Cytochalasin D interferes with contractile actin ring and septum formation in Schizosaccharomyces japonicus var. versatilis Free

Abstract

The cells of var. responded to the presence of cytochalasin D (CD), an inhibitor of actin polymerization, by the disappearance of contractile actin rings (ARs) that had already formed and by inhibition of new ring formation. Actin cables disappeared. Actin patches remained preserved and became co-localized with regions of actual cell wall formation (at cell poles and at the site of septum development). Removal of the AR arrested formation of the primary septum and led to the production of aberrant septum protrusions in that region. Nuclear division was accomplished in the presence of CD but new ARs were not produced. The wall (septum) material was deposited in the form of a wide band at the inner surface of the lateral cell wall in the cell centre. This layer showed a thin fibrillar structure. The removal of CD resulted in rapid formation of new ARs in the equatorial region of the cells. This implies that the signal for AR localization was not abolished either by CD effects or by removal of an AR already formed. Some of the newly developed ARs showed atypical localization and orientation. In addition, redundant, subcortically situated actin bundles were produced. The removal of CD was quickly followed by the development of primary septa co-localized with ARs. Wall protrusions occurred co-localized with the redundant actin bundles. If these were completed in a circle, redundant septa developed. The AR is a mechanism which, in time and space, triggers cytokinesis by building a septum sequentially dependent on the AR. Aberrant septa were not capable of separating daughter cells. However, non-separated daughter cells subsequently gave rise to normal cells.

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1998-08-01
2024-03-28
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References

  1. Adams A.E.M., Pringle J.R. 1984; Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic mutant Saccharomyces cerevisiae.. J Cell Biol 98:934–943
    [Google Scholar]
  2. Akashi T., Kanbe T., Tanaka K. 1994; The role of the actin cytoskeleton in the polarized growth of the germ tube in Candida albicans.. Microbiology 140:271–280
    [Google Scholar]
  3. Alfa C.E., Hyams J.S. 1990; Distribution of tubulin and actin through the cell division cycle of the fission yeast Schizo- saccharomyces japonicus var. versatilis: a comparison with Schizosaccharomyces pombe.. J Cell Sci 96:71–77
    [Google Scholar]
  4. Balasubramanian M.K., Helfman D.M., Hemmingsen S.M. 1992; A new tropomyosin essential for cytokinesis in the fission yeast S. pombe.. Nature 360:84–87
    [Google Scholar]
  5. Balasubramanian M.K., Hirani B.R., Burke J.D., Gould K.L. 1994; The Schizosaccharomyces pombe cdc-3 gene encodes a profilin essential for cytokinesis.. J Cell Biol 125:1289–1301
    [Google Scholar]
  6. Barja F., Turian G. 1994; Cytochalasin B-sensitive actin- mediated nuclear RNA export in germinating conidia of Neuro- spora crassa.. Cell Biol Int 18:903–906
    [Google Scholar]
  7. Boone Ch., Sommer S.S., Hensel A., Bussey H. 1990; Yeast KRE genes provide evidence for a pathway of cell wall yS-glucan assembly.. J Cell Biol 110:1833–1843
    [Google Scholar]
  8. Cabib E., Drgoň T., Drgoňoá J., Ford R.A., Kollár R. 1997; The yeast cell wall, a dynamic structure engaged in growth and morphogenesis.. Biochem Soc Trans 25:200–204
    [Google Scholar]
  9. Chang F., Nurse P. 1996; How fission yeast fission in the middle.. Cell 84:191–194
    [Google Scholar]
  10. Chang F., Woollard A., Nurse P. 1996; Identification and characterization of fission yeast mutants defective in contractile actin ring assembly.. J Cell Sci 109:131–142
    [Google Scholar]
