al.  Molecular control of fission yeast cytokinesis. , 2016, Seminars in cell & developmental biology.

[18]  Jian-Qiu Wu,et al.  Roles of the TRAPP-II Complex and the Exocyst in Membrane Deposition during Fission Yeast Cytokinesis , 2016, PLoS biology.

[19]  L. Hellman,et al.  Role of Munc13-4 as a Ca2+-dependent tether during platelet secretion. , 2016, The Biochemical journal.

[20]  Franz Meitinger,et al.  Actomyosin ring driven cytokinesis in budding yeast , 2016, Seminars in cell & developmental biology.

[21]  Jinzhong Zhang,et al.  Munc13-4 interacts with syntaxin 7 and regulates late endosomal maturation, endosomal signaling, and TLR9-initiated cellular responses , 2016, Molecular biology of the cell.

[22]  K. Gould,et al.  Oligomerization but Not Membrane Bending Underlies the Function of Certain F-BAR Proteins in Cell Motility and Cytokinesis. , 2015, Developmental cell.

[23]  Jinzhong Zhang,et al.  Munc13-4 Is a Rab11-binding Protein That Regulates Rab11-positive Vesicle Trafficking and Docking at the Plasma Membrane* , 2015, The Journal of Biological Chemistry.

[24]  Timothy E. Vanderleest,et al.  Exocyst-Dependent Membrane Addition Is Required for Anaphase Cell Elongation and Cytokinesis in Drosophila , 2015, PLoS genetics.

[25]  Junjie Xu,et al.  The Synaptic Vesicle Release Machinery. , 2015, Annual review of biophysics.

[26]  T. Martin.  PI(4,5)P₂-binding effector proteins for vesicle exocytosis. , 2015, Biochimica et biophysica acta.

[27]  J. Rizo,et al.  Syntaxin opening by the MUN domain underlies the function of Munc13 in synaptic-vesicle priming , 2015, Nature Structural &Molecular Biology.

[28]  Jian-Qiu Wu,et al.  Mechanistic insights into the anchorage of the contractile ring by anillin and Mid1. , 2015, Developmental cell.

[29]  M. Petronczki,et al.  Cytokinesis in animal cells. , 2015, Cold Spring Harbor perspectives in biology.

[30]  Yuejie Chi,et al.  3D multifocus astigmatism and compressed sensing (3D MACS) based superresolution reconstruction. , 2015, Biomedical optics express.

[31]  Jian-Qiu Wu,et al.  Regulation of Rho-GEF Rgf3 by the arrestin Art1 in fission yeast cytokinesis , 2015, Molecular biology of the cell.

[32]  Beverly Wendland,et al.  Actin and Endocytosis in Budding Yeast , 2015, Genetics.

[33]  E. Dere,et al.  Fast Cerebellar Reflex Circuitry Requires Synaptic Vesicle Priming by Munc13-3 , 2015, The Cerebellum.

[34]  K. Gould,et al.  The Cdc15 and Imp2 SH3 domains cooperatively scaffold a network of proteins that redundantly ensure efficient cell division in fission yeast , 2015, Molecular biology of the cell.

[35]  Jian-Qiu Wu,et al.  The Rho-GEF Gef3 interacts with the septin complex and activates the GTPase Rho4 during fission yeast cytokinesis , 2015, Molecular biology of the cell.

[36]  S. Bär,et al.  Membrane Trafficking in the Yeast Saccharomyces cerevisiae Model , 2015, International journal of molecular sciences.

[37]  Minoru Yoshida,et al.  Balance between exocytosis and endocytosis determines the efficacy of sterol-targeting antibiotics. , 2014, Chemistry & biology.

[38]  R. Martín-García,et al.  F-BAR domain protein Rga7 collaborates with Cdc15 and Imp2 to ensure proper cytokinesis in fission yeast , 2014, Journal of Cell Science.

