Characterization of two related Drosophila γ-tubulin complexes that differ in their ability to nucleate microtubules

Journal of Cell Biology

Volumn 144, Issue 4, 1999, Pages 721-733

  Oegema, Karen ^a,e   Wiese, Christiane ^b   Martin, Ona C ^b   Milligan, Ronald A ^c   Iwamatsu, Akihiro ^d   Mitchison, Timothy J ^a   Zheng, Yixian ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b GEOPHYSICAL LABORATORY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d KIRIN BREWERY CO LTD   (Japan)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Centrosome; Cytoskeleton; GDP; GTP; Nucleation

Indexed keywords

TUBULIN;

ARTICLE; CENTROSOME; CRYOELECTRON MICROSCOPY; CYTOSKELETON; DROSOPHILA; GEL FILTRATION CHROMATOGRAPHY; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY;

AMINO ACID SEQUENCE; ANIMALS; CRYOELECTRON MICROSCOPY; DROSOPHILA; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; INSECT PROTEINS; MACROMOLECULAR SUBSTANCES; MICROTUBULES; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PROTEIN BINDING; TUBULIN; XENOPUS;

HEXAPODA;

EID: 0033593802     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.144.4.721     Document Type: Article

References (45)

1. Alberts, B., D. Bray, J. Lewis, M. Raff, K. Roberts, and J. Watson. 1994. Molecular Biology of the Cell. Garland Publishing, Inc., New York, 803-815.
2. Burns, R. 1995. Analysis of the γ-tubulin sequences: implications for the functional properties of γ-tubulin. J. Cell Sci. 108:2123-2130.
3. Desai, A., and T. Mitchison. 1997. Microtubule polymerization dynamics. Ann. Rev. Cell Dev. Biol. 13:83-117.
4. Detraves, C., H. Mazarguil, I. Lajoie-Mazenc, M. Julian, B. Raynaud-Messina, and M. Wright. 1997. Protein complexes containing γ-tubulin are present in mammalian brain microtubule protein preparations. Cell Motil. Cytoskeleton. 36:179-189.
5. Erickson, H.P., and D. Stoffler. 1996. Protofilaments and rings, two conformations of the tubulin family conserved from bacterial FtsZ to α/β and γ-tubulin. J. Cell Biol. 135:5-8.
6. Felix, M. A., C. Antony, M. Wright, and B. Maro. 1994. Centrosome assembly in vitro: role of γ-tubulin recruitment in Xenopus sperm aster formation. J. Cell Biol. 124:19-31.
7. Field, C.M., K. Oegema, Y. Zheng, T.J. Mitchison, and C.E. Walczak. 1998. Purification of cytoskeleton proteins using peptide antibodies. Methods Enzymol. 298:525-541.
8. Frankel, F.R. 1976. Organization and energy-dependent growth of microtubules in cells. Proc. Natl. Acad. Sci. USA. 73:2798-2802.
9. Fygenson, D.K., H. Flyvbjerg, K. Sneppen, A. Libchaber, and S. Leibler. 1995. Spontaneous nucleation of microtubules. Physical Rev. E. 51:5058-5063.
10. Geissler, S., G. Pereira, A. Spang, M. Knop, S. Soues, J. Kilmartin, and E. Schiebel. 1996. The spindle pole body component Spc98p interacts with the γ-tubulin-like Tub4p of Saccharomyces cerevisiae at the sites of microtubule attachment. EMBO (Eur. Mol. Biol. Organ.) J. 15:3899-3911.
11. Horio, T., S. Uzawa, M.K. Jung, B.R. Oakley, K. Tanaka, and M. Yanagida. 1991. The fission yeast γ-tubulin is essential for mitosis and is localized at microtubule organizing centers. J. Cell Sci. 99:693-700.
12. Hyman, A.A., S. Salser, D.N. Drechsel, N. Unwin, and T.J. Mitchison. 1992. Role of GTP hydrolysis in microtubule dynamics: information from a slowly hydrolyzable analogue. GMPCPP. Mol. Biol. Cell. 3:1155-1167.
13. Joshi, H.C. 1994. Microtubule organizing centers and γ-tubulin. Curr. Opin. Cell Biol. 6:54-62.
14. Joshi, H.C., M.J. Palacios, L., McNamara, and D.W. Cleveland. 1992. γ-tubulin is a centrosomal protein required for cell cycle-dependent microtubule nucleation. Nature. 356:80-83.
15. Kellogg, D., and B. Alberts. 1992. Purification of a multiprotein complex containing centrosomal proteins from the Drosophila embryo by chromatography with low affinity polyclonal antibodies. Mol. Biol. Cell. 3:1-11.
16. Keryer, G. H. Ris, and G.G. Borisy. 1984. Centriole distribution during tripolar mitosis in Chinese hamster ovary cells. J. Cell Biol. 98:2222-2229.
17. Knop, M., and E. Schiebel. 1997. Spc98p and Spc97p of the yeast γ-tubulin complex mediate binding to the spindle pole body via their interaction with Spc110p. EMBO (Eur. Mol. Biol. Organ.) J. 16:6985-6995.
18. Knop, M., and E. Schiebel. 1998. Receptors determine the cellular localization of a γ-tubulin complex and thereby the site of microtubule formation. EMBO (Eur. Mol. Biol. Organ.) J. 17:3952-3967.
