Cell cycle-dependent phosphorylation of the 77 kDa echinoderm microtubule-associated protein (EMAP) in vivo and association with the p34cdc2 kinase

Journal of Cell Science

Volumn 109, Issue 12, 1996, Pages 2885-2893

  Brisch, Ellen ^a   Daggett, Melissa A F ^a   Suprenant, Kathy A ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

Cell cycle; Cell division; Cytoskeleton; Mitosis; MPF; p34cdc2 kinase

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN; PROTEIN KINASE;

ANIMAL CELL; ARTICLE; ECHINODERM; EMBRYO; INTERPHASE; MITOSIS; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SEA URCHIN;

ANIMALS; CDC28 PROTEIN KINASE, S CEREVISIAE; CELL CYCLE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR WEIGHT; PHOSPHORYLATION; SEA URCHINS; SERINE;

ANIMALIA; ECHINODERMATA; ECHINOIDEA;

EID: 0030447533     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. Alfa, C. E., Ducommun, B., Beach, D. and Hyams, J. S. (1990). Distinct nuclear and spindle pole body population of cyclin-cdc2 in fission yeast. Nature 347, 680-682.
2. Andersen, S. S. L., Buendia, B., Dominiguez, J. E., Sawyer, A. and Karsenti, E. (1994). Effect on microtubule dynamics of XMAP 230, a microtubule-associated protein present in Xenopus laevis eggs and dividing cells. J. Cell Biol. 127, 1289-1299.
3. Andreasson, P. R. and Margolis, R. L. (1994). Microtubule dependency of p34cdc2 inactivation and mitotic exit in mammalian cells. J. Cell Biol. 127, 789-802.
4. Bailly, E., Pines, J., Hunter, T. and Bornens, M. (1989). p34cdc2 kinase is located in both nucleus and cytoplasm: part is centrosomally associated at G2/M and enters vesicles at anaphase. EMBO J. 13, 3985-3995.
5. Ballinger, D. G. and Hunt, T. (1981). Fertilization of sea urchin eggs is accompanied by 40S ribosomal subunit phosphorylation. Dev. Biol. 87, 277-285.
6. Belmont, L. D., Hyman, A., Sawin, K. E. and Mitchison, T. J. (1990). Realtime visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell 62, 579-589.
7. 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.
8. Bestor, T. H. and Schatten, G. (1981). Anti-tubulin immunofluorescence microscopy of microtubules present during the pronuclear movements of sea urchin fertilization. Dev. Biol. 88, 80-91.
9. Buendia, B., Draetta, G. and Karsenti, E. (1992). Regulation of the microtubule nucleating activity of centrosomes in Xenopus egg extracts: role of cyclin A-associated protein kinase. J. Cell Biol. 116, 1431-1442.
10. Cassimeris, L. (1993). Regulation of microtubule dynamic instability. Cell Motil. Cytoskel. 26, 275-281.
11. Coleman, T. R. and Dunphy, W. G. (1994). Cdc2 regulatory factors. Curr. Opin. Cell Biol. 6, 877-882.
12. Doxsey, S. J., Stein, P., Evans, L., Calarco, P. D. and Kirschner, M. (1994). Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76, 639-650.
13. Edgecombe, M., Patel, R. and Whitaker, M. (1991). A cyclin-abundance cycle-independent p34cdc2 tyrosine phosphorylation cycle in early sea urchin embryos. EMBO J. 10, 3769-3775.
14. Evans, T., Rosenthal, E. T., Youngbloom, J., Distel, D. and Hunt, T. (1983). Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33, 389-396.
15. Faruki, S. and Karsenti, E. (1994). Purification of microtubule proteins from Xenopus egg extracts: identification of a MAP-4 like protein. Cell Motil. Cytoskel. 28, 108-118.
16. Faux, M. C. and Scott, J. D. (1996). Molecular glue: kinase anchoring and scaffold proteins. Cell 85, 9-12.
17. Gard, D. L. and Kirschner, M. W. (1987). A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus end. J. Cell Biol. 105, 2203-2215.
18. Hollenbeck, P. J. (1993). Phosphorylation of neuronal kinesin heavy and light chains in vivo. J. Neurochem. 60, 2265-2275.
