γ-Tubulin ring complexes regulate microtubule plus end dynamics

Journal of Cell Biology

Volumn 187, Issue 3, 2009, Pages 327-334

  Bouissou, Anaïs ^a   Vérollet, Christel ^a   Sousa, Aureliana ^b   Sampaio, Paula ^b   Wright, Michel ^a   Sunkel, Claudio E ^b,c   Merdes, Andreas ^a   Raynaud Messina, Brigitte ^a  

^a CNRS   (France)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA TUBULIN; DROSOPHILA PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; TUBULIN;

ANIMAL CELL; ARTICLE; CELL CYCLE PROGRESSION; CELL VIABILITY; DROSOPHILA; DYNAMICS; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; INTERPHASE; MICROTUBULE; MICROTUBULE ASSEMBLY; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; ANIMAL; CELL CULTURE; DROSOPHILA MELANOGASTER; GENETICS; METABOLISM; PHYSIOLOGY; ULTRASTRUCTURE;

DROSOPHILA MELANOGASTER;

ANIMALS; CELLS, CULTURED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; INTERPHASE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; TUBULIN;

EID: 75549091741     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200905060     Document Type: Article

References (41)

1. Anders, A., P.C. Lourenço, and K.E. Sawin. 2006. Noncore components of the fission yeast gamma-tubulin complex. Mol. Biol. Cell. 17:5075-5093. doi:10.1091/mbc.E05-11-1009
2. Barbosa, V., R.R. Yamamoto, D.S. Henderson, and D.M. Glover. 2000. Mutation of a Drosophila gamma tubulin ring complex subunit encoded by discs degenerate-4 differentially disrupts centrosomal protein localization. Genes Dev. 14:3126-3139. doi:10.1101/gad.182800
3. Brittle, A.L., and H. Ohkura. 2005. Mini spindles, the XMAP215 homologue, suppresses pausing of interphase microtubules in Drosophila. EMBO J. 24:1387-1396. doi:10.1038/sj.emboj.7600629
4. Colombié, N., C. Vérollet, P. Sampaio, A. Moisand, C. Sunkel, H.M. Bourbon, M. Wright, and B. Raynaud-Messina. 2006. The Drosophila gamma-tubulin small complex subunit Dgrip84 is required for structural and functional integrity of the spindle apparatus. Mol. Biol. Cell. 17:272-282. doi:10.1091/mbc.E05-08-0722
5. Cuschieri, L., R. Miller, and J. Vogel. 2006. Gamma-tubulin is required for proper recruitment and assembly of Kar9-Bim1 complexes in budding yeast. Mol. Biol. Cell. 17:4420-4434. doi:10.1091/mbc.E06-03-0245
6. Dimitrov, A., M. Quesnoit, S. Moutel, I. Cantaloube, C. Poüs, and F. Perez. 2008. Detection of GTP-tubulin conformation in vivo reveals a role for GTP remnants in microtubule rescues. Science. 322:1353-1356. doi:10.1126/science.1165401
7. Fujita, A., L. Vardy, M.A. Garcia, and T. Toda. 2002. A fourth component of the fission yeast γ-tubulin complex, Alp16, is required for cytoplasmic microtubule integrity and becomes indispensable when γ-tubulin function is compromised. Mol. Biol. Cell. 13:2360-2373. doi:10.1091/mbc.02-01-0603
8. Goshima, G., M. Mayer, N. Zhang, N. Stuurman, and R.D. Vale. 2008. Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J. Cell Biol. 181:421-429. doi:10.1083/jcb.200711053
9. Gunawardane, R.N., O.C. Martin, K. Cao, L. Zhang, K. Dej, A. Iwamatsu, and Y. Zheng. 2000. Characterization and reconstitution of Drosophila γ-tubulin ring complex subunits. J. Cell Biol. 151:1513-1524. doi:10.1083/jcb.151.7.1513
10. Haren, L., M.-H. Remy, I. Bazin, I. Callebaut, M. Wright, and A. Merdes. 2006. NEDD1-dependent recruitment of the γ-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J. Cell Biol. 172:505-515. doi:10.1083/jcb.200510028
