1887

Abstract

Organization of the cytoskeleton was studied in the ascomycetous black yeast , an opportunistic human pathogen, in an effort to present it as a potential target of antifungal therapy. Long cytoplasmic microtubules, extending along the hyphae from the base to the growing apex, were the dominant structures in multinucleate interphase cells. Before mitosis these microtubules disappeared and were replaced by intranuclear spindles. This reorganization of microtubules occurred along the whole length of hypha before synchronous division of the nuclei. Actin cytokinetic rings were rarely seen. Cortical actin in the form of patches accumulated in areas of cell wall growth, i.e. in the hyphal apex and near the occasionally formed septum. Actin cables were not seen. During synchronous conidiogenesis, the cytoplasmic microtubules extended along developing conidia, and actin patches lined their subcortical areas. Actin rings were formed regularly at the base of uninuclear conidia. Microtubule inhibitor methyl benzimidazol-2-ylcarbamate disintegrated the microtubules, and inhibited nuclear division, development of hyphae and conidiogenesis. Actin inhibitor Cytochalasin D induced swelling of hyphal apexes and developing conidia. This inhibitory activity ceased after 5 to 12 h when the occasional septa appeared and conidiogenesis was completed. The lack of unicellular organization in multinucleate hyphae of seems be related to a rarity of F-actin structures: i.e. absence of actin cables, the lack of actin cytokinetic rings in particular, resulting in the uncoupling of the nuclear division from cytokinesis; the association of both processes is, however, retained during conidiogenesis.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26006-0
2003-04-01
2020-01-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/4/mic149865.html?itemId=/content/journal/micro/10.1099/mic.0.26006-0&mimeType=html&fmt=ahah

References

  1. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. & Walter, P. ( 2002; ). Molecular Biology of the Cell, 4th edn. New York: Taylor & Francis.
  2. Balasubramanian, M. K., McCollum, D. & Surana, U. ( 2000; ). Tying the knot: linking cytokinesis to the nuclear cycle. J Cell Sci 113, 1503–1513.
    [Google Scholar]
  3. Botstein, D., Amberg, D., Mulholland, J., Huffaker, T., Adams, A., Drubin, D. & Stearns, T. ( 1997; ). The yeast cytoskeleton. In The Molecular and Cell Biology of the Yeast Saccharomyces cerevisiae, pp. 1–90. Edited by J. R. Broach, J. R. Pringle & E. W. Jones. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  4. Bracker, C. E. ( 1967; ). Ultrastructure of fungi. Annu Rev Phytopathol 5, 343–374.[CrossRef]
    [Google Scholar]
  5. Brunner, D. & Nurse, P. ( 2000; ). New concepts in fission yeast morphogenesis. Philos Trans R Soc Lond B Biol Sci 355, 873–877.[CrossRef]
    [Google Scholar]
  6. Butt, T. M. & Heath, I. B. ( 1988; ). The changing distribution of actin and nuclear behaviour during the cell cycle of the mite-pathogenic fungus Neozygites sp. Eur J Cell Biol 46, 499–505.
    [Google Scholar]
  7. Cavalier-Smith, T. ( 1993; ). Kingdom Protozoa and its 18 phylla. Microbiol Rev 57, 953–994.
    [Google Scholar]
  8. Cavalier-Smith, T. ( 1998; ). A revised six-kingdom system of life. Biol Rev 73, 203–266.[CrossRef]
    [Google Scholar]
  9. Cid, V. J., Jiménez, J., Molina, M., Sánchez, M., Nombela, C. & Thorner, J. W. ( 2002; ). Orchestrating the cell cycle in yeast: sequential localization of key mitotic regulators at the spindle pole and the bud neck. Microbiology 148, 2647–2659.
