γ-tubulin complexes: Binding to the centrosome, regulation and microtubule nucleation

Current Opinion in Cell Biology

Volumn 12, Issue 1, 2000, Pages 113-118

  Schiebel, Elmar ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA BINDING PROTEIN; GAMMA TUBULIN; GUANOSINE TRIPHOSPHATASE;

CENTRIOLE; CENTROSOME; COMPLEX FORMATION; MICROTUBULE ASSEMBLY; MITOSIS SPINDLE; PARAMECIUM; PRIORITY JOURNAL; PROTEIN DNA BINDING; REVIEW;

PARAMECIUM;

EID: 0033954226     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(99)00064-2     Document Type: Review

References (38)

1. Zheng Y., Wong M.L., Alberts B., Mitchison T. Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature. 378:1995;578-583.
2. Erickson H.P., Stoffler D. Protofilaments and rings, two conformations of the tubulin family conserved from bacterial FtsZ to α/β and γ-tubulin. J Cell Biol. 135:1996;5-8.
3. Pereira G., Schiebel E. Centrosome-microtubule nucleation. J Cell Sci. 110:1997;295-300.
4. Knop M., Schiebel E. Receptors determine the cellular localization of a γ-tubulin complex and thereby the site of microtubule formation. EMBO J. 17:1998;3952-3967.
5. Knop M., Schiebel E. Spc98p and Spc97p of the yeast γ-tubulin complex mediate binding to the spindle pole body via their interaction with Spc110p. EMBO J. 16:1997;6985-6995.
6. Heald R., Tournebize R., Blank T., Sandaltzopoulos R., Becker P., Hyman A., Karsenti E. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature. 382:1996;420-425.
7. Tassin A-M., Celati C., Moudjou M., Bornens M. Characterization of the human homologue of the yeast Spc98p and its association with γ-tubulin. J Cell Biol. 141:1998;689-701.
8. Martin O.C., Gunawardane R.N., Iwamatsu A., Zheng Y. Xgrip109: a γ-tubulin-associated protein with an essential role in γ-tubulin ring complex (γTuRC) assembly and centrosome function. J Cell Biol. 141:1998;675-687.
9. Murphy S.M., Urbani L., Stearns T. The mammalian γ-tubulin complex contains homologues of the yeast spindle pole body components Spc97p and Spc98p. J Cell Biol. 141:1998;663-674.
10. Moritz M., Zheng Y., Alberts B.M., Oegema K. Recruitment of the γ-tubulin ring complex to Drosphila salt-stripped centrosome scaffolds. J Cell Biol. 142:1998;775-786. Shows that in Drosophila γ-tubulin is found in two distinct complexes, the γ-TuRC and another one of 240 kDa. γ-TuRC is necessary but not sufficient to restore microtubule nucleation activity of salt-stripped Drosophila centrosomes. An additional factor of 220 kDa is required.
11. Oegema K., Wiese C., Martin O.C., Milligan R.A., Iwamatsu A., Mitchison T.J., Zheng Y. Characterization of two related Drosophila γ-tubulin complexes that differ in their ability to nucleate microtubules. J Cell Biol. 144:1999;721-733. The authors describe the purification of γ-TuRC and a smaller 280 kDa γ-tubulin complex from Drosophila. The 280 kDa γ-tubulin complex contains γ-tubulin and homologues of Spc97p and Spc98p. γ-TuRC seems to disassemble into the 280 kDa complex in the presence of high salt. Cryo-electron microscopy of γ-TuRC reveals an open ring structure with about 13 radial repeats. It is also shown that γ-tubulin preferentially binds GDP over GTP.
12. Moudjou M., Bordes N., Paintrand M., Bornens M. γ-tubulin in mammalian cells: the centrosomal and the cytosolic forms. J Cell Sci. 109:1996;875-887.
13. Moritz M., Braunfeld M.B., Sedat J.W., Alberts B., Agard D.A. Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature. 378:1995;638-640.
14. Vogel J.M., Stearns T., Rieder C.L., Palazzo R.E. Centrosomes isolated from Spisula solidissima oocytes contain rings and an unusual stoichiometric ratio of α/β tubulin. J Cell Biol. 137:1997;193-202.
15. •] are identical.
16. Fava F., Raynaud-Messina B., Leung-Tack J., Mazzolini L., Li M., Guillemot J.C., Cachot D., Tollon Y., Ferrara P., Wright M. Human 76p: a new member of the γ-tubulin associated protein family. J Cell Biol. 147:1999;857-868. The cDNA coding for p76 in the human γ-tubulin complex was identified. Surprisingly, p76 is related to the human Spc97/98 proteins and is required for microtubule nucleation.
17. Nguyen T., Vinh D.B.N., Crawford D.K., Davis T.N. A genetic analysis of interactions with Spc110p reveals distinct functions of Spc97p and Spc98p, components of the yeast γ-tubulin complex. Mol Biol Cell. 9:1998;2201-2216.
18. Tassin A.M., Celati C., Paintrand M., Bornens M. Identification of an Spc110p-related protein in vertebrates. J Cell Sci. 110:1997;2533-2545.
19. 1 to mitosis.