  11. Chang F., Drubin D., Nurse P. 1997; cdcl2p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin.. J Cell Biol 137:169–182
    [Google Scholar]
  12. Cid V.J., Durán A., Del Rey F., Snyder M.P., Nombela C., Sánchez D. 1995; Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae.. Microbiol Rev 59:345–386
    [Google Scholar]
  13. Doyle T., Botstein D. 1996; Movement of cortical actin cytoskeleton visualized in vivo.. Proc Natl Acad Sci USA 93:3886–3891
    [Google Scholar]
  14. Fankhauser Ch., Simanis V. 1994; The cdc7 protein kinase: a dosage-dependent regulator of septum formation in fission yeast.. EMBO J 13:3011–3019
    [Google Scholar]
  15. Fankhauser Ch., Marks J., Reymond A., Simanis V. 1993; TheS. pombe cdcl6 gene is required both for maintenance of p34cdc2 kinase activity and regulation of septum formation: a link between mitosis and cytokinesis ?. EMBO J 12:2697–2704
    [Google Scholar]
  16. Fankhauser Ch., Reymond A., Cerutti L., Utzig S., Hofmann K., Simanis V. 1995; The S. pombe cdcl5 gene is a key element in the reorganization of F-actin at mitosis.. Cell 82:435–444
    [Google Scholar]
  17. Fishkind D.J., Wang Y. 1995; New horizons for cytokinesis.. Curr Opin Cell Biol 7:23–31
    [Google Scholar]
  18. Fujiwara M., Horiuchi H., Ohta A., Takagi M. 1997; A novel fungal gene encoding chitin synthase with a myosin motor-like domain.. Biochem Biophys Res Commun 236:75–78
    [Google Scholar]
  19. Gabriel M., Kopecká D. 1995; Disruption of the actincytoskeleton in budding yeast results in formation of an aberrant cell wall.. Microbiology 141:891–899
    [Google Scholar]
  20. Glover D.M., Ohkura H., Tavares A. 1996; Polo kinase: the choreographer of the mitotic stage?. J Cell Biol 135:1681–1684
    [Google Scholar]
  21. Hašpek J., Svobodová J., Streiblová E. 1986; Immunofluorescence of the microtubular skeleton in growing and drug treated yeast protoplasts.. Eur J Cell Biol 41:150–156
    [Google Scholar]
  22. Inoue S.B., Takewaki N., Takasuka T., Mio T., Adachi M., Fujii Y., Miyamoto C., Arisawa M., Furuichi Y., Watanabe T. 1995; Characterization and gene cloning of l,3-β-D-glucan synthase from Saccharomyces cerevisiae.. Eur J Biochem 231:845–854
    [Google Scholar]
  23. Inoue S.B., Qadota H., Arisawa M., Anraku Y., Watanabe T., Ohya Y. 1996; Signaling toward yeast 1,3-β-glucan synthesis.. Cell Struct Fund 21:395–402
    [Google Scholar]
  24. Ishiguro J., Kobayashi W. 1996; An actin point-mutation neighboring the ‘hydrophobic plug’ causes defects in the main-tenance of cell polarity and septum organization in the fission yeast Schizosaccharomyces pombe.. FEBS Lett 392:237–241
    [Google Scholar]
  25. Kanbe T., Kobayashi I., Tanaka K. 1989; Dynamics of cytoplasmic organelles in the cell cycle of the fission yeast Schizosaccharomyces pombe: three-dimensional reconstruction from serial sections.. J Cell Sci 94:647–656
    [Google Scholar]
  26. Kanbe T., Akashi T., Tanaka K. 1993; The effect of cytochalasin A on actin distribution in the fission yeast Schizo-saccharomyces pombe studied by fluorescence and electron microscopy.. Protoplasma 176:24–32
    [Google Scholar]
  27. Kanbe T., Akashi T., Tanaka K. 1994; Changes in the distribution of F-actin in the fission yeast Schizosaccharomyces pombe by arresting growth in distilled water: correlative studies with fluorescence and electron microscopy.. J Electron Microsc 43:20–24
    [Google Scholar]
  28. Kilmartin J.V., Adams A.E.M. 1984; Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces.. J Cell Biol 98:922–933
    [Google Scholar]
  29. Klis F.M., Caro L.H.P., Vossen J.H., Kapteyn J.C., Ram A.F.J., Montijn R.C., Van Berkel M.A.A., Van Den Ende H. 1997; Identification and characterization of a major building block in the cell wall of Saccharomyces cerevisiae.. Biochem Soc Trans 25:856–860