19. Inoue, S. and Salmon, E. D. (1995). Force generation by microtubule assembly/disassembly in mitosis and related movements. Mol. Biol. Cell 6, 1619-1640.
20. Johnston, J. A., Sloboda, R. D. and Silver, R. B. (1994). Phosphoprotein phosphatase 1 (PP1) is a component of the isolated sea urchin mitotic apparatus. Cell Motil. Cytoskel. 29, 280-290.
21. Kamps, M. A. and Sefton, B. M. (1989). Acid and base hydrolysis of phosphoproteins bound to immobilon: a rapid technique for the analysis of phosphoaminoacids in gel-fractionated proteins. Anal. Biochem. 176, 22-27.
22. Karsenti, E. (1993). Severing microtubules in mitosis. Curr. Biol. 3, 208-210.
23. Keller, T. C. S. and Rebhun, L. I. (1982). Strongylocentrotus purpuratus spindle tubulin. I. Characteristics of its polymerization and depolymerization in vitro. J. Cell Biol. 93, 788-796.
24. Labbe, J. C., Capony, J. C., Caput, D., Cavadore, J. C., Derancourt, J., Kaghad, M., Lelias, J. M., Picard, A. and Doree, M. (1989). MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. EMBO J. 8, 3053-3058.
25. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
26. Li, Q. and Suprenant, K. A. (1994). Molecular characterization of the 77 kD echinoderm microtubule-associated protein. J. Biol. Chem. 269, 31777-31784.
27. Lohka, M. J., Hayes, M. K. and Maller, J. L. (1988). Purification of maturation-promoting factor, an intracellular regulator of early mitotic events. Proc. Nat. Acad. Sci. USA 85, 3009-3013.
28. Lohka, M. F. (1989). Mitotic control by metaphase-promoting factor and cdc proteins. J. Cell Sci. 92. 131-135.
29. Maccioni, R. B. and Cambiazo, V. (1995). Role of microtubule-associated proteins in the control of microtubule assembly. Physiol. Rev. 75, 835-864.
30. Maldonado-Codina, G. and Glover, D. (1992). Cyclins A and B associate with chromatin and the polar regions of spindles, respectively, and do not undergo complete degradation at anaphase in syncytial Drosophila embryos. ]. Cell Biol. 116, 967-976.
31. Masson, D. and Kreis, T. E. (1995). Binding of E-MAP-115 to microtubules is regulated by cell cycle-dependent phosphorylation. J. Cell Biol. 131, 1015-1024.
32. McNally, F. J., Okawa, K., Iwamatsu, A. and Vale, R. (1996). Katanin, the microtubule-severing ATPase, is concentrated at the centrosomes. J. Cell Sci. 109, 561-567.
33. Meijer, L., Arion, D., Golsteyn, R., Pines, J., Brizuela, L., Hunt, T. and Beach, D. (1989). Cyclin is a component of the sea urchin egg M-phase specific histone H1 kinase. EMBO J. 8, 2275-2282.
34. Meijer, L., Azzi, L. and Wang, J. Y. J. (1991). Cyclin B targets p34cdc2 for tyrosine phosphorylation. EMBO J. 10, 1545-1554.
35. Mejillano, M. R., Barton, J. S., Nath, J. P. and Himes, R. H. (1990). GTP analogues interact with the tubulin exchangeable site during assembly and upon binding. Biochemistry 29, 1208-1216.
36. Mitchison, T. J. and Kirschner, M. W. (1984). Dynamic instability of microtubule growth. Nature 312, 237-242.
37. Nigg, E. A. (1993). Targets of cyclin-dependent protein kinases. Curr. Opin. Cell Biol. 3, 296-301.
38. Ookata, K., Hisanaga, S., Okano, T., Tachibana, K. and Kishimoto, T. (1992). Relocation and distinct subcellular localization of p34cdc2-cyclin B complex at meiosis reinitiation in starfish oocytes. EMBO J. 11, 1763-1772.
39. 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 interactions with microtubule-associated protein 4 (MAP 4) targets p34cdc2 kinase to microtubules and is a potential regulator of M-phase microtubule dynamics. J. Cell Biol. 128, 849-862.
40. Pines, J. and Hunter, T. (1991). Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell Biol. 115, 1-7.
