Model of Fission Yeast Cell Shape Driven by Membrane-Bound Growth Factors and the Cytoskeleton

PLoS Computational Biology

Volumn 9, Issue 10, 2013, Pages

  Drake, Tyler ^a   Vavylonis, Dimitrios ^a  

^a LEHIGH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; CELL SIGNALING; COMPUTATION THEORY; COMPUTATIONAL METHODS; PROTEINS; SCAFFOLDS (BIOLOGY); YEAST;

CELL DIAMETERS; CELL SHAPES; CELL WALLS; COMPUTATIONAL MODELLING; CYTOSKELETONS; FISSION YEAST; MICROTUBULES; SPATIAL EXTENT; WALL REMODELING; YEAST CELL;

MACHINERY;

GROWTH FACTOR; PROTEIN CDC42; REGULATOR PROTEIN;

ARTICLE; CELL DIVISION; CELL GROWTH; CELL POLARITY; CELL SHAPE; CELL SIZE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MICROTUBULE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; SCHIZOSACCHAROMYCES; SEQUENCE ALIGNMENT; TURGOR PRESSURE;

SCHIZOSACCHAROMYCETACEAE;

CELL SHAPE; COMPUTER SIMULATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICROTUBULES; MODELS, BIOLOGICAL; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84887294438     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003287     Document Type: Article

References (81)

