A mutation in γ-tubulin alters microtubule dynamics and organization and is synthetically lethal with the kinesin-like protein Pkl1p

Molecular Biology of the Cell

Volumn 11, Issue 4, 2000, Pages 1225-1239

  Paluh, Janet L ^a   Nogales, Eva ^a   Oakley, Berl R ^b   McDonald, Kent ^a   Pidoux, Alison L ^c   Cande, W Z ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA TUBULIN; KINESIN;

ARTICLE; CELL STRUCTURE; MICROSCOPY; MICROTUBULE ASSEMBLY; MITOSIS INHIBITION; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SACCHAROMYCES;

SACCHAROMYCES;

EID: 0034044992     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.4.1225     Document Type: Article

References (102)

1. Brinkley, B.R., and Cartwright, J., Jr. (1975). Cold-labile and cold-stable microtubules in the mitotic spindle of mammalian cells. Ann. NY Acad. Sci., 253, 428-439.
2. Burke, D., Gasdaska, P., and Hartwell, L. (1989). Dominant effects of tubulin overexpression in Saccharomyces cerevisiae. Mol. Cell. Biol. 9, 1049-1059.
3. Burns, R.G. (1995). Analysis of the γ-tubulin sequences: implications for the functional properties of γ-tubulin. J. Cell Sci. 108, 2123-2130.
4. Chen, H., Swedlow, J.R., Grote, M.A., Sedat, J.W., and Agard, D.A. (1995). The collection, processing and display of digital three-dimensional images of biological specimens. In: Handbook of Biological Confocal Microscopy, ed. J. Pawley, New York: Plenum Press, 197-210.
5. Compton, D.A. (1998). Focusing on spindle poles. J. Cell Sci. 111, 1477-1481.
6. Desai, A., Maddox, P.S., Mitchison, T.J., and Salmon, E.D. (1998). Anaphase A chromosome movement and poleward spindle microtubule flux occur at similar rates in Xenopus extract spindles. J. Cell Biol. 141, 703-713.
7. Desai, A., and Mitchison, T.A. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell. Dev. Biol. 23, 83-117.
8. Desai, A., Verma, S., Mitchison, T.J., and Walczak, C.E. (1999). KinI kinesins are microtubule-destabilizing enzymes. Cell 96, 69-78.
9. DeZwaan, T.M., Ellingson, E., Pellman, D., and Roof, D.M. (1997). Kinesin-related KIP3 of Saccharomyces cerevisiae is required for a distinct step in nuclear migration. J. Cell Biol. 138, 1023-1040.
10. Ding, D.Q., Chikashige, Y., Haraguchi, T., and Hiraoka, Y. (1998). Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells. J. Cell Sci. 111, 701-712.
11. Ding, R., McDonald, K.L., and McIntosh, J.R. (1993). Three-dimensional reconstruction and analysis of mitotic spindles from the yeast Schizosaccharomyces pombe. J. Cell Biol. 120, 141-151.
12. Downing, K.H., and Nogales, E. (1998). Tubulin and microtubule structure. Curr. Opin. Cell Biol. 10, 16-22.
13. Efimov, V.P., and Morris, N.R. (1998). A screen for dynein synthetic lethals in Aspergillus nidulans identifies spindle assembly checkpoint genes and other genes involved in mitosis. Genetics 149, 101-116.
14. Egel, R. (1973). Commitment to meiosis in fission yeast. Mol. Gen. Genet. 121, 277-284.
15. Egel, R., Willer, M., Kjaerulff, S., Davey, J., and Nielsen, O. (1994). Assessment of pheromone production and response in fission yeast by a halo test of induced sporulation. Yeast 10, 1347-1354.
16. Endow, S.A., Chandra, R., Komma, D.J., Yamamoto, A.H., and Salmon, E.D. (1994a). Mutants of the Drosophila ncd microtubule motor protein cause centrosomal and spindle pole defects in mitosis. J. Cell Biol. 107, 859-867.
17. Endow, S.A., Kang, S.J., Satterwhite, L.L., Rose, M.D., Skeen, V.P., and Salmon, E.D. (1994b). Yeast KAR3 is a minus-end microtubule motor protein that destabilizes microtubules preferentially at the minus ends. EMBO J. 13, 2708-2713.
18. Endow, S.A., and Komma, D.J. (1996). Centrosome and spindle function of the Drosophila Ncd microtubule motor visualized in live embryos using Ncd-GFP fusion proteins. J. Cell Sci. 109, 2429-2442.