[39]  J. Bähler,et al.  Regulation of spindle pole body assembly and cytokinesis by the centrin-binding protein Sfi1 in fission yeast , 2014, Molecular biology of the cell.

[40]  T. Pollard,et al.  Contractile ring stability in S. pombe depends on F-BAR protein Cdc15p and Bgs1p transport from the Golgi complex. , 2014, Cell reports.

[41]  A. Sinz,et al.  Structural insights into calmodulin/Munc13 interaction , 2014, Biological chemistry.

[42]  Valerie C. Coffman,et al.  Every laboratory with a fluorescence microscope should consider counting molecules , 2014, Molecular biology of the cell.

[43]  Sophie G. Martin,et al.  The novel proteins Rng8 and Rng9 regulate the myosin-V Myo51 during fission yeast cytokinesis , 2014, The Journal of cell biology.

[44]  Hsueh-Cheng Chiang,et al.  Exocytosis and endocytosis: modes, functions, and coupling mechanisms. , 2014, Annual review of physiology.

[45]  M. Geli,et al.  Zooming in on the molecular mechanisms of endocytic budding by time-resolved electron microscopy , 2014, Cellular and Molecular Life Sciences.

[46]  P. Pérez,et al.  Rho1 GTPase and PKC Ortholog Pck1 Are Upstream Activators of the Cell Integrity MAPK Pathway in Fission Yeast , 2014, PloS one.

[47]  T. Martin,et al.  CAPS and Munc13: CATCHRs that SNARE Vesicles , 2013, Front. Endocrinol..

[48]  G. Gould,et al.  Exocyst proteins in cytokinesis , 2013, Communicative & integrative biology.

[49]  Jian-Qiu Wu,et al.  Cooperation between Rho-GEF Gef2 and its binding partner Nod1 in the regulation of fission yeast cytokinesis , 2013, Molecular biology of the cell.

[50]  Valerie C. Coffman,et al.  The formins Cdc12 and For3 cooperate during contractile ring assembly in cytokinesis , 2013, The Journal of cell biology.

[51]  Yishi Jin,et al.  Position of UNC-13 in the active zone regulates synaptic vesicle release probability and release kinetics , 2013, eLife.

[52]  P. Pérez,et al.  Negative Functional Interaction Between Cell Integrity MAPK Pathway and Rho1 GTPase in Fission Yeast , 2013, Genetics.

[53]  M. R. Sharifmoghadam,et al.  Regulation of Cell Wall Synthesis by the Clathrin Light Chain Is Essential for Viability in Schizosaccharomyces pombe , 2013, PloS one.

[54]  J. Kaplan,et al.  UNC-13L, UNC-13S, and Tomosyn form a protein code for fast and slow neurotransmitter release in Caenorhabditis elegans , 2013, eLife.

[55]  C. Shimoda,et al.  The Fission Yeast Synaptobrevin Ortholog Syb1 Plays an Important Role in Forespore Membrane Formation and Spore Maturation , 2013, Eukaryotic Cell.

[56]  P. Lipp,et al.  Different Munc13 Isoforms Function as Priming Factors in Lytic Granule Release from Murine Cytotoxic T Lymphocytes , 2013, Traffic.

[57]  V. Wood,et al.  A genome-wide resource of cell cycle and cell shape genes of fission yeast , 2013, Open Biology.

[58]  S. Roßner,et al.  Munc13 genotype regulates secretory amyloid precursor protein processing via postsynaptic glutamate receptors , 2013, International Journal of Developmental Neuroscience.

[59]  Qing Nie,et al.  Signaling regulated endocytosis and exocytosis lead to mating pheromone concentration dependent morphologies in yeast , 2012, FEBS letters.

[60]  A. Echard.  Phosphoinositides and cytokinesis: The “PIP” of the iceberg , 2012, Cytoskeleton.

[61]  J. Canman,et al.  Rho GTPases in animal cell cytokinesis: An occupation by the one percent , 2012, Cytoskeleton.