1. Fischer R, Zekert N, Takeshita N, (2008) Polarized growth in fungi-interplay between the cytoskeleton, positional markers and membrane domains. Mol Microbiol 68: 813-826.
2. Geitmann A, Ortega JKE, (2009) Mechanics and modeling of plant cell growth. Trends Plant Sci 14: 467-478.
3. Brown PJ, Kysela DT, Brun YV, (2011) Polarity and the diversity of growth mechanisms in bacteria. Semin Cell Dev Biol 22: 790-798.
4. Chang F, Martin SG, (2009) Shaping fission yeast with microtubules. Cold Spring Harb Perspect Biol 1: a001347.
5. Huisman SM, Brunner D, (2011) Cell polarity in fission yeast: a matter of confining, positioning, and switching growth zones. Semin Cell Dev Biol 22: 799-805.
6. Hachet O, Bendezu FO, Martin SG, (2012) Fission yeast: in shape to divide. Curr Opin Cell Biol 24: 858-864.
7. Verde F, Mata J, Nurse P, (1995) Fission Yeast-Cell Morphogenesis- Identification of New Genes and Analysis of Their Role during the Cell-Cycle. J Cell Biol 131: 1529-1538.
8. Verde F, Wiley DJ, Nurse P, (1998) Fission yeast orb6, a ser/thr protein kinase related to mammalian rho kinase and myotonic dystrophy kinase, is required for maintenance of cell polarity and coordinates cell morphogenesis with the cell cycle. Proc Natl Acad Sci U S A 95: 7526-7531.
9. Villar-Tajadura MA, Coll PM, Madrid M, Cansado J, Santos B, et al. (2008) Rga2 is a Rho2 GAP that regulates morphogenesis and cell integrity in S. pombe. Mol Microbiol 70: 867-881.
10. Das M, Wiley DJ, Chen X, Shah K, Verde F, (2009) The conserved NDR kinase Orb6 controls polarized cell growth by spatial regulation of the small GTPase Cdc42. Curr Biol 19: 1314-1319.
11. Kelly FD, Nurse P, (2011) Spatial control of Cdc42 activation determines cell width in fission yeast. Mol Biol Cell 22: 3801-3811.
12. Mata J, Nurse P, (1997) tea1 and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell. Cell 89: 939-949.
13. Cheung AY, Wu HM, (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59: 547-572.
14. La Carbona S, Le Goff C, Le Goff X, (2006) Fission yeast cytoskeletons and cell polarity factors: connecting at the cortex. Biol Cell 98: 619-631.
15. Das M, Drake T, Wiley DJ, Buchwald P, Vavylonis D, et al. (2012) Oscillatory Dynamics of Cdc42 GTPase in the Control of Polarized Growth. Science 337: 239-243.
16. Kelly FD, Nurse P, (2011) De Novo Growth Zone Formation from Fission Yeast Spheroplasts. Plos One 6: e27977.
17. Bendezu FO, Martin SG, (2011) Actin cables and the exocyst form two independent morphogenesis pathways in the fission yeast. Mol Biol Cell 22: 44-53.
18. Cortes JCG, Ishiguro J, Duran A, Ribas JC, (2002) Localization of the (1,3)beta-D-glucan synthase catalytic subunit homologue Bgs1p/Cps1p from fission yeast suggests that it is involved in septation, polarized growth, mating, spore wall formation and spore germination. J Cell Sci 115: 4081-4096.
19. Cortes JCG, Carnero E, Ishiguro J, Sanchez Y, Duran A, et al. (2005) The novel fission yeast (1,3)beta-D-glucan synthase catalytic subunit Bgs4p is essential during both cytokinesis and polarized growth. J Cell Sci 118: 157-174.
20. Minc N, Bratman SV, Basu R, Chang F, (2009) Establishing New Sites of Polarization by Microtubules. Curr Biol 19: 83-94.
21. Terenna CR, Makushok T, Velve-Casquillas G, Baigl D, Chen Y, et al. (2008) Physical Mechanisms Redirecting Cell Polarity and Cell Shape in Fission Yeast. Curr Biol 18: 1748-1753.
22. Minc N, Boudaoud A, Chang F, (2009) Mechanical Forces of Fission Yeast Growth. Curr Biol 19: 1096-1101.
23. Drake T, Vavylonis D, (2010) Cytoskeletal dynamics in fission yeast: a review of models for polarization and division. HFSP J 4: 122-130.
24. Mitchison JM, Nurse P, (1985) Growth in Cell Length in the Fission Yeast Schizosaccharomyces-Pombe. J Cell Sci 75: 357-376.
25. Dumais J, Shaw SL, Steele CR, Long SR, Ray PM, (2006) An anisotropic-viscoplastic model of plant cell morphogenesis by tip growth. Int J Dev Biol 50: 209-222.
26. Ugural AC (1999) Stresses in plates and shells. Boston: WCB/McGraw Hill. 502 p.
27. Slaughter BD, Das A, Schwartz JW, Rubinstein B, Li R, (2009) Dual modes of cdc42 recycling fine-tune polarized morphogenesis. Dev Cell 17: 823-835.
