Global regulation of the interphase microtubule system by abundantly expressed Op18/stathmin

Molecular Biology of the Cell

Volumn 19, Issue 7, 2008, Pages 2897-2906

  Sellin, Mikael E ^a   Holmfeldt, Per ^a   Stenmark, Sonja ^a   Gullberg, Martin ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

COLCHICINE; HETERODIMER; MESSENGER RNA; STATHMIN; TUBULIN;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL TYPE; CONTROLLED STUDY; GENE CONTROL; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTERPHASE; LEUKEMIA CELL; MICROTUBULE ASSEMBLY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN SYNTHESIS;

COLCHICINE; DIMERIZATION; GENE EXPRESSION REGULATION; HUMANS; INTERPHASE; JURKAT CELLS; K562 CELLS; MICROTUBULE PROTEINS; MICROTUBULES; PHENOTYPE; POLYMERS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA PROCESSING, POST-TRANSCRIPTIONAL; STATHMIN; TUBULIN;

EID: 51349160529     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-01-0058     Document Type: Article

References (42)

1. Bachurski, C. J., Theodorakis, N. G., Coulson, R. M., and Cleveland, D. W. (1994). An amino-terminal tetrapeptide specifies cotranslational degradation of beta-tubulin but not alpha-tubulin mRNAs. Mol. Cell Biol. 14, 4076-4086.
2. Barlow, S. B., Gonzalez-Garay, M. L., and Cabral, F. (2002). Paclitaxel-dependent mutants have severely reduced microtubule assembly and reduced tubulin synthesis. J. Cell Sci. 115, 3469-3478.
3. Belmont, L. D., and Mitchison, T. J. (1996). Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell 84, 623-631.
4. Boggs, B., and Cabral, F. (1987). Mutations affecting assembly and stability of tubulin: evidence for a nonessential beta-tubulin in CHO cells. Mol. Cell Biol. 7, 2700-2707.
5. Brattsand, G., Roos, G., Marklund, U., Ueda, H., Landberg, G., Nanberg, E., Sideras, P., and Gullberg, M. (1993). Quantitative analysis of the expression and regulation of an activation-regulated phosphoprotein (oncoprotein 18) in normal and neoplastic cells. Leukemia 7, 569-579.
6. Caron, J. M., Jones, A. L., and Kirschner, M. W. (1985). Autoregulation of tubulin synthesis in hepatocytes and fibroblasts. J. Cell Biol. 101, 1763-1772.
7. Cassimeris, L. (2002). The oncoprotein 18/stathmin family of microtubule destabilizers. Curr. Opin. Cell Biol. 14, 18-24.
8. Cleveland, D. W. (1989). Autoregulated control of tubulin synthesis in animal cells. Curr. Opin. Cell Biol. 1, 10-14.
9. Deacon, H., Mitchison, T. J., and Gullberg, M. (1999). Op18/stathmin, Part 2. Tubulin and associated proteins. In: Guidebook to the Cytoskeletal and Motor Proteins, 2nd ed., ed. T. Kreis and R. Vale, Oxford, United Kingdom: Oxford University Press, 222-224.
10. Desai, A., and Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83-117.
11. Fletcher, G., and Rorth, P. (2007). Drosophila stathmin is required to maintain tubulin pools. Curr. Biol. 17, 1067-1071.
12. Gay, D. A., Yen, T. J., Lau, J. T., and Cleveland, D. W. (1987). Sequences that confer beta-tubulin autoregulation through modulated mRNA stability reside within exon 1 of a beta-tubulin mRNA. Cell 50, 671-679.
13. Gigant, B., Curmi, P. A., Martin-Barbey, C., Charbaut, E., Lachkar, S., Lebeau, L., Siavoshian, S., Sobel, A., and Knossow, M. (2000). The 4 A X-ray structure of a tubulin:stathmin-like domain complex. Cell 102, 809-816.
14. Gonzalez-Garay, M. L., and Cabral, F. (1996). α-Tubulin limits its own synthesis: evidence for a mechanism involving translational repression. J. Cell Biol. 135, 1525-1534.
15. Gradin, H. M., Larsson, N., Marklund, U., and Gullberg, M. (1998). Regulation of microtubule dynamics by extracellular signals: cAMP-dependent protein kinase switches off the activity of oncoprotein 18 in intact cells. J. Cell Biol. 140, 131-141.
16. Hanash, S. M., Strahler, J. R., Kuick, R., Chu, E. H., and Nichols, D. (1988). Identification of a polypeptide associated with the malignant phenotype in acute leukemia. J. Biol. Chem. 263, 12813-12815.
17. Holmfeldt, P., Brannstrom, K., Stenmark, S., and Gullberg, M. (2003a). Deciphering the cellular functions of the Op18/Stathmin family of microtubule-regulators by plasma membrane-targeted localization. Mol. Biol. Cell 14, 3716-3729.
18. Holmfeldt, P., Brannstrom, K., Stenmark, S., and Gullberg, M. (2006). Aneugenic activity of Op18/stathmin is potentiated by the somatic Q18->e mutation in leukemic cells. Mol. Biol. Cell 17, 2921-2930.
19. Holmfeldt, P., Brattsand, G., and Gullberg, M. (2002). MAP4 counteracts microtubule catastrophe promotion but not tubulin-sequestering activity in intact cells. Curr. Biol. 12, 1034-1039.