20. Salas P.J.I. Insoluble γ-tubulin-containing structures are anchored to the apical network of intermediate filaments in polarized CACO-2 epithelial cells. J Cell Biol. 146:1999;645-657. Describes the colocalization of noncentrosomal γ-tubulin with apical intermediate filaments in CACO-2 cells. Downregulation of cytokeratin 19 delocalized the non-centrosomal γ-tubulin. In addition, fragments of intermediate filaments were found to co-immunoprecipitate with γ-tubulin.
21. Pereira G., Knop M., Schiebel E. 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. 9:1998;775-793.
22. Pereira G., Grueneberg U., Knop M., Schiebel E. Interaction of the yeast γ-tubulin complex binding protein Spc72p with Kar1p is essential for microtubule function during karyogamy. EMBO J. 18:1999;4180-4196. It is shown that the γ-tubulin complex binding protein Spc72p interacts with Kar1p at the half bridge, thereby directing the yeast γ-tubulin complex to this SPB substructure. The association of Spc72p with the half bridge via Kar1p and the outer plaque is regulated throughout the cell cycle and by the pheromone response pathway.
23. Wigge P.A., Jensen O.N., Holmes S., Souès S., Mann M., Kilmartin J.V. Analysis of the Saccharomyces spindle pole by matrix-assisted laser desorption/ionization (MALDI) mass spectrometry. J Cell Biol. 141:1998;967-977.
24. Adams I.R., Kilmartin J.V. Localization of core spindle pole body (SPB) components during SPB duplication in Saccharomyces cerevisiae. J Cell Biol. 145:1999;809-823.
25. Carminati J.L., Stearns T. Microtubules orient the mitotic spindle in yeast through dynein-dependent interactions with the cell cortex. J Cell Biol. 138:1997;629-641.
26. Shaw S.L., Yeh E.Y., Maddox P., Salmon E.D., Bloom K. Astral microtubule dynamics in yeast: a microtubule-based searching mechanism for spindle orientation and nuclear migration into the bud. J Cell Biol. 139:1997;985-994.
27. •].
28. Kuriyama R., Borisy G.G. Microtubule-nucleating activity of centrosomes in chinese hamster ovary cells is independent of the centriole cycle but coupled to the mitotic cycle. J Cell Biol. 91:1981;822-826.
29. Nakamura M., Masuda H., Horii J., Kuma K., Yokoyama N., Ohba T., Nishitani H., Miyata T., Tanaka M., Nishimoto T. When overexpressed, a novel centrosomal protein, RanBPM, causes ectopic microtubule nucleation similar to γ-tubulin. J Cell Biol. 143:1998;1041-1052. Describes the identification of a novel centrosomal protein, RanBPM, that interacts with Ran GTP and when overexpressed causes ectopic microtubule nucleation. Thus, for the first time this paper implicates Ran in the regulation of microtubule aster formation.
30. ••] that implicates Ran GTP in mitotic spindle assembly.
31. ••].
32. ••] that shows that Ran in its GTP-bound state induces microtubule asters and spindle assembly in an in vitro system. In addition, it is shown that microtubule aster assembly is dependent on γ-TuRC and XMAP215.
33. Zhang C., Hughes M., Clarke P.R. Ran-GTP stabilises microtubule asters and inhibits nuclear assembly in Xenopus egg extracts. J Cell Sci. 112:1999;2453-2461. Describes that Ran GTP stabilizes large microtubule asters nucleated by sperm centrosomes; furthermore, the authors provide convincing evidence that Ran associates with microtubule asters in egg extracts and with mitotic spindles in somatic Xenopus cells.
34. Gard D.L., Kirschner M.W. A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end. J Cell Biol. 105:1987;2203-2215.
35. Carazo-Salas R.E., Guarguaglini G., Gruss O.J., Segref A., Karsenti E., Mattaj I.W. Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature. 400:1999;178-181. This paper explains the previous finding [6] that bipolar spindles can self-organize around chromatin. It is shown that the chromosome-associated RCC1 protein, the guanine-nucleotide-exchange factor for Ran, is responsible for this reaction. It is proposed that RCC1 generates a high local concentration of Ran GTP around chromosomes which then induces microtubule nucleation at the onset or mitosis.
36. Stearns T., Evans L., Kirschner M. γ-tubulin is a highly conserved component of the centrosome. Cell. 65:1991;825-836.
37. Ruiz F., Beisson J., Rossier J., Dupuis-Williams P. Basal body duplication in Paramecium reguries γ-tubulin. Curr Biol. 9:1999;43-46. The first demonstration that inactivation of γ-tubulin genes leads to inhibition of basal body duplication.
38. Bobinnec Y., Khodjakov L.M., Rieder C.L., Eddé B., Bornens M. Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. J Cell Biol. 143:1998;1575-1589.