    [Google Scholar]
  10. Coskey, R. J., Mehregan, A. H., Rippon, J. H. & Wood, D. ( 1983; ). Implantation with phaeomycotic contamination. J Am Acad Dermatol 8, 428–429.[CrossRef]
    [Google Scholar]
  11. De Bary, A. ( 1866; ). Morphologie und Physiologie der Pilze, Flechten und Myxomyceten. Leipzig: Engelmann.
  12. De Hoog, G. S. ( 1998; ). A key to the anamorph genera of yeastlike Archi- and Euascomycetes. In The Yeasts. A Taxonomic Study, 4th edn, pp.123–125. Edited by C. P. Kurtzman & J. W. Fell. Amsterdam: Elsevier.
  13. Fischer, R. ( 1999; ). Nuclear movement in filamentous fungi. FEMS Microbiol Rev 23, 39–68.[CrossRef]
    [Google Scholar]
  14. Fuller, M. S. ( 1976; ). Mitosis in fungi. Int Rev Cytol 45, 113–153.
    [Google Scholar]
  15. Gabriel, M. ( 1983; ). Karyokinesis and cell septum formation during incomplete cell wall regeneration in flattened Schizosaccharomyces versatilis protoplasts. In Progress in Cell Cycle Controls (6th European Cell Cycle Workshop), pp. 144–146. Editored by J. Chaloupka, A. Kotyk & E. Streiblová. Prague: Institute of Microbiology, Academy of Sciences.
  16. Gabriel, M. ( 1984; ). Karyokinesis and septum formation during the regeneration of incomplete cell walls in protoplasts of Schizosaccharomyces japonicus var. versatilis: a time-lapse microcinematographic study. J Gen Microbiol 130, 625–630.
    [Google Scholar]
  17. Gabriel, M. & Kopecká, M. ( 1992; ). Single mutation in the actin gene can dissociate nuclear division from cytokinesis in the cell cycle of budding yeast. Yeast 8, S537.
    [Google Scholar]
  18. Gabriel, M. & Kopecká, M. ( 1995; ). Disruption of the actin cytoskeleton in budding yeast results in formation of an aberrant cell wall. Microbiology 141, 891–899.[CrossRef]
    [Google Scholar]
  19. Gabriel, M., Horký, D., Svoboda, A. & Kopecká, M. ( 1998; ). Cytochalasin D interferes with contractile actin ring and septum formation in Schizosaccharomyces japonicus var. versatilis. Microbiology 144, 2331–2344.[CrossRef]
    [Google Scholar]
  20. Geitmann, A. & Emons, A. M. C. ( 2000; ). The cytoskeleton in plant and fungal tip growth. J Microsc 198, 218–245.[CrossRef]
    [Google Scholar]
  21. Georgopapadakou, N. H. & Walsh, T. J. ( 1994; ). Human mycoses: drugs and targets for emerging pathogens. Science 264, 371–373.[CrossRef]
    [Google Scholar]
  22. Giradi, L. S., Malowitz, R., Tortora, G. T. & Spitzer, E. D. ( 1993; ). Aureobasidium pullulans septicaemia. Clin Infect Dis 16, 338–339.
    [Google Scholar]
  23. Grove, S. N. & Bracker, C. E. ( 1970; ). Protoplasmic organization of hyphal tips among fungi: vesicles and Spitzenkörper. J Bacteriol 104, 989–1009.
    [Google Scholar]
  24. Hagan, I. M. ( 1998; ). The fission yeast microtubule cytoskeleton. J Cell Sci 111, 1603–1612.
    [Google Scholar]
  25. Heath, I. B. ( 1990; ). The roles of actin in tip growth of fungi. Int Rev Cytol 123, 95–127.
    [Google Scholar]
  26. Heath, I. B. ( 1994; ). The cytoskeleton in hyphal growth, organelle movements and mitosis. In The Mycota, vol. 1, pp. 43–65. Edited by J. G. H. Wessels & O. Meindhardt. Berlin: Springer.
  27. Heath, I. B. ( 2000; ). Organization and functions of actin in hyphal tip growth. In Actin: a Dynamic Framework for Multiple Plant Cell Functions, pp. 275–300. Edited by C. J. Staiger and others. The Netherlands: Kluwer Academic.
