GTP regulates the microtubule nucleation activity of γ-tubulin

Nature Cell Biology

Volumn 15, Issue 11, 2013, Pages 1317-1327

  Gombos, Linda ^a   Neuner, Annett ^a   Berynskyy, Mykhaylo ^b   Fava, Luca L ^a,d   Wade, Rebecca C ^a,b   Sachse, Carsten ^c   Schiebel, Elmar ^a  

^a GERMAN CANCER RESEARCH CENTER   (Germany)

^b HEIDELBERG INSTITUTE FOR THEORETICAL STUDIES   (Germany)

^c EMBL Heidelberg   (Germany)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BENOMYL; BETA TUBULIN; GAMMA TUBULIN; GUANOSINE TRIPHOSPHATE; RECEPTOR PROTEIN; SPC97 PROTEIN; SPC98 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SPINDLE POLE BODY;

GUANOSINE TRIPHOSPHATE; MICROTUBULES; MODELS, MOLECULAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TUBULIN;

EID: 84887260519     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2863     Document Type: Article

References (52)

1. Downing, K. H. & Nogales, E. Tubulin and microtubule structure. Curr. Opin. Cell Biol. 10, 16-22 (1998). (Pubitemid 28066117)
2. Weisenberg, R. C., Borisy, G. G. & Taylor, E. W. The colchicine-binding protein of mammalian brain and its relation to microtubules. Biochemistry 7, 4466-4479 (1968).
3. Löwe, J., Li, H., Downing, K. H. & Nogales, E. Refined structure of alpha beta-tubulin at 3.5 Å resolution. J. Mol. Biol. 313, 1045-1057 (2001). (Pubitemid 33081900)
4. Menéndez, M., Rivas, G., Díaz, J. F. & Andreu, J. M. Control of the structural stability of the tubulin dimer by one high affinity bound magnesium ion at nucleotide N-site. J. Biol. Chem. 273, 167-176 (1998). (Pubitemid 28042190)
5. Nogales, E. A structural view of microtubule dynamics. Cell Mol. Life Sci. 56, 133-142 (1999). (Pubitemid 29471931)
6. Rice, L. M., Montabana, E. A. & Agard, D. A. The lattice as allosteric effector: structural studies ofαβ-and γ-tubulin clarify the role of GTP in microtubule assembly. Proc. Natl Acad. Sci. USA 105, 5378-5383 (2008). (Pubitemid 351753871)
7. Kollman, J. M., Merdes, A., Mourey, L. & Agard, D. A. Microtubule nucleation by-tubulin complexes. Nat. Rev. Mol. Cell Biol. 12, 709-721 (2011).
8. Pereira, G. & Schiebel, E. Centrosome-microtubule nucleation. J. Cell Sci. 110, 295-300 (1997). (Pubitemid 27095650)
9. Spang, A., Geissler, S., Grein, K. & Schiebel, E. 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 (1996). (Pubitemid 26250710)
10. Zheng, Y., Jung, K. & Oakley, B. R.-Tubulin is present in Drosophila melanogaster and Homo sapiens and is associated with the centrosome. Cell 65, 817-823 (1991). (Pubitemid 121001313)
11. Knop, M., Pereira, G., Geissler, S., Grein, K. & Schiebel, E. 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 (1997). (Pubitemid 27151950)
12. 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, 6985-6995 (1997). (Pubitemid 27520799)
13. Kollman, J. M. et al. The structure of the γ-tubulin small complex: implications of its architecture and fiexibility for microtubule nucleation. Mol. Biol. Cell 19, 207-215 (2008). (Pubitemid 351186146)
14. Knop, M. & Schiebel, E. Receptors determine the cellular localization of a-tubulin complex and thereby the site of microtubule formation. EMBO J. 17, 3952-3967 (1998). (Pubitemid 28333981)
15. 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, 2201-2216 (1998). (Pubitemid 28373634)
16. Kollman, J. M., Polka, J. K., Zelter, A., Davis, T. N. & Agard, D. A. Microtubule nucleating γ-TuSC assembles structures with 13-fold microtubule-like symmetry. Nature 466, 879-882 (2010).
17. Aldaz, H., Rice, L. M., Stearns, T. & Agard, D. A. Insights into microtubule nucleation from the crystal structure of human γ-tubulin. Nature 435, 523-527 (2005). (Pubitemid 40734251)
18. Shang, Y., Tsao, C. C. & Gorovsky, M. A. Mutational analyses reveal a novel function of the nucleotide-binding domain of gamma-tubulin in the regulation of basal body biogenesis. J. Cell Biol. 171, 1035-1044 (2005). (Pubitemid 41815835)
19. Nishimura, K., Fukagawa, T., Takisawa, H., Kakimoto, T. & Kanemaki, M. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat. Methods 6, 917-922 (2009).
20. Ghaemmaghami, S. et al. Global analysis of protein expression in yeast. Nature 425, 737-741 (2003). (Pubitemid 37314318)
21. Erlemann, S. et al. An extended γ-tubulin ring functions as a stable platform in microtubule nucleation. J. Cell Biol. 197, 59-74 (2012).
22. Paluh, J. L. et al. A mutation in γ-tubulin alters microtubule dynamics and organization and is synthetically lethal with the kinesin-like protein pkl1p. Mol. Biol. Cell 11, 1225-1239 (2000). (Pubitemid 30211026)
23. Zimmerman, S. & Chang, F. Effects of γ-tubulin complex proteins on microtubule nucleation and catastrophe in fission yeast. Mol. Biol. Cell 16, 2719-2733 (2005). (Pubitemid 40741219)
