Microtubule organization requires cell cycle-dependent nucleation at dispersed cytoplasmic sites: Polar and perinuclear microtubule organizing centers in the plant pathogen Ustilago maydis

Molecular Biology of the Cell

Volumn 14, Issue 2, 2003, Pages 642-657

  Straube, Anne ^a   Brill, Marianne ^a,d   Oakley, Berl R ^b   Horio, Tetsuya ^c   Steinberg, Gero ^a  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

^d Inst Med Mikrobiol Immunol/Hyg   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA TUBULIN; GREEN FLUORESCENT PROTEIN;

ARTICLE; CELL BUDDING; CELL CYCLE; CELL CYCLE G2 PHASE; CELL GROWTH; CELL NUCLEUS; CELL POLARITY; CENTROSOME; CONTROLLED STUDY; CYTOSOL; FUNGUS; GENE OVEREXPRESSION; IN VIVO STUDY; INTERPHASE; MICROTUBULE ASSEMBLY; MICROTUBULE ORGANIZING CENTER; MITOSIS; NONHUMAN; PATHOGENICITY; PLANT; PRIORITY JOURNAL; SPINDLE POLE BODY; USTILAGO MAYDIS;

ACTINS; CELL DIVISION; CELL NUCLEUS; CYTOPLASM; EPITOPES; G1 PHASE; GENOTYPE; GREEN FLUORESCENT PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; KINESIN; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MICROTUBULES; MITOSIS; MODELS, BIOLOGICAL; PHENOTYPE; PHYLOGENY; PLANT DISEASES; PLASMIDS; PROTEIN BINDING; RECOMBINATION, GENETIC; TIME FACTORS; TUBULIN; USTILAGO;

EUKARYOTA; FUNGI; USTILAGO MAYDIS;

EID: 0037329235     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-08-0513     Document Type: Article

References (65)