19. Endow, S.A., and Komma, D.J. (1998). Assembly and dynamics of an anastraliastral spindle: the meiosis II spindle of Drosophila oocytes. J. Cell Sci. 111, 2487-2495.
20. Fan, J., Griffiths, A.D., Lockhart, A., Cross, R.A., and Amos, L.A. (1996). Microtubule minus ends can be labeled with a phage display antibody specific to alpha-tubulin. J Mol. Biol. 259, 325-330.
21. Fantes, P.A. (1989). Cell cycle controls. In: Molecular Biology of the Fission Yeast, ed. A. Nasim, P. Young, and B.F. Johnson, San Diego: Acdemic Press, 127-204.
22. 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.
23. Gaglio, T., Saredi, A., Bingham, J.B., Hasbani, M.J., Gill, S.R., Schroer, T.A., and Compton, D.A. (1996). Opposing motor activities are required for the organization of the mammalian mitotic spindle pole. J. Cell Biol. 135, 399-414.
24. Geissler, S., Pereira, G., Spang, A., Knop, M., Soues, S., Kilmartin, J., and Schiebel, E. (1996). The spindle pole body component Spc98p interacts with the γ-tubulin-like Tub4p of Saccharomyces cerevisiae at the sites of microtubule attachment. EMBO J. 15, 3899-3911.
25. Gueth-Hallonet, C., Antony, C., Aghion, J., Santa-Maria, A., Lajoie-Mazenc, I., Wright, M., and Maro, B. (1993). γ-Tubulin is present in acentriolar MTOCs during early mouse development. J. Cell Sci. 105, 157-166.
26. Hagan, I.M. (1998). The fission yeast microtubule cytoskeleton. J. Cell Sci. 111, 1603-1612.
27. Hagan, I.M., and Hyams, J.S. (1988). The use of cell division cycle mutants to investigate the control of microtubule distribution in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 89, 343-357.
28. + gene. Nature 347, 563-566.
29. Hagan, I.M., and Yanagida, M. (1992). Kinesin-related cut7 protein associates with mitotic and meiotic spindles in fission yeast. Nature 356, 74-76.
30. Hardwick, K.G., Li, R., Mistrot, C., Chen, R.-H., Dann, P., Rudner, A., and Murray, A.W. (1999). Lesions in many different spindle components activate the spindle checkpoint in the budding yeast Saccharomyces cerevisiae. Genetics 152, 509-518.
31. He, X., Patterson, T.E., and Sazer, S. (1997). The Schizosaccharomyces pombe spindle checkpoint protein mad2p blocks anaphase and genetically interacts with the anaphase-promoting complex. Proc. Natl. Acad. Sci. USA 94, 7965-7970.
32. Heald, R., Tournebize, R., Blank, T., Sandaltzopoulos, R., Becker, P., Hyman, A., and Karsenti, E. (1996). Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382, 420-425.
33. Hiraoka, Y., Toda, T., and Yanagida, M. (1984). The nda3 gene of fission yeast encodes beta-tubulin: a cold-sensitive nda3 mutation reversibly blocks spindle formation and chromosome movement in mitosis. Cell 39, 349-358.
34. Horio, T., and Oakley, B.R. (1994). Human γ-tubulin functions in fission yeast. J. Cell Biol. 126, 1465-1473.
35. 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.
36. Huyett, A., Kahana, J., Silver, P., Zeng, X., and Saunders, W.S. (1998). The Kar3p and Kip2p motors function antagonistically at the spindle poles to influence cytoplasmic microtubule numbers. J. Cell Sci. 111, 295-301.
37. Inoue, S., Turgeon, B.G., Yoder, O.C., and Aist, J.R. (1998a). Role of fungal dynein in hyphal growth, microtubule organization, spindle pole body motility and nuclear migration. J. Cell Sci. 111, 1555-1566.
38. Inoue, S., Yoder, O.C., Turgeon, B.G., and Aist, J.R. (1998b). A cytoplasmic dynein required for mitotic aster formation in vivo. J. Cell Sci. 111, 2607-2614.
39. Javerzat, J.P., Cranston, G., and Allshire, R.C. (1996). Fission yeast genes which disrupt mitotic chromosome segregation when overexpressed. Nucleic Acids Res. 24, 4676-4683.