24. Jung, M. K., Prigozhina, N., Oakley, C. E., Nogales, E. & Oakley, B. R. Alaninescanning mutagenesis of Aspergillus γ-tubulin yields diverse and novel phenotypes. Mol. Biol. Cell 12, 2119-2136 (2001). (Pubitemid 33049704)
25. Tange, Y., Fujita, A., Toda, T. & Niwa, O. Functional dissection of the γ-tubulin complex by suppressor analysis of gtb1 and alp4 mutations in Schizosaccharomyces pombe. Genetics 167, 1095-1107 (2004). (Pubitemid 39045620)
26. Machin, N. A., Lee, J. M. & Barnes, G. Microtubule stability in budding yeast-characterization and dosage suppression of a benomyl-dependent tubulin mutant. Mol. Biol. Cell 6, 1241-1259 (1995).
27. Kitamura, E. et al. Kinetochores generate microtubules with distal plus ends: their roles and limited lifetime in mitosis. Dev. Cell 18, 248-259 (2010).
28. Ortiz, J., Funk, C., Schafer, A. & Lechner, J. Stu1 inversely regulates kinetochore capture and spindle stability. Genes Dev. 23, 2778-2791 (2009).
29. Goh, P. Y. & Kilmartin, J. V. NDC10: a gene involved in chromosome segregation in Saccharomyces cerevisiae. J. Cell Biol. 121, 503-512 (1993). (Pubitemid 23131263)
30. Nogales, E., Wolf, S. G. & Downing, K. H. Structure of the aβ tubulin dimer by electron crystallography. Nature 391, 199-203 (1998). (Pubitemid 28092482)
31. Anders, K. R. & Botstein, D. Dominant-lethal α-tubulin mutants defective in microtubule depolymerization in yeast. Mol. Biol. Cell 12, 3973-3986 (2001). (Pubitemid 34001086)
32. Oliva, M. A., Cordell, S. C. & Lowe, J. Structural insights into FtsZ protofilament formation. Nat. Struct. Mol. Biol. 11, 1243-1250 (2004).
33. Huffaker, T. C., Thomas, J. H. & Botstein, D. Diverse effects of β-tubulin mutations on microtubule formation and function. J. Cell Biol. 106, 1997-2010 (1988).
34. Zabala, J. C., Fontalba, A. & Avila, J. Tubulin folding is altered by mutations in a putative GTP-binding motif. J. Cell Sci. 109, 1471-1478 (1996). (Pubitemid 26190496)
35. Tian, G., Bhamidipati, A., Cowan, N. J. & Lewis, S. A. Tubulin folding cofactors as GTPase-activating proteins. GTP hydrolysis and the assembly of the α/β-tubulin heterodimer. J. Biol. Chem. 274, 24054-24058 (1999).
36. Hendrickson, T. W., Yao, J., Bhadury, S., Corbett, A. H. & Joshi, H. C. Conditional mutations in gamma-tubulin reveal its involvement in chromosome segregation and cytokinesis. Mol. Biol. Cell 12, 2469-2481 (2001). (Pubitemid 33051969)
37. Cuschieri, L., Miller, R. K. & Vogel, J. γ-tubulin is required for proper recruitment and assembly of Kar9-Bim1 complexes in budding yeast. Mol. Biol. Cell 17, 4420-4434 (2006). (Pubitemid 44522060)
38. Dougherty, C. A., Sage, C. R., Davis, A. & Farrell, K. W. Mutation in the β-tubulin signature motif suppresses microtubule GTPase activity and dynamics, and slows mitosis. Biochemistry 40, 15725-15732 (2001). (Pubitemid 34015201)
39. Oegema, K. et al. Characterization of two related Drosophila γ-tubulin complexes that differ in their ability to nucleate microtubules. J. Cell Biol. 144, 721-733 (1999). (Pubitemid 29234550)
40. Lin, T. C. et al. Phosphorylation of the yeast-tubulin Tub4 regulates microtubule function. PLoS One 6, e19700 (2011).
41. Schwede, T., Kopp, J., Guex, N. & Peitsch, M. C. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385 (2003). (Pubitemid 37442164)
42. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 (2006). (Pubitemid 43205406)
43. Eswar, N. et al. Comparative protein structure modeling using MODELLER. Curr. Protoc. Bioinformatics Ch. 5, Unit 5.6, http://dx.doi.org/10.1002/ 0471250953. bi0506s15 (2006).
44. Guthrie, C. & Fink, G. R. Guide to yeast genetics and molecular biology. Methods Enzymol. 194, 429-663 (1991).
45. Janke, C. et al. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962 (2004). (Pubitemid 39206863)
46. Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, 1989).
47. Sezen, B., Seedorf, M. & Schiebel, E. The SESA network links duplication of the yeast centrosome with the protein translation machinery. Genes Dev. 23, 1559-1570 (2009).
48. Kosco, K. A. et al. Control of microtubule dynamics by Stu2p is essential for spindle orientation and metaphase chromosome alignment in yeast. Mol. Biol. Cell 12, 2870-2880 (2001). (Pubitemid 33051950)
49. Kupke, T. et al. Targeting of Nbp1 to the inner nuclear membrane is essential for spindle pole body duplication. EMBO J. 16, 3337-3352 (2011).
50. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007). (Pubitemid 44880785)
51. Hohn, M. et al. SPARX, a new environment for Cryo-EM image processing. J. Struct. Biol. 157, 47-55 (2007). (Pubitemid 44880795)
52. Vinh, D. B. N., Kern, J. W., Hancock, W. O., Howard, J. & Davis, T. N. Reconstitution and characterization of the budding yeast γ-tubulin complex. Mol. Biol. Cell 13, 1144-1157 (2002). (Pubitemid 34309612)