Interphase and monoastral-mitotic phenotypes of overexpressed MAP4 are modulated by free tubulin concentrations

Journal of Cell Science

Volumn 116, Issue 18, 2003, Pages 3701-3711

  Holmfeldt, Per ^a   Brattsand, Goran ^a   Gullberg, Martin ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

MAP4; Microtubule associated proteins; Microtubules; Recombinant fusion proteins; Tubulin

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN 4; STATHMIN; TUBULIN;

ARTICLE; BINDING AFFINITY; CELL CYCLE PHASE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CHIMERA; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INTERPHASE; LEUKEMIA CELL; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION;

FLOW CYTOMETRY; HUMANS; INTERPHASE; JURKAT CELLS; K562 CELLS; MICROSCOPY, FLUORESCENCE; MICROTUBULE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; STATHMIN; TUBULIN; TUMOR CELLS, CULTURED;

EID: 0141836838     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00685     Document Type: Article

References (39)

1. Andersen, S. S. and Wittmann, T. (2002). Toward reconstitution of in vivo microtubule dynamics in vitro. Bioessays 24, 305-307.
2. Barlow, S., Gonzalez-Garay, M. L., West, R. R., Olmsted, J. B. and Cabral, F. (1994). Stable expression of heterologous microtubule-associated proteins (MAPs) in Chinese hamster ovary cells: evidence for differing roles of MAPs in microtubule organization. J. Cell Biol. 126, 1017-1029.
3. Bulinski, J. C. and Borisy, G. G. (1980). Immunofluorescence localization of HeLa cell microtubule-associated proteins on microtubules in vitro and in vivo. J. Cell Biol. 87, 792-801.
4. Cassimeris, L. (1999). Accessory protein regulation of microtubule dynamics throughout the cell cycle. Curr. Opin. Cell Biol. 11, 134-141.
5. Chang, W., Gruber, D., Chari, S., Kitazawa, H., Hamazumi, Y., Hisanaga, S. and Bulinski, J. C. (2001). Phosphorylation of MAP4 affects microtubule properties and cell cycle progression. J. Cell Sci. 114, 2879-2887.
6. Chapin, S. J., Lue, C. M., Yu, M. T. and Bulinski, J. C. (1995). Differential expression of alternatively spliced forms of MAP4: a repertoire of structurally different microtubule-binding domains. Biochemistry 34, 2289-2301.
7. Charbaut, E., Curmi, P. A., Ozon, S., Lachkar, S., Redeker, V. and Sobel, A. (2001). Stathmin family proteins display specific molecular and tubulin binding properties. J. Biol. Chem. 276, 16146-16154.
8. Charrasse, S., Schroeder, M., Gauthier-Rouviere, C., Ango, F., Cassimeris, L., Gard, D. L. and Larroque, C. (1998). The TOGp protein is a new human microtubule-associated protein homologous to the Xenopus XMAP215. J. Cell Sci. 111, 1371-1383.
9. Cleveland, D. W., Lopata, M. A., Sherline, P. and Kirschner, M. W. (1981). Unpolymerized tubulin modulates the level of tubulin mRNAs. Cell 25, 537-546.
10. Desai, A. and Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83-117.
11. Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E. M. and Mandelkow, E. (1997). MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89, 297-308.
12. Ebneth, A., Drewes, G. and Mandelkow, E. (1999). Phosphorylation of MAP2c and MAP4 by MARK kinases leads to the destabilization of microtubules in cells. Cell Motil. Cytoskeleton 44, 209-224.
13. Epstein, R. J., Watson, J. V. and Smith, P. J. (1988). Subpopulation analysis of drug-induced cell-cycle delay in human tumor cells using 90 degrees light scatter. Cytometry 9, 349-358.
14. 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.
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. He, Q., Beyers, A. D., Barclay, A. N. and Williams, A. F. (1988). A role in transmembrane signaling for the cytoplasmic domain of the CD2 T lymphocyte surface antigen. Cell 54, 979-984.
17. Hendzel, M. J., Wei, Y., Mancini, M. A., Van Hooser, A., Ranalli, T., Brinkley, B. R., Bazett-Jones, D. P. and Allis, C. D. (1997). Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348-360.