20. Holmfeldt, P., Brattsand, G., and Gullberg, M. (2003b). Interphase and monoastral-mitotic phenotypes of overexpressed MAP4 are modulated by free tubulin concentrations. J. Cell Sci. 116, 3701-3711.
21. Holmfeldt, P., Larsson, N., Segerman, B., Howell, B., Morabito, J., Cassimeris, L., and Gullberg, M. (2001). The catastrophe-promoting activity of ectopic Op18/stathmin is required for disruption of mitotic spindles but not interphase microtubules. Mol. Biol. Cell 12, 73-83.
22. Holmfeldt, P., Stenmark, S., and Gullberg, M. (2004). Differential functional interplay of TOGp/XMAP215 and the KinI kinesin MCAK during interphase and mitosis. EMBO J. 23, 627-637.
23. Holmfeldt, P., Stenmark, S., and Gullberg, M. (2007). Interphase-specific phosphorylation-mediated regulation of tubulin dimer partitioning in human cells. Mol. Biol. Cell 18, 1909-1917.
24. Horwitz, S. B., Shen, H. J., He, L., Dittmar, P., Neef, R., Chen, J., and Schubart, U. K. (1997). The microtubule-destabilizing activity of metablastin (p19) is controlled by phosphorylation. J. Biol. Chem. 272, 8129-8132.
25. Howell, B., Deacon, H., and Cassimeris, L. (1999). Decreasing oncoprotein 18/stathmin levels reduces microtubule catastrophes and increases microtubule polymer in vivo. J. Cell Sci. 112, 3713-3722.
26. Jourdain, L., Curmi, P., Sobel, A., Pantaloni, D., and Carlier, M. F. (1997). Stathmin: a tubulin-sequestering protein which forms a ternary T2S complex with two tubulin molecules. Biochemistry 36, 10817-10821.
27. Koppel, J., Boutterin, M. C., Doye, V., Peyro-Saint-Paul, H., and Sobel, A. (1990). Developmental tissue expression and phylogenetic conservation of stathmin, a phosphoprotein associated with cell regulations. J. Biol. Chem. 265, 3703-3707.
28. Larsson, N., Marklund, U., Gradin, H. M., Brattsand, G., and Gullberg, M. (1997). Control of microtubule dynamics by oncoprotein 18, dissection of the regulatory role of multisite phosphorylation during mitosis. Mol. Cell Biol. 17, 5530-5539.
29. Larsson, N., Melander, H., Marklund, U., Osterman, O., and Gullberg, M. (1995). G2/M transition requires multisite phosphorylation of oncoprotein 18 by two distinct protein kinase systems. J. Biol. Chem. 270, 14175-14183.
30. Liedtke, W., Leman, E. E., Fyffe, R. E., Raine, C. S., and Schubart, U. K. (2002). Stathmin-deficient mice develop an age-dependent axonopathy of the central and peripheral nervous systems. Am. J. Pathol. 160, 469-480.
31. Luduena, R. F. (1998). Multiple forms of tubulin: different gene products and covalent modifications. Int. Rev. Cytol. 178, 207-275.
32. Marklund, U., Larsson, N., Gradin, H. M., Brattsand, G., and Gullberg, M. (1996). Oncoprotein 18 is a phosphorylation-responsive regulator of microtubule dynamics. EMBO J. 15, 5290-5298.
33. Marklund, U., Osterman, O., Melander, H., Bergh, A., and Gullberg, M. (1994). The phenotype of a "Cdc2 kinase target site-deficient" mutant of oncoprotein 18 reveals a role of this protein in cell cycle control. J. Biol. Chem. 269, 30626-30635.
34. Melander Gradin, H., Marklund, U., Larsson, N., Chatila, T. A., and Gullberg, M. (1997). Regulation of microtubule dynamics by Ca2+/calmodulin- dependent kinase IV/Gr-dependent phosphorylation of oncoprotein 18. Mol. Cell Biol. 17, 3459-3467.
35. Mori, N., and Morii, H. (2002). SCG10-related neuronal growth-associated proteins in neural development, plasticity, degeneration, and aging. J. Neurosci. Res. 70, 264-273.
36. Narishige, T., Blade, K. L., Ishibashi, Y., Nagai, T., Hamawaki, M., Menick, D. R., Kuppuswamy, D., and Cooper, G. T. (1999). Cardiac hypertrophic and developmental regulation of the β-tubulin multigene family. J. Biol. Chem. 274, 9692-9697.
37. Pachter, J. S., Yen, T. J., and Cleveland, D. W. (1987). Autoregulation of tubulin expression is achieved through specific degradation of polysomal tubulin mRNAs. Cell 51, 283-292.
38. Schubart, U. K., Yu, J., Amat, J. A., Wang, Z., Hoffmann, M. K., and Edelmann, W. (1996). Normal development of mice lacking metablastin (P19), a phosphoprotein implicated in cell cycle regulation. J. Biol. Chem. 271, 14062-14066.
39. Shumyatsky, G. P. et al. (2005). stathmin, a gene enriched in the amygdala, controls both learned and innate fear. Cell 123, 697-709.
40. Steinmetz, M. O., Kammerer, R. A., Jahnke, W., Goldie, K. N., Lustig, A., and van Oostrum, J. (2000). Op18/stathmin caps a kinked protofilament-like tubulin tetramer. EMBO J. 19, 572-580.
41. Theodorakis, N. G., and Cleveland, D. W. (1992). Physical evidence for cotranslational regulation of beta-tubulin mRNA degradation. Mol. Cell Biol. 12, 791-799.
42. Wang, Y., Tian, G., Cowan, N. J., and Cabral, F. (2006). Mutations affecting β-tubulin folding and degradation. J. Biol. Chem. 281, 13628-13635.