11. Izumi, N., K. Fumoto, S. Izumi, and A. Kikuchi. 2008. GSK-3beta regulates proper mitotic spindle formation in cooperation with a component of the gamma-tubulin ring complex, GCP5. J. Biol. Chem. 283:12981-12991. doi:10.1074/jbc.M710282200
12. Janson, M.E., T.G. Setty, A. Paoletti, and P.T. Tran. 2005. Efficient formation of bipolar microtubule bundles requires microtubule-bound γ-tubulin complexes. J. Cell Biol. 169:297-308. doi:10.1083/jcb.200410119
13. Joshi, H.C., M.J. Palacios, L. McNamara, and D.W. Cleveland. 1992. Gammatubulin is a centrosomal protein required for cell cycle-dependent microtubule nucleation. Nature. 356:80-83. doi:10.1038/356080a0
14. Knop, M., and E. Schiebel. 1997. Spc98p and Spc97p of the yeast gamma-tubulin complex mediate binding to the spindle pole body via their interaction with Spc110p. EMBO J. 16:6985-6995. doi:10.1093/emboj/16.23. 6985
15. Lajoie-Mazenc, I., Y. Tollon, C. Détraves, M. Julian, A. Moisand, C. Gueth-Hallonet, A. Debec, I. Salles-Passador, A. Puget, H. Mazarguil, et al. 1994. Recruitment of antigenic gamma-tubulin during mitosis in animal cells: presence of gamma-tubulin in the mitotic spindle. J. Cell Sci. 107:2825-2837.
16. Lüders, J., U.K. Patel, and T. Stearns. 2006. GCP-WD is a gamma-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat. Cell Biol. 8:137-147. doi:10.1038/ncb1349
17. Mahoney, N.M., G. Goshima, A.D. Douglass, and R.D. Vale. 2006. Making microtubules and mitotic spindles in cells without functional centrosomes. Curr. Biol. 16:564-569. doi:10.1016/j.cub.2006.01.053
18. Masuda, H., R. Miyamoto, T. Haraguchi, and Y. Hiraoka. 2006. The carboxyterminus of Alp4 alters microtubule dynamics to induce oscillatory nuclear movement led by the spindle pole body in Schizosaccharomyces pombe. Genes Cells. 11:337-352. doi:10.1111/j.1365-2443.2006.00947.x
19. Moritz, M., M.B. Braunfeld, J.W. Sedat, B. Alberts, and D.A. Agard. 1995. Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature. 378:638-640. doi:10.1038/378638a0
20. Murata, T., S. Sonobe, T.I. Baskin, S. Hyodo, S. Hasezawa, T. Nagata, T. Horio, and M. Hasebe. 2005. Microtubule-dependent microtubule nucleation based on recruitment of gamma-tubulin in higher plants. Nat. Cell Biol. 7:961-968. doi:10.1038/ncb1306
21. 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. doi:10.1038/338662a0
22. Oegema, K., C. Wiese, O.C. Martin, R.A. Milligan, A. Iwamatsu, T.J. Mitchison, and Y. Zheng. 1999. Characterization of two related Drosophila γ-tubulin complexes that differ in their ability to nucleate microtubules. J. Cell Biol. 144:721-733. doi:10.1083/jcb.144.4.721
23. Paluh, J.L., E. Nogales, B.R. Oakley, K. McDonald, A.L. Pidoux, and W.Z. Cande. 2000. A mutation in gamma-tubulin alters microtubule dynamics and organization and is synthetically lethal with the kinesin-like protein pkl1p. Mol. Biol. Cell. 11:1225-1239.
24. Raynaud-Messina, B., and A. Merdes. 2007. Gamma-tubulin complexes and microtubule organization. Curr. Opin. Cell Biol. 19:24-30. doi:10.1016/j.ceb.2006.12.008
25. Raynaud-Messina, B., L. Mazzolini, A. Moisand, A.M. Cirinesi, and M. Wright. 2004. Elongation of centriolar microtubule triplets contributes to the formation of the mitotic spindle in gamma-tubulin-depleted cells. J. Cell Sci. 117:5497-5507. doi:10.1242/jcs.01401
26. Rogers, S.L., G.C. Rogers, D.J. Sharp, and R.D. Vale. 2002. Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J. Cell Biol. 158:873-884. doi:10.1083/jcb.200202032