  28. Heath, I. B. & Harold, R. L. ( 1992; ). Actin has multiple roles in the formation and architecture of zoospores of the oomycetes, Saprolegnia ferax and Achlya bisexualis. J Cell Sci 102, 611–627.
    [Google Scholar]
  29. Heath, I. B., Gupta, G. & Bai, S. ( 2000; ). Plasma membrane-adjacent actin filaments, but not microtubules, are essential for both polarization and hyphal tip morphogenesis in Saprolegnia ferax and Neurospora crassa. Fungal Genet Biol 30, 45–62.[CrossRef]
    [Google Scholar]
  30. Ishiguro, J. ( 1998; ). Genetic control of fission yeast cell wall synthesis: the genes involved in wall biogenesis and their interactions in Schizosaccharomyces pombe. Genes Genet Syst 73, 181–191.[CrossRef]
    [Google Scholar]
  31. Ishiguro, J. & Kobayashi, W. ( 1996; ). An actin point-mutation neighboring the ‘hydrophobic plug’ causes defects in the maintenance of cell polarity and septum organization in the fission yeast Schizosaccharomyces pombe. FEBS Letters 392, 237–241.[CrossRef]
    [Google Scholar]
  32. Kopecká, M. & Gabriel, M. ( 1998; ). The aberrant positioning of nuclei and the microtubular cytoskeleton in Saccharomyces cerevisiae due to improper actin function. Microbiology 144, 1783–1797.[CrossRef]
    [Google Scholar]
  33. Kopecká, M., Hata, K. & Takeo, K. ( 1998; ). Searching for an actin cytoskeleton in Aureobasidium pullulans. In Proceedings of the 6th International Symposium of the Mycological Society of Japan (1998 Japan–UK International Mycological Symposium), p. 57. Japan: Chiba University.
  34. Kopecká, M., Gabriel, M., Takeo, K., Yamaguchi, M., Svoboda, A., Ohkusu, M., Hata, K. & Yoshida, S. ( 2001; ). Microtubules and actin cytoskeleton in Cryptococcus neoformans compared with ascomycetous budding and fission yeasts. Eur J Cell Biol 80, 303–311.[CrossRef]
    [Google Scholar]
  35. Koppans, H. S., Olsen, I., Stuge, U. & Sandven, P. ( 1991; ). Aureobasidium infection of the jaw. J Oral Pathol 20, 191–195.[CrossRef]
    [Google Scholar]
  36. Kwon-Chung, K. J. & Bennet, J. E. ( 1992; ). Medical Mycology. Philadelphia: Lea & Febiger.
  37. Laskin, A. I. & Lechevalier, H. A. ( 1978; ). CRC Handbook of Microbiology, vol. II, 2nd edn. Boca Raton, FL: CRC Press.
  38. Le Goff, X., Utzig, S. & Simanis, V. ( 1999; ). Controlling septation in fission yeast: finding the middle, and timing it right. Curr Genet 35, 571–584.[CrossRef]
    [Google Scholar]
  39. Li, J. & Heath, I. B. ( 1994; ). The behaviour of F-actin during the zoosporic phases of the chytridiomycete gut fungi Neocallimastix and Orphinomyces. Exp Mycol 18, 57–69.[CrossRef]
    [Google Scholar]
  40. May, K. M. & Hyams, J. S. ( 1998; ). The yeast cytoskeleton: the closer we look, the more we see. Fungal Genet Biol 24, 110–122.[CrossRef]
    [Google Scholar]
  41. McCollum, D. & Gould, K. L. ( 2001; ). Timing is everything: regulation of mitotic exit and cytokinesis by the MEN and SIN. Trends Cell Biol 11, 89–95.[CrossRef]
    [Google Scholar]
  42. Mehregan, A. H. & Rudner, E. J. ( 1980; ). Implantation dermatosis: wood splinter with fungus contamination. J Cutan Pathol 7, 330–331.[CrossRef]
    [Google Scholar]
  43. Nakaseko, Y. & Yanagida, M. ( 2001; ). Cell biology: cytoskeleton in the cell cycle. Nature 412, 291–292.[CrossRef]
    [Google Scholar]
  44. Nelken, N., Ignatius, J., Skinner, M. & Christensen, N. ( 1987; ). Changing clinical spectrum of splenic abscess. A multicenter study and review of the literature. Am J Surg 154, 27–34.[CrossRef]
    [Google Scholar]
  45. Nishimura, K., Miyaji, M., Takeo, K., Mikami, Y., Kamei, K., Yokoyama, K. & Tanaka, R. ( 1998; ). IFM List of Pathogenic Fungi and Actinomycetes with Photomicrographs. Chiba, Japan: Culture Collection Research Center for Pathogenic Fungi and Microbial Toxicoses.