28. Lee IJ, Wu JQ, (2012) Characterization of Mid1 domains for targeting and scaffolding in fission yeast cytokinesis. J Cell Sci 125: 2973-2985.
29. Tatebe H, Nakano K, Maximo R, Shiozaki K, (2008) Pom1 DYRK regulates localization of the Rga4 GAP to ensure bipolar activation of Cdc42 in fission yeast. Curr Biol 18: 322-330.
30. Levin DE, Bishop JM, (1990) A putative protein kinase gene (kin1+) is important for growth polarity in Schizosaccharomyces pombe. Proc Natl Acad Sci U S A 87: 8272-8276.
31. Osumi M, (1998) The ultrastructure of yeast: Cell wall structure and formation. Micron 29: 207-233.
32. Wang H, Vavylonis D, (2008) Model of For3p-Mediated Actin Cable Assembly in Fission Yeast. Plos One 3: e4078.
33. Berro J, Sirotkin V, Pollard TD, (2010) Mathematical Modeling of Endocytic Actin Patch Kinetics in Fission Yeast: Disassembly Requires Release of Actin Filament Fragments. Mol Biol Cell 21: 2905-2915.
34. Sirotkin V, Beltzner CC, Marchand JB, Pollard TD, (2005) Interactions of WASp, myosin-I, and verprolin with Arp2/3 complex during actin patch assembly in fission yeast. J Cell Biol 170: 637-648.
35. Janson ME, Loughlin R, Loiodice I, Fu CH, Brunner D, et al. (2007) Crosslinkers and motors organize dynamic microtubules to form stable bipolar arrays in fission yeast. Cell 128: 357-368.
36. Drummond DR, Cross RA, (2000) Dynamics of interphase microtubules in Schizosaccharomyces pombe. Curr Biol 10: 766-775.
37. Tischer C, Brunner D, Dogterom M, (2009) Force- and kinesin-8-dependent effects in the spatial regulation of fission yeast microtubule dynamics. Mol Syst Biol 5: 250.
38. Snaith HA, Sawin KE, (2003) Fission yeast mod5p regulates polarized growth through anchoring of tea1p at cell tips. Nature 423: 647-651.
39. Martin SG, (2009) Microtubule-dependent cell morphogenesis in the fission yeast. Trends Cell Biol 19: 447-454.
40. Martin SG, McDonald WH, Yates JR, Chang F, (2005) Tea4p links microtubule plus ends with the formin For3p in the establishment of cell polarity. Dev Cell 8: 479-491.
41. Bicho CC, Kelly DA, Snaith HA, Goryachev AB, Sawin KE, (2010) A catalytic role for Mod5 in the formation of the Tea1 cell polarity landmark. Curr Biol 20: 1752-1757.
42. Foethke D, Makushok T, Brunner D, Nedelec F, (2009) Force- and length-dependent catastrophe activities explain interphase microtubule organization in fission yeast. Mol Syst Biol 5: 241.
43. Goryachev AB, Pokhilko AV, (2008) Dynamics of Cdc42 network embodies a Turing-type mechanism of yeast cell polarity. Febs Lett 582: 1437-1443.
44. Saunders TE, Pan KZ, Angel A, Guan Y, Shah JV, et al. (2012) Noise reduction in the intracellular pom1p gradient by a dynamic clustering mechanism. Dev Cell 22: 558-572.
45. Hirata D, Masuda H, Eddison M, Toda T, (1998) Essential role of tubulin-folding cofactor D in microtubule assembly and its association with microtubules in fission yeast. EMBO J 17: 658-666.
46. Thadani R, Huang D, Oliferenko S, (2011) Robust polarity specification operates above a threshold of microtubule dynamicity. Cytoskeleton (Hoboken) 68: 290-299.
47. Marco E, Wedlich-Soldner R, Li R, Altschuler SJ, Wu LF, (2007) Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity. Cell 129: 411-422.
48. Glynn JM, Lustig RJ, Berlin A, Chang F, (2001) Role of bud6p and tea1p in the interaction between actin and microtubules for the establishment of cell polarity in fission yeast. Curr Biol 11: 836-845.
49. Martin SG, Rincon SA, Basu R, Perez P, Chang F, (2007) Regulation of the formin for3p by cdc42p and bud6p. Mol Biol Cell 18: 4155-4167.
50. Dodgson J, Chessel A, Yamamoto M, Vaggi F, Cox S, et al. (2013) Spatial segregation of polarity factors into distinct cortical clusters is required for cell polarity control. Nat Commun 4: 1834.
51. de Gennes PG, (1982) Kinetics of Diffusion-Controlled Processes in Dense Polymer Systems. 1. Non-Entangled Regimes. J Chem Phys 76: 3316-3321.
52. Feierbach B, Chang F, (2001) Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Curr Biol 11: 1656-1665.
53. Yaffe MP, Harata D, Verde F, Eddison M, Toda T, et al. (1996) Microtubules mediate mitochondrial distribution in fission yeast. Proc Natl Acad Sci USA 93: 11664-11668.