27. Rogers, G.C., N.M. Rusan, M. Peifer, and S.L. Rogers. 2008. A multicomponent assembly pathway contributes to the formation of acentrosomal microtubule arrays in interphase Drosophila cells. Mol. Biol. Cell. 19:3163-3178. doi:10.1091/mbc.E07-10-1069
28. Rusan, N.M., C.J. Fagerstrom, A.M. Yvon, and P. Wadsworth. 2001. Cell cycle-dependent changes in microtubule dynamics in living cells expressing green fluorescent protein-alpha tubulin. Mol. Biol. Cell. 12:971-980.
29. Sawin, K.E., P.C. Lourenco, and H.A. Snaith. 2004. Microtubule nucleation at non-spindle pole body microtubule-organizing centers requires fission yeast centrosomin-related protein mod20p. Curr. Biol. 14:763-775. doi:10.1016/j.cub.2004.03.042
30. Schnorrer, F., S. Luschnig, I. Koch, and C. Nüsslein-Volhard. 2002. γ-tubulin37C and γ-tubulin ring complex protein 75 are essential for bicoid RNA localization during Drosophila oogenesis. Dev. Cell. 3:685-696. doi:10.1016/S1534-5807(02)00301-5
31. Sousa, A., R. Reis, P. Sampaio, and C.E. Sunkel. 2007. The Drosophila CLASP homologue, Mast/Orbit regulates the dynamic behaviour of interphase microtubules by promoting the pause state. Cell Motil. Cytoskeleton. 64:605-620. doi:10.1002/cm.20208
32. Sunkel, C.E., R. Gomes, P. Sampaio, J. Perdigão, and C. González. 1995. Gamma-tubulin is required for the structure and function of the microtubule organizing centre in Drosophila neuroblasts. EMBO J. 14:28-36.
33. Vardy, L., and T. Toda. 2000. The fission yeast γ-tubulin complex is required in G(1) phase and is a component of the spindle assembly checkpoint. EMBO J. 19:6098-6111. doi:10.1093/emboj/19.22.6098
34. Venkatram, S., J.J. Tasto, A. Feoktistova, J.L. Jennings, A.J. Link, and K.L. Gould. 2004. Identification and characterization of two novel proteins affecting fission yeast gamma-tubulin complex function. Mol. Biol. Cell. 15:2287-2301. doi:10.1091/mbc.E03-10-0728
35. Vérollet, C., N. Colombié, T. Daubon, H.M. Bourbon, M. Wright, and B. Raynaud-Messina. 2006. Drosophila melanogaster γ-TuRC is dispensable for targeting γ-tubulin to the centrosome and microtubule nucleation. J. Cell Biol. 172:517-528. doi:10.1083/jcb. 200511071
36. Vogt, N., I. Koch, H. Schwarz, F. Schnorrer, and C. Nüsslein- Volhard. 2006. The gammaTuRC components Grip75 and Grip128 have an essential microtubule-anchoring function in the Drosophila germline. Development. 133:3963-3972. doi:10.1242/dev.02570
37. Wiese, C., and Y. Zheng. 2000. A new function for the gamma-tubulin ring complex as a microtubule minus-end cap. Nat. Cell Biol. 2:358-364. doi:10.1038/35014051
38. Wilde, A., and Y. Zheng. 1999. Stimulation of microtubule aster formation and spindle assembly by the small GTPase Ran. Science. 284:1359-1362. doi:10.1126/science.284.5418.1359
39. Zheng, Y., M.L. Wong, B. Alberts, and T. Mitchison. 1995. Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature. 378:578-583. doi:10.1038/378578a0
40. Zhu, H., J.A. Coppinger, C.Y. Jang, J.R. Yates III, and G. Fang. 2008. FAM29A promotes microtubule amplification via recruitment of the NEDD1-γ-tubulin complex to the mitotic spindle. J. Cell Biol. 183:835-848. doi:10.1083/jcb.200807046
41. Zimmerman, S., and F. Chang. 2005. Effects of gamma-tubulin complex proteins on microtubule nucleation and catastrophe in fission yeast. Mol. Biol. Cell. 16:2719-2733. doi:10.1091/mbc.E04-08-0676