[62]  A. Bretscher,et al.  Myosin-V is activated by binding secretory cargo and released in coordination with Rab/exocyst function. , 2012, Developmental cell.

[63]  B. Wendland,et al.  Conserved roles for yeast Rho1 and mammalian RhoA GTPases in clathrin-independent endocytosis , 2012, Small GTPases.

[64]  Valerie C. Coffman,et al.  Contractile‐ring assembly in fission yeast cytokinesis: Recent advances and new perspectives , 2012, Cytoskeleton.

[65]  D. Kellogg,et al.  Cdk1-dependent control of membrane-trafficking dynamics , 2012, Molecular biology of the cell.

[66]  Jian-Qiu Wu,et al.  α-Actinin and fimbrin cooperate with myosin II to organize actomyosin bundles during contractile-ring assembly , 2012, Molecular biology of the cell.

[67]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[68]  Jian-Qiu Wu,et al.  Characterization of Mid1 domains for targeting and scaffolding in fission yeast cytokinesis , 2012, Journal of Cell Science.

[69]  Pengcheng Wu,et al.  Roles of the DYRK Kinase Pom2 in Cytokinesis, Mitochondrial Morphology, and Sporulation in Fission Yeast , 2011, PloS one.

[70]  D. E. Levin,et al.  Regulation of Cell Wall Biogenesis in Saccharomyces cerevisiae: The Cell Wall Integrity Signaling Pathway , 2011, Genetics.

[71]  T. Drivas,et al.  Existence of a novel clathrin-independent endocytic pathway in yeast that depends on Rho1 and formin , 2011, The Journal of cell biology.

[72]  J. Rizo,et al.  The crystal structure of a Munc13 C-terminal module exhibits a remarkable similarity to vesicle tethering factors. , 2011, Structure.

[73]  C. Shimoda,et al.  Endocytosis is essential for dynamic translocation of a syntaxin 1 orthologue during fission yeast meiosis , 2011, Molecular biology of the cell.

[74]  Craig C. Garner,et al.  v-SNARE Composition Distinguishes Synaptic Vesicle Pools , 2011, Neuron.

[75]  H. Gerritsen,et al.  The munc13-4-rab27 complex is specifically required for tethering secretory lysosomes at the plasma membrane. , 2011, Blood.

[76]  P. Newburger,et al.  Hemophagocytic lymphohistiocytosis with MUNC13‐4 gene mutation or reduced natural killer cell function prior to onset of childhood leukemia , 2011, Pediatric blood & cancer.

[77]  Valerie C. Coffman,et al.  Assembly and architecture of precursor nodes during fission yeast cytokinesis , 2011, The Journal of cell biology.

[78]  M. Balasubramanian,et al.  Marker reconstitution mutagenesis: a simple and efficient reverse genetic approach , 2011, Yeast.

[79]  Wei Li,et al.  Munc13 Mediates the Transition from the Closed Syntaxin–Munc18 complex to the SNARE complex , 2011, Nature Structural &Molecular Biology.

[80]  Anita T. Layton,et al.  Modeling Vesicle Traffic Reveals Unexpected Consequences for Cdc42p-Mediated Polarity Establishment , 2011, Current Biology.

[81]  W. Kiosses,et al.  Munc13-4 Restricts Motility of Rab27a-expressing Vesicles to Facilitate Lipopolysaccharide-induced Priming of Exocytosis in Neutrophils* , 2010, The Journal of Biological Chemistry.

[82]  T. Pollard,et al.  Cooperation Between the Septins and the Actomyosin Ring and Role of a Cell-Integrity Pathway During Cell Division in Fission Yeast , 2010, Genetics.

[83]  Thomas D. Pollard,et al.  Quantitative Analysis of the Mechanism of Endocytic Actin Patch Assembly and Disassembly in Fission Yeast , 2010, Molecular biology of the cell.

