Stathmin regulates centrosomal nucleation of microtubules and tubulin dimer/polymer partitioning

Molecular Biology of the Cell

Volumn 20, Issue 15, 2009, Pages 3451-3458

  Ringhoff, Danielle N ^a   Cassimeris, Lynne ^a  

^a LEHIGH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYAN FLUORESCENT PROTEIN; DIMER; MESSENGER RNA; POLYMER; STATHMIN;

ANIMAL CELL; ARTICLE; CENTROSOME; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; FIBROBLAST; METAPHASE; MICROTUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CENTROSOME; EMBRYO, MAMMALIAN; FEMALE; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENOTYPE; GREEN FLUORESCENT PROTEINS; LLC-PK1 CELLS; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; POLYMERS; PREGNANCY; PROTEIN MULTIMERIZATION; STATHMIN; SWINE; TUBULIN;

SUS; VERTEBRATA;

EID: 68149083108     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-02-0140     Document Type: Article

References (49)

1. Belmont, L., and Mitchison, T. (1996). Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell 84, 623-631. (Pubitemid 26071742)
2. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., and Wheeler, D. L. (2007). GenBank. Nucleic Acids Res. 35, D21-25.
3. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
4. 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. (Pubitemid 23139861)
5. Cassimeris, L. (2002). The oncoprotein 18/stathmin family of microtubule destabilizers. Curr. Opin. Cell Biol. 14, 18-24.
6. Curmi, P., Noguès, C., Lachkar, S., Carelle, N., Gonthier, M., Sobel, A., Lidereau, R., and Bièche, I. (2000). Overexpression of stathmin in breast carcinomas points out to highly proliferative tumours. Br. J. Cancer 82, 142-150. (Pubitemid 30008973)
7. Desai, A., and Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell. Dev. Biol. 13, 83-117.
8. Fletcher, G., and Rorth, P. (2007). Drosophila stathmin is required to maintain tubulin pools. Curr. Biol. 17, 1067-1071.
9. Graessmann, A., Graessmann, M., and Mueller, C. (1980). Microinjection of early SV40 DNA fragments and T antigen. Methods Enzymol. 65, 816-825.
10. Gregoretti, I., Margolin, G., Alber, M., and Goodson, H. (2006). Insights into cytoskeletal behavior from computational modeling of dynamic microtubules in a cell-like environment. J. Cell Sci. 119, 4781-4788. (Pubitemid 44964274)
11. Gründemann, J., Schlaudraff, F., Haeckel, O., and Liss, B. (2008). Elevated alpha-synuclein mRNA levels in individual UV-laser-microdissected dopaminergic substantia nigra neurons in idiopathic Parkinson's disease. Nucleic Acids Res. 36, e38. (Pubitemid 351575094)
12. Hiller, G., and Weber, K. (1978). Radioimmunoassay for tubulin: a quantitative comparison of the tubulin content of different established tissue culture cells and tissues. Cell 14, 795-804. (Pubitemid 8405170)
13. 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.
14. Holmfeldt, P., Brännström, 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.
15. 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.
16. Howell, B., Deacon, H., and Cassimeris, L. (1999a). Decreasing oncoprotein 18/stathmin levels reduces microtubule catastrophes and increases microtubule polymer in vivo. J. Cell Sci. 112, 3713-3722.
17. Howell, B., Hoffman, D., Fang, G., Murray, A., and Salmon, E. (2000). Visualization of Mad2 dynamics at kinetochores, along spindle fibers, and at spindle poles in living cells. J. Cell Biol. 150, 1233-1250. (Pubitemid 30728898)
18. Howell, B., Larsson, N., Gullberg, M., and Cassimeris, L. (1999b). Dissociation of the tubulin-sequestering and microtubule catastrophe-promoting activities of oncoprotein 18/stathmin. Mol. Biol. Cell 10, 105-118.
19. Kuriyama, R., and Borisy, G. (1981). 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, 822-826. (Pubitemid 12211171)
20. 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.
21. Larsson, N., Segerman, B., Howell, B., Fridell, K., Cassimeris, L., and Gullberg, M. (1999). Op18/stathmin mediates multiple region-specific tubulin and microtubule- regulating activities. J. Cell Biol. 146, 1289-1302. (Pubitemid 29477696)
22. 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.
23. Marklund, U., Larsson, N., Gradin, H., Brattsand, G., and Gullberg, M. (1996). Oncoprotein 18 is a phosphorylation-responsive regulator of microtubule dynamics. EMBO J. 15, 5290-5298. (Pubitemid 26336212)
24. Matthes, T., Wolff, A., Soubiran, P., Gros, F., and Dighiero, G. (1988). Antitubulin Antibodies. 2. Natural autoantibodies and induced antibodies recognize different epitopes on the tubulin molecule. J. Immunol. 141, 3135-3141.
