Cytoskeletal dynamics in fission yeast: A review of models for polarization and division

We review modeling studies concerning cytoskeletal activity of fission yeast. Recent models vary in length and time scales, describing a range of phenomena from cellular morphogenesis to polymer assembly. The components of cytoskeleton act in concert to mediate cell‐scale events and interactions such as polarization. The mathematical models reduce these events and interactions to their essential ingredients, describing the cytoskeleton by its bulk properties. On a smaller scale, models describe cytoskeletal subcomponents and how bulk properties emerge.

[1]  F. Jülicher,et al.  Self-organization and mechanical properties of active filament bundles. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[2]  V. Doye,et al.  A Mechanism for Nuclear Positioning in Fission Yeast Based on Microtubule Pushing , 2001, The Journal of cell biology.

[3]  Sophie G. Martin,et al.  New End Take Off: Regulating Cell Polarity during the Fission , 2005, Cell cycle.

[4]  R. Daga,et al.  Asymmetric Microtubule Pushing Forces in Nuclear Centering , 2006, Current Biology.

[5]  A. Mogilner,et al.  Quantitative modeling in cell biology: what is it good for? , 2006, Developmental cell.

[6]  P. Camilli,et al.  The BAR Domain Superfamily: Membrane-Molding Macromolecules , 2009, Cell.

[7]  M. Marchetti,et al.  Rheology of active filament solutions. , 2006, Physical review letters.

[8]  A. Mogilner,et al.  Modeling mitosis. , 2006, Trends in cell biology.

[9]  D. Riveline Explaining Lengths and Shapes of Yeast by Scaling Arguments , 2009, PloS one.

[10]  Eugenio Marco,et al.  Endocytosis Optimizes the Dynamic Localization of Membrane Proteins that Regulate Cortical Polarity , 2007, Cell.

[11]  X. Le Goff,et al.  Fission yeast cytoskeletons and cell polarity factors: connecting at the cortex. , 2006, Biology of the cell.

[12]  G. Oster,et al.  Endocytic vesicle scission by lipid phase boundary forces , 2006, Proceedings of the National Academy of Sciences.

[13]  Jacqueline Hayles,et al.  A journey into space , 2001, Nature Reviews Molecular Cell Biology.

[14]  I. Tolic-Nørrelykke,et al.  Self-Organization of Dynein Motors Generates Meiotic Nuclear Oscillations , 2009, PLoS biology.

[15]  David J. Odde,et al.  Chromosome Congression by Kinesin-5 Motor-Mediated Disassembly of Longer Kinetochore Microtubules , 2008, Cell.

[16]  A. Bretscher,et al.  Analysis of unregulated formin activity reveals how yeast can balance F-actin assembly between different microfilament-based organizations. , 2008, Molecular biology of the cell.

[17]  Sophie G. Martin,et al.  Shaping fission yeast with microtubules. , 2009, Cold Spring Harbor perspectives in biology.

[18]  M. Mishra,et al.  Cytokinesis: Catch and Drag , 2008, Current Biology.

[19]  S. Carbona,et al.  Fission yeast cytoskeletons and cell polarity factors: connecting at the cortex , 2006 .

[20]  David G. Drubin,et al.  The Mechanochemistry of Endocytosis , 2009, PLoS biology.

[21]  G Danuser,et al.  Yeast kinetochore microtubule dynamics analyzed by high-resolution three-dimensional microscopy. , 2005, Biophysical journal.

[22]  P. Fantes,et al.  Yeast cell cycle. , 1989, Current opinion in cell biology.

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

[24]  Anthony A. Hyman,et al.  Supporting Material : Stress Generation and Filament Turnover During Actin Ring Constriction , 2007 .

[25]  Paul Nurse,et al.  A spatial gradient coordinates cell size and mitotic entry in fission yeast , 2009, Nature.

[26]  Kamila Larripa,et al.  Transport of a 1D viscoelastic actin-myosin strip of gel as a model of a crawling cell. , 2006, Physica A.

[27]  Alexander van Oudenaarden,et al.  A system of counteracting feedback loops regulates Cdc42p activity during spontaneous cell polarization. , 2005, Developmental cell.

[28]  Kerry Bloom,et al.  Tension-dependent regulation of microtubule dynamics at kinetochores can explain metaphase congression in yeast. , 2005, Molecular biology of the cell.

[29]  J. J. Ward,et al.  Phospho-regulated interaction between kinesin-6 Klp9p and microtubule bundler Ase1p promotes spindle elongation. , 2009, Developmental cell.

[30]  K. Gould,et al.  Stepping into the ring: the SIN takes on contractile ring assembly. , 2008, Genes & development.

[31]  I. Tolic-Nørrelykke,et al.  Growth pattern of single fission yeast cells is bilinear and depends on temperature and DNA synthesis. , 2009, Biophysical journal.

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

[33]  Thomas D. Pollard,et al.  Actin, a Central Player in Cell Shape and Movement , 2009, Science.

[34]  F. Nédélec,et al.  Force- and length-dependent catastrophe activities explain interphase microtubule organization in fission yeast , 2008, Molecular systems biology.

[35]  H. Meinhardt,et al.  Pattern formation by local self-activation and lateral inhibition. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[36]  D. Drubin,et al.  The yeast actin cytoskeleton. , 1994, Current opinion in cell biology.

[37]  P. Tran,et al.  Cell Shape and Cell Division in Fission Yeast , 2009, Current Biology.

[38]  M. Gardel,et al.  Identification and characterization of a small molecule inhibitor of formin-mediated actin assembly. , 2009, Chemistry & biology.

[39]  I. Tolic-Nørrelykke Push-me-pull-you: how microtubules organize the cell interior , 2008, European Biophysics Journal.