[84]  Thomas D. Pollard,et al.  Mathematical Modeling of Endocytic Actin Patch Kinetics in Fission Yeast: Disassembly Requires Release of Actin Filament Fragments , 2010, Molecular biology of the cell.

[85]  T. Südhof,et al.  Munc13 C2B-Domain – an Activity-Dependent Ca2+-Regulator of Synaptic Exocytosis , 2010, Nature Structural &Molecular Biology.

[86]  Thomas D. Pollard,et al.  Understanding cytokinesis: lessons from fission yeast , 2010, Nature Reviews Molecular Cell Biology.

[87]  Valerie C. Coffman,et al.  Roles of formin nodes and myosin motor activity in Mid1p-dependent contractile-ring assembly during fission yeast cytokinesis. , 2009, Molecular biology of the cell.

[88]  B. Grant,et al.  Pathways and mechanisms of endocytic recycling , 2009, Nature Reviews Molecular Cell Biology.

[89]  N. Grishin,et al.  Remote homology between Munc13 MUN domain and vesicle tethering complexes. , 2009, Journal of molecular biology.

[90]  T. Pollard,et al.  Characterization of two classes of small molecule inhibitors of Arp2/3 complex , 2009, Nature.

[91]  Wei Guo,et al.  The exocyst complex in polarized exocytosis. , 2004, International review of cytology.

[92]  C. Griesinger,et al.  Structural insights into the calmodulin-Munc13 interaction obtained by cross-linking and mass spectrometry. , 2009, Biochemistry.

[93]  C. Shimoda,et al.  The Schizosaccharomyces pombe Syntaxin 1 Homolog, Psy1, Is Essential in the Development of the Forespore Membrane , 2009, Bioscience, biotechnology, and biochemistry.

[94]  B. Beutler,et al.  The Rab27a Effectors JFC1/Slp1 and Munc13‐4 Regulate Exocytosis of Neutrophil Granules , 2008, Traffic.

[95]  P. Chavrier,et al.  Endocytic traffic in animal cell cytokinesis. , 2008, Current opinion in cell biology.

[96]  A. Echard.  Membrane traffic and polarization of lipid domains during cytokinesis. , 2008, Biochemical Society transactions.

[97]  J. Rizo,et al.  Binding of the Munc13-1 MUN domain to membrane-anchored SNARE complexes. , 2008, Biochemistry.

[98]  Yu Ting Zheng,et al.  Bidirectional regulation of Munc13–3 protein expression by age and dark rearing during the critical period in mouse visual cortex , 2007, Neuroscience.

[99]  L. Sheu,et al.  Interaction Between Munc13-1 and RIM Is Critical for Glucagon-Like Peptide-1–Mediated Rescue of Exocytotic Defects in Munc13-1–Deficient Pancreatic β-Cells , 2007, Diabetes.

[100]  T. Kirchhausen,et al.  Endosomal recycling controls plasma membrane area during mitosis , 2007, Proceedings of the National Academy of Sciences.

[101]  Y. Sánchez,et al.  Role of Rho GTPases and Rho‐GEFs in the regulation of cell shape and integrity in fission yeast , 2006, Yeast.

[102]  T. Pollard,et al.  Assembly of the cytokinetic contractile ring from a broad band of nodes in fission yeast , 2006, The Journal of cell biology.

[103]  M. Balasubramanian,et al.  Cell cycle-dependent roles for the FCH-domain protein Cdc15p in formation of the actomyosin ring in Schizosaccharomyces pombe. , 2006, Molecular biology of the cell.

[104]  Y. Hiraoka,et al.  ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe , 2006, Nature Biotechnology.

[105]  T. Südhof,et al.  Structural Basis for a Munc13–1 Homodimer to Munc13–1/RIM Heterodimer Switch , 2006, PLoS biology.

[106]  F. Baluška,et al.  Cytokinesis in plant and animal cells: endosomes 'shut the door'. , 2006, Developmental biology.