25. Minotti, A., Barlow, S., and Cabral, F. (1991). Resistance to antimitotic drugs in Chinese hamster ovary cells correlates with changes in the level of polymerized tubulin. J. Biol. Chem. 266, 3987-3994.
26. Mistry, S., Bank, A., and Atweh, G. (2005). Targeting stathmin in prostate cancer. Mol Cancer Ther. 4, 1821-1829.
27. Mitchison, T., and Kirschner, M. (1987). Dynamic instability of microtubule growth. Nature 312, 237-242.
28. Nguyen, H., Gruber, D., and Bulinski, J. (1999). Microtubule-associated protein 4 (MAP4) regulates assembly, protomer-polymer partitioning and synthesis of tubulin in cultured cells. J. Cell Sci. 112, 1813-1824. (Pubitemid 29338807)
29. Parsons, S., and Salmon, E. (1997). Microtubule assembly in clarified Xenopus egg extracts. Cell Motil. Cytoskeleton 36, 1-11.
30. Piehl, M., and Cassimeris, L. (2003). Organization and dynamics of growing microtubule plus ends during early mitosis. Mol. Biol. Cell 14, 916-925.
31. Piehl, M., Tulu, U., Wadsworth, P., and Cassimeris, L. (2004). Centrosome maturation: measurement of microtubule nucleation throughout the cell cycle by using GFP-tagged EB1. Proc. Natl. Acad. Sci. USA 101, 1584-1588.
32. Rana, S., Maples, P., Senzer, N., and Nemunaitis, J. (2008). Stathmin 1, a novel therapeutic target for anticancer activity. Expert Rev. Anticancer Ther. 8, 1461-1470.
33. Rodionov, V., Nadezhdina, E., and Borisy, G. (1999). Centrosomal control of microtubule dynamics. Proc. Natl. Acad. Sci. USA 96, 115-120.
34. Rusan, N. M., Fagerstrom, C. J., Yvon, A. M., and Wadsworth, P. (2001). Cell cycle-dependent changes in microtubule dynamics in living cells expressing green fluorescent protein-alpha tubulin. Mol. Biol. Cell 12, 971-980.
35. Saxton, W., Stemple, D., Leslie, R., Salmon, E., Zavortink, M., and McIntosh, J. (1984). Tubulin dynamics in cultured mammalian cells. J. Cell Biol. 99, 2175-2186. (Pubitemid 15181881)
36. 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.
37. Sellin, M. E., Holmfeldt, P., Stenmark, S., and Gullberg, M. (2008). Global regulation of the interphase microtubule system by abundantly expressed Op18/Strathmin. Mol. Biol. Cell 19, 2897-2906.
38. Shumyatsky, G. P., et al. (2005). Stathmin, a gene enriched in the amygdala, controls both learned and innate fear. Cell 123, 697-709.
39. Steinmetz, M. (2007). Structure and thermodynamics of the tubulin-stathmin interaction. J. Struct .Biol. 158, 137-147.
40. Tessarollo, L. (2001). Manipulating mouse embryonic stem cells. Methods Mol. Biol. 158, 47-63.
41. Tournebize, R., Andersen, S., Verde, F., Dorée, M., Karsenti, E., and Hyman, A. (1997). Distinct roles of PP1 and PP2A-like phosphatases in control of microtubule dynamics during mitosis. EMBO J. 16, 5537-5549. (Pubitemid 27399846)
42. Vasquez, R. J., Gard, D. L., and Cassimeris, L. (1994). XMAP from Xenopus eggs promotes rapid plus end assembly of microtubules and rapid microtubule polymer turnover. J. Cell Biol. 127, 985-993.
43. Vorobjev, I. A., Rodionov, V. I., Maly, I. V., and Borisy, G. G. (1999). Contribution of plus and minus end pathways to microtubule turnover. J. Cell Sci. 112, 2277-2289.
44. Walker, R. A., O'Brien, E. T., Pryer, N. K., Soboeiro, M. F., Voter, W. A., Erickson, H. P., and Salmon, E. D. (1988). Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J. Cell Biol. 107, 1437-1448.
45. Warren, J. C., and Cassimeris, L. (2007). The contributions of microtubule stability and dynamic instability to adenovirus nuclear localization efficiency. Cell Motil. Cytoskeleton 64, 675-689.
46. Warren, J. C., Rutkowski, A., and Cassimeris, L. (2006). Infection with replication- deficient adenovirus induces changes in the dynamic instability of host cell microtubules. Mol. Biol. Cell 17, 3557-3568.
47. Westberry, J., Prewitt, A., and Wilson, M. (2008). Epigenetic regulation of the estrogen receptor alpha promoter in the cerebral cortex following ischemia in male and female rats. Neuroscience 152, 982-989.
48. Wittmann, T., Bokoch, G., and Waterman-Storer, C. (2004). Regulation of microtubule destabilizing activity of Op18/stathmin downstream of Rac1. J. Biol. Chem. 279, 6196-6203.
49. Zhai, Y., Kronebusch, P., Simon, P., and Borisy, G. (1996). Microtubule dynamics at the G2/M transition: abrupt breakdown of cytoplasmic microtubules at nuclear envelope breakdown and implications for spindle morphogenesis. J. Cell Biol. 135, 201-214. (Pubitemid 26337748)