  46. Novick, P. & Botstein, D. ( 1985; ). Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell 40, 405–416.[CrossRef]
    [Google Scholar]
  47. Oakley, B. R. ( 2000; ). An abundance of tubulins. Trends Cell Biol 10, 537–542.[CrossRef]
    [Google Scholar]
  48. Pringle, J. R., Preston, R. A., Adams, A. E. M., Stearns, T., Drubin, D. G., Haarer, B. K. & Jones, W. E. ( 1989; ). Fluorescence microscopy methods for yeasts. Methods Cell Biol 31, 375–435.
    [Google Scholar]
  49. Pruyne, D. & Bretscher, A. ( 2000a; ). Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J Cell Sci 113, 365–375.
    [Google Scholar]
  50. Pruyne, D. & Bretscher, A. ( 2000b; ). Polarization of cell growth in yeast. II. The role of the cortical actin cytoskeleton. J Cell Sci 113, 571–585.
    [Google Scholar]
  51. Redondo-Bellon, P., Idoate, M., Rubio, M. & Herrero, J. I. ( 1997; ). Chromoblastomycosis produced by Aureobasidium pullulans in an immunosuppressed patient. Arch Dermatol 133, 663–664.[CrossRef]
    [Google Scholar]
  52. Rippon, J. W. ( 1982; ). Medical Mycology, 5th edn. Philadelphia, PA: W. E. Saunders.
  53. Svoboda, A., Bähler, 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.[CrossRef]
    [Google Scholar]
  54. Takeo, K. & de Hoog, G. S. ( 1991; ). Karyology and hyphal character as taxonomic criteria in ascomycetous black yeasts and related fungi. Antonie Van Leeuwenhoek 60, 35–42.[CrossRef]
    [Google Scholar]
  55. Tram, U., Riggs, B. & Sullivan, W. ( 2001; ). Cleavage and gastrulation in Drosophila embryos. In Encyclopedia of Life Sciences, pp. 1–7. London: Macmillan Publishers & Nature Publishing Group.
  56. Wainright, P. O., Hinkle, G., Sogin, M. L. & Stickel, S. K. ( 1993; ). Monophyletic origins of the metazoa: an evolutionary link with fungi. Science 260, 340–342.[CrossRef]
    [Google Scholar]
  57. Winsor, B. & Schiebel, E. ( 1997; ). An overview of the Saccharomyces cerevisiae microtubule and microfilament cytoskeleton. Yeast 13, 399–434.[CrossRef]
    [Google Scholar]
  58. Woods, A., Sherwin, T., Sasse, R., MacRae, 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]
  59. Yamaguchi, M., Miyatsu, Y., Horikawa, Y., Sugahara, K., Mizokami, H., Kawase, M. & Tanaka, H. ( 1994; ). Dynamics of hepatitis B virus core antigen in a transformed yeast cell: analysis with an inducible system. J Electron Microsc 43, 386–393.
    [Google Scholar]
  60. Yokoyama, K., Kaji, H., Nishimura, K. & Miyaji, M. ( 1990; ). The role of microfilaments and microtubules in apical growth and dimorphism of Candida albicans. J Gen Microbiol 136, 1067–1075.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26006-0
Loading
/content/journal/micro/10.1099/mic.0.26006-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error