19. Knop, M., G. Pereira, S. Geissler, K. Grein, and E. Schiebel. 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 (Eur. Mol. Biol. Organ.) J. 16:1550-1564.
20. Marschall, L.G., R.L. Jeng, J. Mulholland, and T. Stearns. 1996. Analysis of Tub4p, a yeast γ-tubulin-like protein: implications for microtubule-organizing center function. J. Cell Biol. 134:443-454.
21. Martin, M.A., S.A. Osmani, and B.R. Oakley. 1997. The role of γ-tubulin in mitotic spindle formation and cell cycle progression in Aspergillus nidulans. J. Cell Sci. 110:623-633.
22. Martin, O.C., R.N. Gunawardane, A. Iwamatsu, and Y. Zheng. 1998. Xgrip109: a γ-tubulin-associated protein with an essential role in gamma tubulin ring complex (γTuRC) assembly and centrosome function. J. Cell Biol. 141:675-687.
23. Meads, T., and T.A. Schroer. 1995. Polarity and nucleation of microtubules in polarized epithelial cells. Cell Motil. Cytoskeleton. 32:273-288.
24. Moritz, M., M.B. Braunfeld, J.C. Fung, J.W. Sedat, B.M. Alberts, and D.A. Agard. 1995a. Three-dimensional structural characterization of centrosomes from early Drosophila embryos. J. Cell Biol. 130:1149-1159.
25. Moritz, M., M.B. Braunfeld, J.W. Sedat, B. Alberts, and D.A. Agard. 1995b. Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature. 378:638-640.
26. Moritz, M., Y. Zheng, B.M. Alberts, and K. Oegema. 1998. Recruitment of the γ-tubulin ring complex to Drosophila salt-stripped ccntrosome scaffolds. J. Cell Biol. 142:1-12.
27. Murphy, S.M., L. Urbani, and T. Stearns. 1998. The mammalian γ-tubulin complex contains homologues of the yeast spindle pole body components spc97p and spc98p. J. Cell Biol. 141:663-674.
28. Oakley, B.R., C.E. Oakley, Y. Yoon, and M.K. Jung. 1990. γ-tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell. 61:1289-1301.
29. Oakley, C.E., and B.R. Oakley. 1989. Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature. 338:662-664.
30. Osborn, M., and K. Weber. 1976. Cytoplasmic microtubules in tissue culture cells appear to grow from an organizing structure towards the plasma membrane. Proc. Natl. Acad. Sci. USA. 73:867-871.
31. Pereira, G., and E. Schiebel. 1997. Centrosome-microtubule nucleation. J. Cell Sci. 110:295-300.
32. Rosenblatt, J., P. Peluso, and T.J. Mitchison. 1995. The bulk of unpolymerized actin in Xenopus egg extracts is ATP-bound. Mol. Biol. Cell. 6:227-236.
33. Siegel, L.M., and K.J. Monty. 1966. Determination of molecular weights and frictional ratios of proteins in impure systems by use of gel filtration and density gradient centrifugation. Biochim. Biophys. Acta. 112:346-362.
34. Sobel, S.d., and M. Snyder. 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.
35. Spang, A., S. Geissler, K. Grein, and E. Schiebel. 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.
36. Stearns, T., and M. Kirschner. 1994. In vitro reconstitution of centrosome assembly and function: the central role of γ-tubulin. Cell. 76:623-637.
37. Sunkel, C.E., R. Gomes, P. Sampaio, J. Perdigao, and C. Gonzalez. 1995. γ-tubulin is required for the structure and function of the microtubule organizing centre in Drosophila neuroblasts. EMBO (Eur. Mol. Biol. Organ.) J. 14:28-36.
38. Tassin, A.M., C. Celati, M. Moudjou, and M. Bornens. 1998. Characterization of the human homologue of the yeast spc98p and its association with γ-tubulin. J. Cell Biol. 141:689-701.
39. Theurkauf, W.E. 1994. Immunofluorescence analysis of the cytoskeleton during oogenesis and early embryogenesis. Methods Cell Biol. 44:489-505.
40. Vogel, J.M., T. Stearns, C.L. Rieder, and R.E. Palazzo. 1997. Centrosomes isolated from Spisula solidissima oocytes contain rings and an unusual stoichiometric ratio of α/β tubulin. J. Cell Biol. 137:193-202.
41. Voter, W.A., and H.P. Erickson. 1984. The kinetics of microtubule assembly. Evidence for a two-stage nucleation mechanism. J. Biol. Chem. 259:10430-10438.
42. Wade, R.H., and D. Chretien. 1993. Cryoelectron microscopy of microtubules. J. Struct. Biol. 110:1-27.
43. Weisenberg, R.C., W.J. Deery, and P.J. Dickinson. 1976. Tubulin-nucleotide interactions during the polymerization and depolymerization of microtubules. Biochemistry. 15:4248-4254.
44. Zeeberg, B., and M. Caplow. 1979. Determination of free and bound microtubular protein and guanine nucleotide under equilibrium conditions. Biochemistry. 18:3880-3886.
45. Zheng, Y., M.L. Wong, B. Alberts, and T. Mitchison. 1995. Nucleation of microlubule assembly by a γ-tubulin-containing ring complex. Nature. 378:578-583.