40. Johnson, B.F., Miyata, M., and Miyata, H. (1989). Morphogenesis of fission yeasts. In: Molecular Biology of the Fission Yeast, ed. A. Nasim, P. Young, and B.F. Johnson, San Diego: Academic Press, 331-366.
41. Joshi, H.C., Palacios, M.J., McNamara, L., and Cleveland, D.W. (1992). γ-Tubulin is a centrosomal protein required for cell cycle-dependent microtubule nucleation. Nature 356, 80-83.
42. Jung, M.K., May, G.S., and Oakley, B.R. (1998). Mitosis in wild type and β-tubulin mutant strains of Aspergillus nidulans. Fungal Genet. Biol. 24, 146-160.
43. Kahana, J.A., Schlenstedt, G., Evanchuk, D.M., Geiser, J.R., Hoyt, M.A., and Silver, P.A. (1998). The yeast dynactin complex is involved in partitioning the mitotic spindle between mother and daughter cells during anaphase B. Mol. Biol. Cell 9, 1741-1756.
44. Katz, W., Weinstein, B., and Solomon, F. (1990). Regulation of tubulin levels and microtubule assembly in Saccharomyces cerevisiae; consequences of altered tubulin gene copy number. Mol. Cell. Biol. 10, 5286-5294.
45. Knop, M., Pereira, G., Geissler, S., Grein, K., and Schiebel, E. (1997). The spindle pole body component Spc97p interacts with the γ-tubulin of Saccharomyces cerevisiae and functions in microtubule organization and spindle pole body duplication. EMBO J. 16, 1550-1564.
46. Knop, M., and Schiebel, E. (1997). Spc98p and Spc97p of the yeast γ-tubulin complex mediate binding to the spindle pole body via their interaction with Spc110p. EMBO J. 16, 6985-6995.
47. Kohli, j., Hottinger, H., Munz, P., Strauss, A., and Thuriaux, P. (1977). Genetic mapping in Schizosaccharomyces pombe by mitotic and meiotic analysis and induced haploidization. Genetics 87, 471-489.
48. Li, Q., and Joshi, H.C. (1995). γ-Tubulin is a minus-end specific microtubule binding protein. J. Cell Biol. 131, 207-214.
49. Liu, B., Joshi, H.C., Wilson, T.J., Silflow, C.D., Palevitz, B.A., and Snustad, D.P. (1994). γ-Tubulin in Arabidopsis: gene sequence, immunoblot, and immunofluorescence studies. Plant Cell 6, 303-314.
50. Mandelkow, E., and Hoenger, A. (1999). Structures of kinesin and kinesin-microtubule interactions. Curr. Opin. Cell Biol. 11, 34-44.
51. Marschall, L.G., Jeng, R.L., Mulholland, J., Stearns, T. (1996). Analysis of Tub4p, a yeast γ-tubulin-like protein: implications for microrubule-organizing center function. J. Cell Biol. 134, 443-454.
52. 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.
53. Martin, O.C., Gunawardane, R.N., Iwamatsu, A., and Zheng, Y. (1998). Xgrip109: a γ-tubulin-associated protein with an essential role in γ-tubulin ring complex (γTuRC) assembly and centrosome function. J. Cell Biol. 141, 675-687.
54. Masuda, H., and Shibata, T. (1996). Role of γ-tubulin in mitosis-specific microtubule nucleation from the Schizosacchoromyces pombe spindle pole body. J. Cell Sci. 109, 165-177.
55. Maundrell, K. (1993). Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123, 127-130.
56. McDonald, A.R., Liu, B., Joshi, H.C., and Palevitz, B.A. (1993). γ-Tubulin is associated with a cortical-microtubule-organizing zone in the developing guard cells of Allium cepa L. Planta 191, 357-361.
57. McDonald, K. (1999). High pressure freezing for preservation of high resolution fine structure and antigenicity for immunolabeling. Methods Mol. Biol. 117, 77-97.
58. Melki, R., Vainberg, I.E., Chow, R.L., and Cowan, N.J. (1993). Chaperonin-mediated folding of vertebrate actin-related protein and γ-tubulin. J. Cell Biol. 122, 1301-1310.
59. Mitchison, T.J. (1993). Localization of an exchangeable GTP binding site at the plus end of microtubules. Science 261, 1044-1047.
60. Moreno, S., Klar, A., and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
61. Moritz, M., Braunfeld, M.B., Sedat, J.W., Alberts, B., and Agard, D.A. (1995). Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature 378, 638-640.