18. 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.
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. Howell, B., Larsson, N., Gullberg, M. and Cassimeris, L. (1999). Dissociation of the tubulin-sequestering and microtubule catastrophe-promoting activities of oncoprotein 18/stathmin. Mol. Biol. Cell 10, 105-118.
21. Kapoor, T. M., Mayer, T. U., Coughlin, M. L. and Mitchison, T. J. (2000). Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J. Cell Biol. 150, 975-988.
22. Kinoshita, K., Arnal, I., Desai, A., Drechsel, D. N. and Hyman, A. A. (2001). Reconstitution of physiological microtubule dynamics using purified components. Science 294, 1340-1343.
23. Kinoshita, K., Habermann, B. and Hyman, A. A. (2002). XMAP215: a key component of the dynamic microtubule cytoskeleton. Trends Cell Biol. 12, 267-273.
24. 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.
25. 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.
26. 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.
27. Mayer, T. U., Kapoor, T. M., Haggarty, S. J., King, R. W., Schreiber, S. L. and Mitchison, T. J. (1999). Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286, 971-974.
28. Nguyen, H. L., Chari, S., Gruber, D., Lue, C. M., Chapin, S. J. and Bulinski, J. C. (1997). Overexpression of full- or partial-length MAP4 stabilizes microtubules and alters cell growth. J. Cell Sci. 110, 281-294.
29. Nguyen, H. L., Gruber, D. and Bulinski, J. C. (1999). Microtubule-associated protein 4 (MAP4) regulates assembly, protomer-polymer partitioning and synthesis of tubulin in cultured cells. J. Cell Sci. 112, 1813-1824.
30. Olmsted, J. B. (1999). MAP4, Part 2. Tubulin and associated proteins. In Guidebook to the Cytoskeletal and Motor Proteins, 2nd edn (ed. T. Kreis and R. Vale), pp. 212-214. Oxford, UK: Oxford University Press.
31. Ookata, K., Hisanaga, S., Bulinski, J. C., Murofushi, H., Aizawa, H., Itoh, T. J., Hotani, H., Okumura, E., Tachibana, K. and Kishimoto, T. (1995). Cyclin B interaction with microtubule-associated protein 4 (MAP4) targets p34cdc2 kinase to microtubules and is a potential regulator of M-phase microtubule dynamics. J. Cell Biol. 128, 849-862.
32. Ookata, K., Hisanaga, S., Sugita, M., Okuyama, A., Murofushi, H., Kitazawa, H., Chari, S., Bulinski, J. C. and Kishimoto, T. (1997). MAP4 is the in vivo substrate for CDC2 kinase in HeLa cells: identification of an M-phase specific and a cell cycle-independent phosphorylation site in MAP4. Biochemistry 36, 15873-15883.
33. Tournebize, R., Popov, A., Kinoshita, K., Ashford, A. J., Rybina, S., Pozniakovsky, A., Mayer, T. U., Walczak, C. E., Karsenti, E. and Hyman, A. A. (2000). Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nat. Cell Biol. 2, 13-19.
34. Walczak, C. E. (2000). Microtubule dynamics and tubulin interacting proteins. Curr. Opin. Cell Biol. 12, 52-56.
35. Wang, X. M., Peloquin, J. G., Zhai, Y., Bulinski, J. C. and Borisy, G. G. (1996). Removal of MAP4 from microtubules in vivo produces no observable phenotype at the cellular level. J. Cell Biol. 132, 345-357.
36. Yoshida, T., Imanaka-Yoshida, K., Murofushi, H., Tanaka, J., Ito, H. and Inagaki, M. (1996). Microinjection of intact MAP-4 and fragments induces changes of the cytoskeleton in PtK2 cells. Cell Motil. Cytoskeleton 33, 252-262.
37. Zhai, Y. and Borisy, G. G. (1994). Quantitative determination of the proportion of microtubule polymer present during the mitosis-interphase transition. J. Cell Sci. 107, 881-890.
38. Zhai, Y., Kronebusch, P. J., Simon, P. M. and Borisy, G. 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.
39. Zhang, C. C., Yang, J. M., White, E., Murphy, M., Levine, A. and Hait, W. N. (1998). The role of MAP4 expression in the sensitivity to paclitaxel and resistance to vinca alkaloids in p53 mutant cells. Oncogene 16, 1617-1624.