1. Banuett, F. (1995). Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu. Rev. Genet. 29, 179-208.
2. Banuett, F., and Herskowitz, I. (1989). Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc. Natl. Acad. Sci. USA 86, 5878-5882.
3. Barnes, G., Drubin, D.G., and Stearns, T. (1990). The cytoskeleton of Saccharomyces cerevisiae. Curr. Opin. Cell Biol. 2, 109-115.
4. Beinhauer, J.D., Hagan, I.M., Hegemann, J.H., and Fleig, U. (1997). Mal3, the fission yeast homologue of the human APC-interacting protein EB-1 is required for microtubule integrity and the maintenance of cell form. J. Cell Biol. 139, 717-728.
5. Berrueta, L., Kraeft, S.K., Tirnauer, J.S., Schuyler, S.C., Chen, L.B., Hill, D.E., Pellman, D., and Bierer, B.E. (1998). The adenomatous polyposis coli-binding protein EB1 is associated with cytoplasmic and spindle microtubules. Proc. Natl. Acad. Sci. USA 95, 10596-10601.
6. Bottin, A., Kämper, J., and Kahmann, R. (1996). Isolation of a carbon source-regulated gene from Ustilago maydis. Mol. Gen. Genet. 253, 342-352.
7. Centonze, V.E., and Borisy, G.G. (1990). Nucleation of microtubules from mitotic centrosomes is modulated by a phosphorylated epitope. J. Cell Sci. 95, 405-411.
8. Chabin-Brion, K., Marceiller, J., Perez, F., Settegrana, C., Drechou, A., Durand, G., and Pous, C. (2001). The Golgi complex is a microtubule-organizing organelle. Mol. Biol. Cell 12, 2047-2060.
9. Davis, F.M., Tsao, T.Y., Fowler, S.K., and Rao, P.N. (1983). Monoclonal antibodies to mitotic cells. Proc. Natl. Acad. Sci. USA 80, 2926-2930.
10. Desai, A., and Mitchison, T.J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell. Dev. Biol. 13, 83-117.
11. Felgner, H., Frank, R., and Schliwa, M. (1996). Flexural rigidity of microtubules measured with the use of optical tweezers. J. Cell Sci. 109, 509-516.
12. Felix, M.A., Antony, C., Wright, M., and Maro, B. (1994). Centrosome assembly in vitro: role of γ-tubulin recruitment in Xenopus sperm aster formation. J. Cell Biol. 124, 19-31.
13. Hagan, I.M. (1998). The fission yeast microtubule cytoskeleton. J. Cell Sci. 111, 1603-1612.
14. Hayles, J., and Nurse, P. (2001). A journey into space. Nat. Rev. Mol. Cell. Biol. 2, 647-656.
15. Heath, I.B. (1981). Nucleus associated organelles of fungi. Int. Rev. Cytol. 69, 191-221.
16. Heitz, M.J., Petersen, J., Valovin, S., and Hagan, I.M. (2001). MTOC formation during mitotic exit in fission yeast. J. Cell Sci. 114, 4521-4532.
17. Holliday, R. (1974). Ustilago maydis. In: Handbook of Genetics, ed. R.C. King, New York: Plenum Press.
18. Horio, T., Basaki, A., Takeoka, A., and Yamato, M. (1999). Lethal level overexpression of γ-tubulin in fission yeast causes mitotic arrest. Cell Motil. Cytoskeleton 44, 284-295.
19. Horio, T., Uzawa, S., Jung, M.K., Oakley, B.R., Tanaka, K., and Yanagida, M. (1991). The fission yeast γ-tubulin is essential for mitosis and is localized at microtubule organizing centers. J. Cell Sci. 99, 693-700.
20. Hyman, A., and Karsenti, E. (1998). The role of nucleation in patterning microtubule networks. J. Cell Sci. 111, 2077-2083.
21. Joshi, H.C. (1994). Microtubule organizing centers and γ-tubulin. Curr. Opin. Cell Biol. 6, 54-62.
22. Joshi, H.C., Palacios, M.J., McNamara, L., and Cleveland, D.W. (1992). Gamma-tubulin is a centrosomal protein required for cell cycle-dependent microtubule nucleation. Nature 356, 80-83.
23. Keating, T.J., Peloquin, J.G., Rodionov, V.I., Momcilovic, D., and Borisy, G.G. (1997). Microtubule release from the centrosome. Proc. Natl. Acad. Sci. USA 94, 5078-5083.
24. Keon, J.P., White, G.A., and Hargreaves, J.A. (1991). Isolation, characterization and sequence of a gene conferring resistance to the systemic fungicide carboxin from the maize smut pathogen Ustilago maydis. Curr. Genet. 19, 475-481.
25. Khodjakov, A., and Rieder, C.L. (1999). The sudden recruitment of γ-tubulin to the centrosome at the onset of mitosis and its dynamic exchange throughout the cell cycle, do not require microtubules. J. Cell Biol. 146, 585-596.
26. Kirschner, M.W. (1978). Microtubule assembly and nucleation. Int. Rev. Cytol. 54, 1-71.
27. Korinek, W.S., Copeland, M.J., Chaudhuri, A., and Chant, J. (2000). Molecular linkage underlying microtubule orientation toward cortical sites in yeast. Science 287, 2257-2259.
28. Kube-Granderath, E., and Schliwa, M. (1997). Unusual distribution of γ-tubulin in the giant fresh water amoeba Reticulomyxa filosa. Eur. J. Cell Biol. 72, 287-296.
29. Kumar, S., Tamura, K., Jakobsen, I.B., and Nei, M. (2001). MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244-1245.
30. Lee, L., Tirnauer, J.S., Li, J., Schuyler, S.C., Liu, J.Y., and Pellman, D. (2000). Positioning of the mitotic spindle by a cortical-microtubule capture mechanism. Science 287, 2260-2262.
31. Leguy, R., Melki, R., Pantaloni, D., and Carlier, M.F. (2000). Monomeric γ-tubulin nucleates microtubules. J. Biol. Chem. 275, 21975-21980.
32. Lupas, A., Van Dyke, M., and Stock, J. (1991). Predicting coiled coils from protein sequences. Science 252, 1162-1164.
33. Martin, M.A., Osmani, S.A., and Oakley, B.R. (1997). The role of γ-tubulin in mitotic spindle formation and cell cycle progression in Aspergillus nidulans. J. Cell Sci. 110, 623-633.