62. 2+ binding to calmodulin and its role in Schizosaccharomyces pombe as revealed by mutagenesis and NMR spectroscopy. J. Biol. Chem. 270, 20643-20652.
63. Mullins, J.M., and McIntosh, J.R. (1982). Isolation and initial characterization of the mammalian midbody. J. Cell Biol. 94, 654-661.
64. Muresan, V., Joshi, H.C., and Besharse, J. (1993). γ-Tubulin in differentiated cell types: localization in the vicinity of basal bodies in retinal photoreceptors and ciliated epithelia. J. Cell Sci. 104, 1229-1237.
65. Murphy, S.M., Urbani, L., and Stearns, T. (1998). The mammalian γ-tubulin complex contains homologues of the yeast spindle pole body components spc97p and spc98p. J. Cell Biol. 141, 663-674.
66. Nogales, E., Whittaker, M., Milligan, R.A., and Downing, K.H. (1999). High-resolution model of the microtubule. Cell 96, 79-88.
67. Nogales, E., Wolf, S.G., and Downing, K.H. (1998). Structure of the α/β tubulin dimer by electron crystallography. Nature 391, 199-203.
68. Oakley, B.R. (1994). γ-Tubulin. In: Microtubules, ed. J.S. Hyam and C.W. Lloyd, New York: John Wiley and Sons, 33-45.
69. Oakley, B.R., and Morris, N.R. (1981). A β-tubulin mutation in Aspergillus nidulans that blocks microtubule function without blocking assembly. Cell 24, 837-845.
70. Oakley, B.R., Oakley, C.E., and Rinehart, J.E. (1987). Conditionally lethal titbA α-tubulin mutations in Aspergillus nidulans. Mol. Gen. Genet. 208, 135-144.
71. Oakley, B.R., Oakley, C.E., Yoon, Y., and Jung, M.K. (1990). γ-Tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell 63, 1289-1301.
72. Oakley, C.E., and Oakley, B.R. (1989). Identification of γ-tubulin, a new member of the tubulin superfamily encoded by the mipA gene of Aspcrgillus nidulans. Nature 338, 662-664.
73. Oegema, K., Wiese, C., Martin, O.C., Milligan, R.A., Iwamatsu, A., Mitchison, T.J., and Zheng, Y. (1999). Characterization of two related Drosophila gamma-tubulin complexes that differ in their ability to nucleate microtubules. J. Cell Biol. 144, 721-733.
74. Palacios, M., Joshi, H.C., Simerly, D., and Schatten, G. (1993). Dynamic reorganization of γ-tubulin during mouse fertilization and early development. J. Cell Sci. 104, 383-389.
75. Pereira, G., Knop, M., and Schiebel, E. (1998). Spc98p directs the yeast γ-tubulin complex into the nucleus and is subject to cell cycle-dependent phosphorylation on the nuclear side of the spindle pole body. Mol. Biol. Cell 9, 775-793.
76. Pidoux, A.L., LeDizet, M., and Cande, W.Z. (1996). Fission yeast pkl1 is a kinesin-related protein involved in mitotic spindle function. Mol. Biol. Cell 7, 1639-1655.
77. Plamann, M., Minke, P.F., Tinsley, J.H., and Bruno, K.S. (1994). Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi. J. Cell Biol. 127, 139-149.
78. Raff, J.W., Kellogg, D.R., and Alberts, B.M. (1993). Drosophila γ-tubulin is part of a complex containing two previously identified centrosomal MAPs. J. Cell Biol. 121, 823-835.
79. Rieder, C.L. (1981). The structure of the cold-stable kinetochore fiber in metaphase PtK1 cells. Chromosoma 84, 145-158.
80. Rizzolo, L.J., and Joshi, H.C. (1993). Apical orientation of the microtubule organizing center and associated γ-tubulin during the polarization of the retinal pigment epithelium in vivo. Dev. Biol. 157, 147-156.
81. Salmon, E.D., Goode, D., Maugel, T.K., and Bonar, D.B. (1976). Pressure-induced depolymerization of spindle microtubules. III. Differential stability in HeLa cells. J. Cell Biol. 69, 443-454.
82. Saunders, W., Hornack, D., Lengyel, V., and Deng, C. (1997). The Saccharomyces cerevisiae kinesin-related motor Kar3p acts at preanaphase spindle poles to limit the number and length of cytoplasmic microtubules. J. Cell Biol. 137, 417-431.