[40]  Roie Shlomovitz,et al.  Physical model of contractile ring initiation in dividing cells. , 2008, Biophysical journal.

[41]  T. Pollard,et al.  Interactions of WASp, myosin-I, and verprolin with Arp2/3 complex during actin patch assembly in fission yeast , 2005, The Journal of cell biology.

[42]  Francesco S. Pavone,et al.  Nuclear and Division-Plane Positioning Revealed by Optical Micromanipulation , 2005, Current Biology.

[43]  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.

[44]  J. Small The actin cytoskeleton. , 1988, Electron microscopy reviews.

[45]  J. Marks,et al.  Growth Polarity and Cytokinesis in Fission Yeast: The Role of the Cytoskeleton , 1986, Journal of Cell Science.

[46]  P. Nurse,et al.  Growth in cell length in the fission yeast Schizosaccharomyces pombe. , 1985, Journal of cell science.

[47]  E. Salmon,et al.  Stable Kinetochore-Microtubule Attachment Constrains Centromere Positioning in Metaphase , 2004, Current Biology.

[48]  David J Odde,et al.  Mechanisms of microtubule-based kinetochore positioning in the yeast metaphase spindle. , 2003, Biophysical journal.

[49]  A. Carlsson Contractile stress generation by actomyosin gels. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[50]  Michel Bornens,et al.  Physical Mechanisms Redirecting Cell Polarity and Cell Shape in Fission Yeast , 2008, Current Biology.

[51]  G. Salbreux,et al.  Hydrodynamics of cellular cortical flows and the formation of contractile rings. , 2009, Physical review letters.

[52]  V. Simanis,et al.  Mid1p/anillin and the septation initiation network orchestrate contractile ring assembly for cytokinesis. , 2008, Genes & development.

[53]  Sophie G. Martin Microtubule-dependent cell morphogenesis in the fission yeast. , 2009, Trends in cell biology.

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

[55]  Andrew B Goryachev,et al.  Dynamics of Cdc42 network embodies a Turing‐type mechanism of yeast cell polarity , 2008, FEBS letters.

[56]  Dimitrios Vavylonis,et al.  Assembly Mechanism of the Contractile Ring for Cytokinesis by Fission Yeast , 2008, Science.

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

[58]  A. M. Turing,et al.  The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[59]  Brian D. Slaughter,et al.  Dual modes of cdc42 recycling fine-tune polarized morphogenesis. , 2009, Developmental cell.

[60]  F. Nédélec,et al.  Crosslinkers and Motors Organize Dynamic Microtubules to Form Stable Bipolar Arrays in Fission Yeast , 2007, Cell.

[61]  P. Nurse,et al.  tea1 and the Microtubular Cytoskeleton Are Important for Generating Global Spatial Order within the Fission Yeast Cell , 1997, Cell.

[62]  K. Sawin,et al.  Cytoplasmic microtubule organization in fission yeast , 2006, Yeast.

[63]  Mark Bathe,et al.  Cytokinesis and the contractile ring in fission yeast: towards a systems-level understanding. , 2010, Trends in microbiology.

[64]  Sophie G. Martin,et al.  The Cell-End Factor Pom1p Inhibits Mid1p in Specification of the Cell Division Plane in Fission Yeast , 2006, Current Biology.

[65]  I. Rupeš,et al.  Ssp1 promotes actin depolymerization and is involved in stress response and new end take-off control in fission yeast. , 1999, Molecular biology of the cell.

[66]  Sophie G. Martin,et al.  Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle , 2009, Nature.

[67]  Fred Chang,et al.  Dynamics of the Formin For3p in Actin Cable Assembly , 2006, Current Biology.

[68]  Dimitrios Vavylonis,et al.  Model of For3p-Mediated Actin Cable Assembly in Fission Yeast , 2008, PloS one.

[69]  I. Tolic-Nørrelykke Force and length regulation in the microtubule cytoskeleton: lessons from fission yeast. , 2010, Current opinion in cell biology.

[70]  Indrani Bose,et al.  Singularity in Polarization: Rewiring Yeast Cells to Make Two Buds , 2009, Cell.

[71]  C. V. Rao,et al.  Calling heads from tails: the role of mathematical modeling in understanding cell polarization. , 2009, Current opinion in cell biology.

[72]  F. Jülicher,et al.  Continuum description of the cytoskeleton: ring formation in the cell cortex. , 2005, Physical review letters.

[73]  M. Yamamoto Fission yeast. , 1989, Biotechnology.

[74]  Scott V. Bratman,et al.  Establishing New Sites of Polarization by Microtubules , 2009, Current Biology.

[75]  M Piel,et al.  Rebuilding cytoskeleton roads: active-transport-induced polarization of cells. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[76]  Bruce L. Goode,et al.  The Yeast Actin Cytoskeleton: from Cellular Function to Biochemical Mechanism , 2006, Microbiology and Molecular Biology Reviews.

[77]  Sigurd B. Angenent,et al.  On the spontaneous emergence of cell polarity , 2008, Nature.

[78]  J. Cooper,et al.  Distinct Roles for Arp2/3 Regulators in Actin Assembly and Endocytosis , 2008, PLoS biology.

[79]  Å. Fransson,et al.  Pombe Cdc15 homology proteins: regulators of membrane dynamics and the actin cytoskeleton. , 2006, Trends in biochemical sciences.

[80]  Sophie G. Martin,et al.  Regulation of the formin for3p by cdc42p and bud6p. , 2007, Molecular biology of the cell.

[81]  Attila Csikász-Nagy,et al.  Spatial controls for growth zone formation during the fission yeast cell cycle , 2008, Yeast.