34. Masuda, H., Sevik, M., and Cande, W.Z. (1992). In vitro microtubule-nucleating activity of spindle pole bodies in fission yeast Schizosaccharomyces pombe: cell cycle-dependent activation in xenopus cell-free extracts. J. Cell Biol. 117, 1055-1066.
35. McDonald, A.R., Liu, B., Joshi, H.C., and Palevitz, B.A. (1993). Gamma-tubulin is associated with a cortical-microtubule-organizing zone in the developing guard cells of Allium cepa L. Planta 191, 357-361.
36. Meads, T., and Schroer, T.A. (1995). Polarity and nucleation of microtubules in polarized epithelial cells. Cell Motil. Cytoskeleton 32, 273-288.
37. Mimori-Kiyosue, Y., Shiina, N., and Tsukita, S. (2000). The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr. Biol. 10, 865-868.
38. Morrison, E.E., Wardleworth, B.N., Askham, J.M., Markham, A.F., and Meredith, D.M. (1998). EB1, a protein which interacts with the APC tumor suppressor, is associated with the microtubule cytoskeleton throughout the cell cycle. Oncogene 17, 3471-3477.
39. Muresan, V., Joshi, H.C., and Besharse, J.C. (1993). Gamma-tubulin in differentiated cell types: localization in the vicinity of basal bodies in retinal photoreceptors and ciliated epithelia. J. Cell Sci. 104, 1229-1237.
40. Nabi, I.R. (1999). The polarization of the motile cell. J. Cell Sci. 112, 1803-1811.
41. Oakley, B.R. (2000). An abundance of tubulins. Trends Cell Biol. 10, 537-542.
42. Oakley, C.E., and Oakley, B.R. (1989). Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338, 662-664.
43. Oakley, B.R., Oakley, C.E., Yoon, Y., and Jung, M.K. (1990). Gamma-tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell 61, 1289-1301.
44. Ovechkina, Y., and Oakley, B.R. (2001). Gamma tubulin in plant cells. Methods Cell Biol. 67, 195-212.
45. Paluh, J.L., Nogales, E., Oakley, B.R., McDonald, K., Pidoux, A.L., and Cande, W.Z. (2000). A mutation in γ-tubulin alters microtubule dynamics and organization and is synthetically lethal with the kinesin-like protein pk11p. Mol. Biol. Cell 11, 1225-1239.
46. Sambrooke, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
47. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schaefer, W., Martin, T., Herskowitz, I., and Kahmann, R. (1990). The B alleles of Ustilago maydis whose combinations program pathogenic development code for polypeptides containing a homeodomain-related motif. Cell 60, 295-306.
48. Snetselaar, K.M., and McCann, M.P. (1997). Using microdensitometry to correlate cell morphology with the nuclear cycle in Ustilago maydis. Mycologia 89, 689-697.
49. Spellig, T., Bottin, A., and Kahmann, R. (1996). Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol. Gen. Genet. 252, 503-509.
50. Steinberg, G., Wedlich-Soldner, R., Brill, M., and Schulz, I. (2001). Microtubules in the fungal pathogen Ustilago maydis are highly dynamic and determine cell polarity. J. Cell Sci. 114, 609-622.
51. Straube, A., Enard, W., Berner, A., Wedlich-Soldner, R., Kahmann, R., and Steinberg, G. (2001). A split motor domain in a cytoplasmic dynein. EMBO J. 20, 5091-5100.
52. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
53. Tirnauer, J.S., and Bierer, B.E. (2000). EB1 proteins regulate microtubule dynamics, cell polarity, and chromosome stability. J. Cell Biol. 149, 761-766.
54. Tirnauer, J.S., O'Toole, E., Berrueta, L., Bierer, B.E., and Pellman, D. (1999). Yeast Bim1p promotes the G1-specific dynamics of microtubules. J. Cell Biol. 145, 993-1007.
55. Tran, P.T., Marsh, L., Doye, V., Inoue, S., and Chang, F. (2001). A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J. Cell Biol. 153, 397-411.
56. Vaughn, K.C., and Harper, J.D. (1998). Microtubule-organizing centers and nucleating sites in land plants. Int. Rev. Cytol. 181, 75-149.
57. Verde, F., Labbe, J.C., Doree, M., and Karsenti, E. (1990). Regulation of microtubule dynamics by Cdc2 protein kinase in cell-free extracts of Xenopus eggs. Nature 343, 233-238.
58. Vogel, J., Drapkin, B., Oomen, J., Beach, D., Bloom, K., and Snyder, M. (2001). Phosphorylation of γ-tubulin regulates microtubule organization in budding yeast. Dev. Cell 1, 621-631.
59. Vorobjev, I., Malikov, V., and Rodionov, V. (2001). Self-organization of a radial microtubule array by dynein-dependent nucleation of microtubules. Proc. Natl. Acad. Sci. USA 98, 10160-10165.
60. Vorobjev, I.A., Svitkina, T.M., and Borisy, G.G. (1997). Cytoplasmic assembly of microtubules in cultured cells. J. Cell Sci. 110, 2635-2645.
61. Waterman-Storer, C.M., and Salmon, E.D. (1997). Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J. Cell Biol. 139, 417-434.
62. Wedlich-Soldner, R., Bolker, M., Kahmann, R., and Steinberg, G. (2000). A putative endosomal t-SNARE links exo- and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J. 19, 1974-1986.
63. Wedlich-Soldner, R., Straube, A., Friedrich, M.W., and Steinberg, G. (2002). A balance of KIF1A-like kinesin and dynein organizes early endosomes in the fungus Ustilago maydis. EMBO J. 21, 2946-2957.
64. Wiese, C., and Zheng, Y. (2000). A new function for the γ-tubulin ring complex as a microtubule minus-end cap. Nat. Cell Biol. 2, 358-364.
65. Yvon, A.M., and Wadsworth, P. (1997). Non-centrosomal microtubule formation and measurement of minus end microtubule dynamics in A498 cells. J. Cell Sci. 110, 2391-2401.