[107]  Lili Wang,et al.  Schizosaccharomyces pombe Git1 Is a C2-Domain Protein Required for Glucose Activation of Adenylate Cyclase , 2006, Genetics.

[108]  J. Kaplan,et al.  UNC-13 Interaction with Syntaxin Is Required for Synaptic Transmission , 2005, Current Biology.

[109]  C. D’Souza-Schorey,et al.  Endocytosis Resumes during Late Mitosis and Is Required for Cytokinesis* , 2005, Journal of Biological Chemistry.

[110]  David G. Drubin,et al.  A Modular Design for the Clathrin- and Actin-Mediated Endocytosis Machinery , 2005, Cell.

[111]  Thomas D Pollard,et al.  Counting Cytokinesis Proteins Globally and Locally in Fission Yeast , 2005, Science.

[112]  S. Redick,et al.  Centriolin Anchoring of Exocyst and SNARE Complexes at the Midbody Is Required for Secretory-Vesicle-Mediated Abscission , 2005, Cell.

[113]  K. Gould,et al.  Role of septins and the exocyst complex in the function of hydrolytic enzymes responsible for fission yeast cell separation. , 2005, Molecular biology of the cell.

[114]  T. Kuno,et al.  Phosphatidylinositol-4-phosphate 5-Kinase Regulates Fission Yeast Cell Integrity through a Phospholipase C-mediated Protein Kinase C-independent Pathway* , 2005, Journal of Biological Chemistry.

[115]  Lynn VerPlank,et al.  Cell cycle-regulated trafficking of Chs2 controls actomyosin ring stability during cytokinesis. , 2005, Molecular biology of the cell.

[116]  W. Sullivan,et al.  Membrane traffic: a driving force in cytokinesis. , 2005, Trends in cell biology.

[117]  Josep Rizo,et al.  Intramolecular occlusion of the diacylglycerol-binding site in the C1 domain of munc13-1. , 2005, Biochemistry.

[118]  Toshihide Hige,et al.  Vesicle Endocytosis Requires Dynamin-Dependent GTP Hydrolysis at a Fast CNS Synapse , 2005, Science.

[119]  Y. Sánchez,et al.  The novel fission yeast (1,3)β-D-glucan synthase catalytic subunit Bgs4p is essential during both cytokinesis and polarized growth , 2005, Journal of Cell Science.

[120]  M. Cyert,et al.  Molecular Analysis Reveals Localization of Saccharomyces cerevisiae Protein Kinase C to Sites of Polarized Growth and Pkc1p Targeting to the Nucleus and Mitotic Spindle , 2005, Eukaryotic Cell.

[121]  Y. Sánchez,et al.  Schizosaccharomyces pombe Rgf3p is a specific Rho1 GEF that regulates cell wall β-glucan biosynthesis through the GTPase Rho1p , 2004, Journal of Cell Science.

[122]  A. Heck,et al.  Munc13-4 is an effector of rab27a and controls secretion of lysosomes in hematopoietic cells. , 2004, Molecular biology of the cell.

[123]  T. Kawate,et al.  Organization of a sterol-rich membrane domain by cdc15p during cytokinesis in fission yeast , 2004, Nature Cell Biology.

[124]  N. Dekker,et al.  Role of the α-Glucanase Agn1p in Fission-Yeast Cell Separation , 2004 .

[125]  V. Bigl,et al.  Munc13-1-mediated Vesicle Priming Contributes to Secretory Amyloid Precursor Protein Processing* , 2004, Journal of Biological Chemistry.

[126]  F. Varoqueaux,et al.  Regulation of Insulin Exocytosis by Munc13-1* , 2003, Journal of Biological Chemistry.

[127]  A. Martín-Cuadrado,et al.  The endo-β-1,3-glucanase eng1p is required for dissolution of the primary septum during cell separation in Schizosaccharomyces pombe , 2003, Journal of Cell Science.