    [Google Scholar]
  30. Kobori H., Yamada N., Taki A., Osumi M. 1989; Actin is associated with the formation of the cell wall in reverting protoplasts of the fission yeast Schizosaccharomyces pombe.. J Cell Sci 94:635–646
    [Google Scholar]
  31. Kobori H., Sato M., Osumi M. 1992; Relationship of actin organization to growth in the two forms of the dimorphic yeast Candida tropicalis.. Protoplasma 167:193–204
    [Google Scholar]
  32. Kobori H., Toda T., Yaguchi H., Toya M., Yanagida M., Osumi M. 1994; Fission yeast protein kinase C gene homologues are required for protoplast regeneration: a functional link between cell wall formation and cell shape control . J Cell Sci 107:1131–1136
    [Google Scholar]
  33. Kopecká M., Fleet G.H., Phaff H.J. 1995; Ultrastructure of the cell wall of Schizosaccharomyces pombe following treatment with various glucanases.. J Struct Biol 114:140–152
    [Google Scholar]
  34. Kumada K., Su S., Yanagida M., Toda T. 1995; Fission yeast TPR-family protein nuc2 is required for G 1-arrest upon nitrogen starvation and is an inhibitor of septum formation.. J Cell Sci 108:895–905
    [Google Scholar]
  35. McCollum D., Balasubramanian M.K., Pelcher L.E., Hemmingsen S.M., Gould K.L. 1995; Schizosaccharomyces pombe cdc4 + gene encodes a novel EF-hand protein essential for cytokinesis.. J Cell Biol 130:651–660
    [Google Scholar]
  36. McCollum D., Feoktistova A., Morphew M., Balasubramanian M., Gould K.L. 1996; The Schizosaccharomyces pombe actin- related protein, Arp3, is a component of the cortical actin cytoskeleton and interacts with profilin.. EMBO J 15:6438–6446
    [Google Scholar]
  37. Marks J., Hyams J.S. 1985; Localization of F-actin through the cell division cycle of Schizosaccharomyces pombe.. Eur J Cell Biol 39:27–32
    [Google Scholar]
  38. Marks J., Hagan I.M., Hyams J.S. 1986; Growth polarity and cytokinesis in fission yeast: the role of the cytoskeleton.. J Cell Sci (Suppl) 5:229–241
    [Google Scholar]
  39. Marks J., Hagan I.M., Hyams J.S. 1987; Spatial association of F-actin with growth polarity and septation in the fission yeast Schizosaccharomyces pombe. . In Spatial Organization in Eukaryotic Microbes pp. 119–135 Poole R.K., Trinci A.P.J. Edited by Oxford: IRL Press;
    [Google Scholar]
  40. Marks J., Fankhauser C., Simanis V. 1992; Genetic interactions in the control of septation in Schizosaccharomyces pombe.. J Cell Sci 101:801–808
    [Google Scholar]
  41. Mateos P., Domínguez A. 1991; Ultrastructure and cell wall composition in cell division cycle mutants of Schizo-saccharomyces pombe deficient in septum formation.. Antonie Leeuwenhoek 59:155–165
    [Google Scholar]
  42. Mertins P., Gallwitz D. 1987; A single intronless actin gene in the fission yeast Schizosaccharomyces pombe-, nucleotide sequence and transcripts formed in homologous and heterologous yeast.. Nucleic Acids Res 15:7369–7379
    [Google Scholar]
  43. Minet M., Nurse P., Thuriaux P., Mitchison J.M. 1979; Uncontrolled septation in cell division cycle mutant of the fission yeast Schizosaccharomyces pombe.. J Bacteriol 137:440–446
    [Google Scholar]
  44. Mulholland J., Preuss D., Moon A., Drubin D., Botstein D. 1994; Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane.. J Cell Biol 125:381–391
    [Google Scholar]
  45. Novick P., Botstein D. 1985; Phenotypic analysis of tem-perature sensitive yeast actin mutants.. Cell 40:405–416
    [Google Scholar]
  46. Nurse P., Thuriaux P., Nasmyth K. 1976; Genetic control of the cell cycle in the fission yeast Schizosaccharomyces pombe.. Mol Gen Genet 146:167–178
    [Google Scholar]
  47. Ohkura H., Hagan J.M., Glover D.M. 1995; The conserved Schizosaccharomyces pombe kinase plo 1, required to form a bipolar spindle, the actin ring, and septum, can drive septum formation in G(l) and G(2) cells.. Genes Dev 9:1059–1073