83. Saunders, W.S., Koshland, D., Eshel, D., Gibbons, I.R., and Hoyt, M.A. (1995). Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation. J. Cell Biol. 128, 617-624.
84. Shaw, S.L., Yeh, E., Maddox, P., Salmon, E.D., and Bloom, K. (1997). Astral microtubule dynamics in yeast: a microtubule-based searching mechanism for spindle orientation and nuclear migration into the bud. J. Cell Biol. 139, 985-994.
85. Sobel, S.G., and Snyder, M. (1995). A highly divergent γ-tubulin gene is essential for cell growth and proper microtubule organization in Saccharomyces cerevisiae. J. Cell Biol. 131, 1775-1788.
86. Spang, A., Geissler, S., Grein, K., and Schiebel, E. (1996). γ-Tubulin-like Tub4p of Saccharomyces cerevisiae is associated with the spindle pole body substructures that organize microtubules and is required for mitotic spindle formation. J. Cell Biol. 134, 429-441.
87. Stearns, T. (1997). Motoring to the finish: kinesin and dynein work together to orient the yeast mitotic spindle. J. Cell Biol. 138, 957-960.
88. Stearns, T., Evans, L., and Kirschner, M. (1991). γ-Tubulin is a highly conserved component of the centrosome. Cell 65, 825-836.
89. Stearns, T., and Kirschner, M. (1994). In vitro reconstitution of centrosome assembly and function: the central role of γ-tubulin. Cell 76, 623-637.
90. Su, S.S.Y., and Yanagida, M. (1997). Mitosis and cytokinesis in the fission yeast, Schizosaccharomyces pombe. In: The Molecular and Cellular Biology of the Yeast Saccharomyces: Cell Cycle and Cell Biology, ed. J.R. Pringle, J.R. Broach, and E.W. Jones, New York: Cold Spring Harbor Laboratory Press, 765-825.
91. Sunkel, C.E., Gomes, R., Sampaio, P., Perdigao, J., and Gonzalez, C. (1995). γ-Tubulin is required for the structure and function of the microtubule organizing center in Drosophila neuroblasts. EMBO J. 14, 28-36.
92. Tange, Y., Horio, T., Shimanuki, M., Ding, D.-Q., Hiraoka, Y., and Niwa, O. (1998). A novel fission yeast gene, tht1+, is required for the fusion of nuclear envelopes during karyogamy. J. Cell Biol. 140, 247-258.
93. Tassin, A.M., Celati, C., Moudjou, M., and Bornens, M. (1998). Characterization of the human homologue of the yeast spc98p and its association with γ-tubulin. J. Cell Biol. 141, 689-701.
94. Toda, T., Adachi, Y., Hiraoka, Y., and Yanagida, M. (1984). Identification of the pleiotropic cell division cycle gene nda2 as one of two different α-tubulin genes in Schizosaccharomyces pombe. Cell 37, 233-242.
95. Umesono, K., Toda, T., Hayashi, S., and Yanagida, M. (1983). Cell division cycle genes nda2 and nda3 of the fission yeast Schizosaccharomyces pombe control microtubular organization and sensitivity to anti-mitotic benzimidazole compounds. J. Mol. Biol. 168, 271-284.
96. Walczak, C.E., Mitchison, T.J., and Desai, A. (1996). XKCM1: a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell 84, 37-47.
97. Waters, J.C., Chen, R.H., Murray, A.W., Gorbsky, G.J., Salmon, E.D., and Niklas, R.B. (1999). Mad2 binding by phosphorylated kinetochores links error detection and checkpoint action in mitosis. Curr. Biol. 9, 649-652.
98. Waters, J.C., Chen, R.H., Murray, A.W., and Salmon, E.D. (1998). Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J. Cell Biol. 141, 1181-1191.
99. Wigge, P.A., Jensen, O.N., Holmes, S., Soues, S., Mann, M., and Kilmartin, J.V. (1998). Analysis of the Saccharomyces spindle pole by matrix-assisted laser desorption/ionization (MALDI) mass spectrometry. J. Cell Biol. 141, 967-977.
100. Woods, A., Sherwin, T., Sasse, R., MacRae, T.H., Baines, A.J., and 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.
101. Yamamoto, A., West, R.R., McIntosh, J.R., and Hiraoka, Y. (1999). A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast. J. Cell Biol. 145, 1233-1249.
102. Zheng, Y., Wong, M.L., Alberts, B., and Mitchison, T. (1995). Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature 378, 578-583.