[128]  Steven Bedrick,et al.  Furrow microtubules and localized exocytosis in cleaving Xenopus laevis embryos , 2003, Journal of Cell Science.

[129]  Yu Ting Zheng,et al.  Identification of Munc13-3 as a Candidate Gene for Critical-Period Neuroplasticity in Visual Cortex , 2002, The Journal of Neuroscience.

[130]  H. Schwarz,et al.  Furrow-specific endocytosis during cytokinesis of zebrafish blastomeres. , 2002, Experimental cell research.

[131]  D. Burgess,et al.  Targeted new membrane addition in the cleavage furrow is a late, separate event in cytokinesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[132]  Jianhua Liu,et al.  The localization of the integral membrane protein Cps1p to the cell division site is dependent on the actomyosin ring and the septation-inducing network in Schizosaccharomyces pombe. , 2002, Molecular biology of the cell.

[133]  Dannel McCollum,et al.  The multiprotein exocyst complex is essential for cell separation in Schizosaccharomyces pombe. , 2002, Molecular biology of the cell.

[134]  John White,et al.  Completion of cytokinesis in C. elegans requires a brefeldin A-sensitive membrane accumulation at the cleavage furrow apex , 2001, Current Biology.

[135]  I. Maruyama,et al.  Synaptic exocytosis and nervous system development impaired in Caenorhabditis elegans unc-13 mutants , 2001, Neuroscience.

[136]  J. Bähler,et al.  Roles of a fimbrin and an alpha-actinin-like protein in fission yeast cell polarization and cytokinesis. , 2001, Molecular biology of the cell.

[137]  Wei Guo,et al.  Spatial regulation of the exocyst complex by Rho1 GTPase , 2001, Nature Cell Biology.

[138]  T. O'Halloran,et al.  Cytokinesis failure in clathrin-minus cells is caused by cleavage furrow instability. , 2001, Cell motility and the cytoskeleton.

[139]  A. Dautry‐Varsat,et al.  Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. , 2001, Molecular cell.

[140]  Richard H. Scheller,et al.  SNARE-mediated membrane fusion , 2001, Nature Reviews Molecular Cell Biology.

[141]  T. Takenawa,et al.  Phosphatidylinositol 4-Phosphate 5-Kinase Its3 and Calcineurin Ppb1 Coordinately Regulate Cytokinesis in Fission Yeast* , 2000, The Journal of Biological Chemistry.

[142]  J. Ribas,et al.  A family of multifunctional thiamine-repressible expression vectors for fission yeast. , 2000 .

[143]  H. Wang,et al.  Drc1p/Cps1p, a 1,3-beta-glucan synthase subunit, is essential for division septum assembly in Schizosaccharomyces pombe. , 1999, Genetics.

[144]  E. Jorgensen,et al.  UNC-13 is required for synaptic vesicle fusion in C. elegans , 1999, Nature Neuroscience.

[145]  Kendal Broadie,et al.  Drosophila Unc-13 is essential for synaptic transmission , 1999, Nature Neuroscience.

[146]  M. Valdivieso,et al.  Schizosaccharomyces pombe protein kinase C homologues, pck1p and pck2p, are targets of rho1p and rho2p and differentially regulate cell integrity. , 1999, Journal of cell science.

[147]  P. Novick,et al.  Exo84p Is an Exocyst Protein Essential for Secretion* , 1999, The Journal of Biological Chemistry.

[148]  T. Toda,et al.  Fission Yeast α-Glucan Synthase Mok1 Requires the Actin Cytoskeleton to Localize the Sites of Growth and Plays an Essential Role in Cell Morphogenesis Downstream of Protein Kinase C Function , 1999, The Journal of cell biology.

[149]  P. Novick,et al.  The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis , 1999, The EMBO journal.

[150]  P. Philippsen,et al.  Heterologous modules for efficient and versatile PCR‐based gene targeting in Schizosaccharomyces pombe , 1998, Yeast.