    [Google Scholar]
  48. Pringle J.R. 1991; Staining of bud scars and other cell wall chitin with calcofluor.. Methods Enzymol 194:732–735
    [Google Scholar]
  49. Pringle J.R., Preston R.A., Adams A.E.M., Stearns T., Drubin D.G., Harrer B.K., Jones W.E. 1989; Fluorescence microscopy methods for yeasts.. Methods Cell Biol 31:357–435
    [Google Scholar]
  50. Robinow C.F., Hyams J.S. 1989; General cytology of fission yeast.. In The Molecular Biology of the Fission Yeast pp. 273–331 Nasim A., Young P., Johnson B.F. Edited by New York: Academic Press;
    [Google Scholar]
  51. Sampath P., Pollard T.D. 1991; Effect of cytochalasin, phalloidin, and pH on the elongation of actin filaments.. Biochemistry 30:1973–1980
    [Google Scholar]
  52. Satterwhite L.L., Pollard T.D. 1992; Cytokinesis.. Curr Opin Cell Biol 4:43–52
    [Google Scholar]
  53. Schekman R., Novick P. 1982; The secretory process and yeast cell-surface assembly.. In The Molecular Biology of the Yeast Saccharomyces 2 Metabolism and Gene Expression pp. 361–398 Strathern J.N., Jones E.W., Broach J.R. Edited by Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  54. Schmidt S., Sohrmann M., Hofmann K., Woollard A., Simanis V. 1997; The spglp GTPase is an essential, dosage-dependent inducer of septum formation in Schizosaccharomyces pombe.. Genes Dev 11:1519–1534
    [Google Scholar]
  55. Shaw J.A., Mol P.C., Bowers B., Silverman S.J., Valdivieso M.H., Durán A., Cabib E. 1991; The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle.. J Cell Biol 114:111–123
    [Google Scholar]
  56. Shematek E.M., Cabib E. 1980; Biosynthesis of the yeast cell wall. II. Regulation of β-(l→3) glucan synthetase by ATP and GTP.. J Biol Chem 255:895–902
    [Google Scholar]
  57. Sietsma J.H., Wessels J.G.H. 1990; The occurrence of glucosaminoglycan in the wall of Schizosaccharomyces pombe.. J Gen Microbiol 136:2261–2265
    [Google Scholar]
  58. Simanis V. 1995; The control of septum formation and cytokinesis in fission yeast.. Semin Cell Biol 6:79–87
    [Google Scholar]
  59. Sipiczki M., Grallert B., Miklos I. 1993; Mycelial and syncytial growth in Schizosaccharomyces pombe induced by novel sep- tation mutations.. J Cell Sci 104:485–493
    [Google Scholar]
  60. Sohrmann M., Fankhauser Ch., Brodbeck C., Simanis V. 1996; The dmfl/midi gene is essential for correct positioning of the division septum in fission yeast.. Genes Dev 10:2707–2719
    [Google Scholar]
  61. Solomon F. 1991; Analyses of the cytoskeleton in Saccharomyces cerevisiae.. Anna Rev Cell Biol 7:633–662
    [Google Scholar]
  62. Streiblová E., Hašek J., Jelke E. 1984; Septum pattern in ts mutants of Schizosaccharomyces pombe defective in genes cdc 3, cdc 4, cdc 8 and cdc 12.. J Cell Sci 69:47–65
    [Google Scholar]
  63. Svoboda A., Báhler J., Kohli J. 1995; Microtubule-driven nuclear movements and linear elements as meiosis-specific characteristics of the fission yeasts Schizosaccharomyces versatilis and Schizosaccharomyces pombe.. Chromosoma 104:203–214
    [Google Scholar]
  64. Waddle J.A., Karpova T.S., Waterson R.H., Cooper J.A. 1996; Movement of cortical actin patches in yeast.. J Cell Biol 132:861–870
    [Google Scholar]
  65. Welch M.D., Holtzman D.A., Drubin D.G. 1994; The yeast actin cytoskeleton.. Curr Opin Cell Biol 6:110–119
    [Google Scholar]
  66. Woods A., Sherwin T., Sasse R., McRae T.H., Baines A.J., Gull K. 1989; Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies.. J Cell Sci 93:491–500
    [Google Scholar]
  67. Wulf E., Deboben A., Bautz F.A., Faulstich H., Wieland T. 1979; Fluorescent phallotoxin, a tool for the visualisation of cellular actin.. Proc Natl Acad Sci USA 76:4498–4502
    [Google Scholar]
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