54. Hagan IM, (1998) The fission yeast microtubule cytoskeleton. J Cell Sci 111: 1603-1612.
55. Csikasz-Nagy A, Gyorffy B, Alt WG, Tyson JJ, Novak B, (2008) Spatial controls for growth zone formation during the fission yeast cell cycle. Yeast 25: 59-69.
56. Paoletti A, Chang F, (2000) Analysis of mid1p, a protein required for placement of the cell division site, reveals a link between the nucleus and the cell surface in fission yeast. Mol Biol Cell 11: 2757-2773.
57. Castagnetti S, Behrens R, Nurse P, (2005) End4/Sla2 is involved in establishment of a new growth zone in Schizosaccharomyces pombe. J Cell Sci 118: 1843-1850 doi: 10.1242/jcs.02311.
58. Bendezú FO, Martin SG, (2013) Cdc42 Explores the Cell Periphery for Mate Selection in Fission Yeast. Curr Biol 23: 42-47.
59. Chebli Y, Kaneda M, Zerzour R, Geitmann A, (2012) The cell wall of the Arabidopsis pollen tube-spatial distribution, recycling, and network formation of polysaccharides. Plant Physiol 160: 1940-1955.
60. Fayant P, Girlanda O, Chebli Y, Aubin CE, Villemure I, et al. (2010) Finite element model of polar growth in pollen tubes. Plant Cell 22: 2579-2593.
61. Latge JP, (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66: 279-290.
62. Manners DJ, Meyer MT, (1977) Molecular-Structures of Some Glucans from Cell-Walls of Schizosaccharomyces-Pombe. Carbohyd Res 57: 189-203.
63. Howard RJ, (1981) Ultrastructural Analysis of Hyphal Tip Cell-Growth in Fungi- Spitzenkorper, Cytoskeleton and Endomembranes after Freeze-Substitution. J Cell Sci 48: 89-103.
64. Eggen E, de Keijzer MN, Mulder BM, (2011) Self-regulation in tip-growth: The role of cell wall ageing. J Theor Biol 283: 113-121.
65. Gierz G, Bartnicki-Garcia S, (2001) A three-dimensional model of fungal morphogenesis based on the vesicle supply center concept. J Theor Biol 208: 151-164.
66. Goriely A, Tabor M, (2003) Biomechanical models of hyphal growth in actinomycetes. J Theor Biol 222: 211-218.
67. Campas O, Mahadevan L, (2009) Shape and dynamics of tip-growing cells. Curr Biol 19: 2102-2107.
68. Touhami A, Nysten B, Dufrêne YF, (2003) Nanoscale Mapping of the Elasticity of Microbial Cells by Atomic Force Microscopy. Langmuir 19: 4539-4543.
69. Cosgrove DJ, (1993) How do plant cell walls extend? Plant Physiol 102: 1-6.
70. Szymanski DB, Cosgrove DJ, (2009) Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr Biol 19: R800-811.
71. Misra G, Rojas ER, Gopinathan A, Huang KC, (2013) Mechanical consequences of cell-wall turnover in the elongation of a gram-positive bacterium. Biophys J 104: 2342-2352.
72. Daniel RA, Errington J, (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113: 767-776.
73. Dominguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Soldner R, et al. (2011) Processive Movement of MreB-Associated Cell Wall Biosynthetic Complexes in Bacteria. Science 333: 225-228.
74. Garner EC, Bernard R, Wang WQ, Zhuang XW, Rudner DZ, et al. (2011) Coupled, Circumferential Motions of the Cell Wall Synthesis Machinery and MreB Filaments in B. subtilis. Science 333: 222-225.
75. Wang S, Furchtgott L, Huang KC, Shaevitz JW, (2012) Helical insertion of peptidoglycan produces chiral ordering of the bacterial cell wall. Proc Natl Acad Sci USA 109: E595-E604.
76. Swulius MT, Jensen GJ, (2012) The Helical MreB Cytoskeleton in Escherichia coli MC1000/pLE7 Is an Artifact of the N-Terminal Yellow Fluorescent Protein Tag. J Bacteriol 194: 6382-6386.
77. Huang KC, Mukhopadhyay R, Wen B, Gitai Z, Wingreen NS, (2008) Cell shape and cell-wall organization in Gram-negative bacteria. Proc Natl Acad Sci U S A 105: 19282-19287.
78. Furchtgott L, Wingreen NS, Huang KC, (2011) Mechanisms for maintaining cell shape in rod-shaped Gram-negative bacteria. Mol Microbiol 81: 340-353.
79. Jiang H, Si F, Margolin W, Sun SX, (2011) Mechanical control of bacterial cell shape. Biophys J 101: 327-335.
80. Riveline D, (2009) Explaining Lengths and Shapes of Yeast by Scaling Arguments. Plos One 4: e6205.
81. Minc N, Chang F, (2010) Electrical Control of Cell Polarization in the Fission Yeast Schizosaccharomyces pombe. Curr Biol 20: 710-716.