[151]  J. Ishiguro,et al.  cps1+, a Schizosaccharomyces pombe gene homolog of Saccharomyces cerevisiae FKS genes whose mutation confers hypersensitivity to cyclosporin A and papulacandin B , 1997, Journal of bacteriology.

[152]  T. Sasaki,et al.  Bni1p and Bnr1p: downstream targets of the Rho family small G‐proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae , 1997, The EMBO journal.

[153]  P. Novick,et al.  The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. , 1996, The EMBO journal.

[154]  K. Gould,et al.  The Schizosaccharomyces pombe actin‐related protein, Arp3, is a component of the cortical actin cytoskeleton and interacts with profilin. , 1996, The EMBO journal.

[155]  P. Pérez,et al.  Rho 1 GTPase activates the (1–3)beta‐D‐glucan synthase and is involved in Schizosaccharomyces pombe morphogenesis. , 1996, The EMBO journal.

[156]  K. Hofmann,et al.  Mammalian Unc-13 homologues as possible regulators of neurotransmitter release. , 1996, Biochemical Society transactions.

[157]  K. Tanaka,et al.  A downstream target of RHO1 small GTP‐binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae. , 1995, The EMBO journal.

[158]  T. Südhof,et al.  Mammalian Homologues of Caenorhabditis elegans unc-13 Gene Define Novel Family of C2-domain Proteins (*) , 1995, The Journal of Biological Chemistry.

[159]  A. Reymond,et al.  The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis , 1995, Cell.

[160]  Jonathan Pevsner,et al.  Specificity and regulation of a synaptic vesicle docking complex , 1994, Neuron.

[161]  P. De Camilli,et al.  A rat brain Sec1 homologue related to Rop and UNC18 interacts with syntaxin. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[162]  T. Südhof,et al.  Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin , 1993, Nature.

[163]  P. Pérez,et al.  Isolation and characterization of Schizosaccharomyces pombe mutants defective in cell wall (1-3)beta-D-glucan , 1991, Journal of bacteriology.

[164]  K. Maundrell.  nmt1 of fission yeast. A highly transcribed gene completely repressed by thiamine. , 1990, The Journal of biological chemistry.

[165]  P. Thuriaux,et al.  Genetic Mapping in SCHIZOSACCHAROMYCES POMBE by Mitotic and Meiotic Analysis and Induced Haploidization. , 1977, Genetics.

[166]  Jian-Qiu Wu,et al.  Real-Time Visualization and Quantification of Contractile Ring Proteins in Single Living Cells. , 2016, Methods in molecular biology.

[167]  D. Drubin,et al.  Clathrin-mediated endocytosis in budding yeast. , 2012, Trends in cell biology.

[168]  Erik Meijering,et al.  Methods for cell and particle tracking. , 2012, Methods in enzymology.

[169]  S. Nurrish,et al.  Rho is a presynaptic activator of neurotransmitter release at pre-existing synapses in C. elegans. , 2006, Genes & development.

[170]  C. Shimoda,et al.  A fission yeast SNAP-25 homologue, SpSec9, is essential for cytokinesis and sporulation. , 2005, Cell structure and function.

[171]  D. Mastronarde,et al.  Using rapid freeze and freeze-substitution for the preparation of yeast cells for electron microscopy and three-dimensional analysis. , 2001, Methods in cell biology.

[172]  Á. Durán,et al.  A family of multifunctional thiamine‐repressible expression vectors for fission yeast , 2000, Yeast.

[173]  M. Reedy,et al.  Disruption of a dynamin homologue affects endocytosis, organelle morphology, and cytokinesis in Dictyostelium discoideum. , 1999, Molecular biology of the cell.

[174]  D. E. Levin,et al.  Dissecting the protein kinase C/MAP kinase signalling pathway of Saccharomyces cerevisiae. , 1994, Cellular & molecular biology research.

[175]  S. Moreno,et al.  Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. , 1991, Methods in enzymology.

[176]  of the S. , 2022 .