41. Rattner, J. B., Lew, J. and Wang, J. H. (1990). p34cdc2 kinase is localized to distinct domains within the mitotic apparatus. Cell Motil. Cytoskel. 17, 227-235.
42. Riabowol, K., Draetta, G., Brizuela, L., Vandre, D. and Beach, D. (1989). The cdc2 kinase is a nuclear protein that is essential for mitosis in mammalian cells. Cell 57, 393-401.
43. Shiina, N., Moriguci, T., Ohta, K., Gotoh, Y. and Nishida, E. (1992) Regulation of a major microtubule-associated protein by MPF and MAP kinase. EMBO J. 11, 3977-3984.
44. Showman, R. M. and Foerder, C. A. (1979). Removal of the fertilization membrane of sea urchin embryos employing aminotriazole. Exp. Cell Res. 120, 253-255.
45. Silver, R. B., Cole, R. D. and Cande, W. Z. (1980). Isolation of mitotic apparatus containing vesicles with calcium sequestering activity. Cell 19, 505-516.
46. Sontag, E., Nunbhakdi-Craig, V., Bloom G. S. and Mumby, M. C. (1995). A novel pool of protein phosphatase 2A is associated with microtubules during the cell cycle. J. Cell Biol. 128, 1131-1144.
47. Stearns, T., Evans, L. and Kirschner, M. (1991). γ-Tubulin is a highly conserved component of the centrosome. Cell 65, 825-836.
48. Suprenant, K. A. and Marsh, J. C. (1987). Temperature and pH govern the self-assembly of microtubules from unfertilized sea urchin egg extracts. J. Cell Sci. 87, 71-84.
49. Suprenant, K. A., Dean, K., McKee, J. and Hake, S. (1993). EMAP, an echinoderm microtubule-associated protein found in microtubule-ribosome complexes. J. Cell Sci. 104, 445-456.
50. Tombes, R. M., Peloquin, J. G. and Borisy, G. G. (1991). Specific association of an M-phase kinase with isolated mitotic spindles and identification of two of its substrates as M AP4 and MAP1b. Cell Reg. 2, 861-874.
51. Tousson, A., Zeng, C., Brinkley, B. and Valdivia, M. (1991). Centrophilin: a novel mitotic spindle protein involved in microtubule nucleation. J. Cell Biol. 112, 427-440.
52. Towbin, H., Staehelin, T. and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Nat. Acad. Sci. USA 76, 4350-4354.
53. Turner, J. E., Minkoff, L. G., Martin, K. H., Misra, R. and Swensen, K. I. (1995). Oocyte activation and passage through the metaphase/anaphase transition of the meiotic cell cycle is blocked in clams by inhibitors of HMG-CoA reductase. J. Cell Biol. 128, 1145-1162.
54. Vale, R. D. (1991). Severing of stable microtubules by a mitotically activated protein in Xenopus egg extracts. Cell 64, 827-839.
55. Vallee, R. B. and Bloom, G. S. (1983). Isolation of sea urchin egg microtubules with taxol and identification of mitotic spindle microtubule-associated proteins with monoclonal antibodies. Proc. Nat. Acad. Sci. USA 80, 6259-6263.
56. van der Geer, P., Luo, K., Sefton, B. M. and Hunter, T. (1993) Phosphopeptide mapping and phosphoaminoacid analysis on cellulose thin-layer plates. In Protein Phosphorylation (ed. D. G. Hardie), pp. 31-59. IRL Press, Oxford, UK.
57. Vandre, D. D., Centonze, V. E., Peloquin, J., Tombes, R. M. and Borisy, G. G. (1991). Proteins of the mammalian mitotic spindle: phosphorylation/dephosphorylation of MAP-4 during mitosis. J. Cell Sci. 98, 577-588.
58. Verde, F., Labbe, J.-C., Doree, M. and Karsenti, E. (1990). Regulation of microtubule dynamics by cdc2 protein kinase in cell-free extracts of Xenopus eggs. Nature 343, 233-238.
59. Walczak, C. E., Mitchison, T. J. and Desai, A. (1996). XKCMI : a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell 84, 37-47.
60. Whitely, A. H. and Chambers, E. L. (1966). Phosphate transport in fertilized sea urchin eggs. J. Cell. Physiol. 68, 309-314.
61. 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.