Protein phosphatase 4 is an essential enzyme required for organisation of microtubules at centrosomes in Drosophila embryos

Journal of Cell Science

Volumn 111, Issue 10, 1998, Pages 1331-1340

  Helps, Nicholas R ^a   Brewis, Neil D ^a,c   Lineruth, Katrin ^b   Davis, Terence ^b,d   Kaiser, Kim ^b   Cohen, Patricia T W ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c MARIE CURIE RESEARCH INSTITUTE   (United Kingdom)

^d UNIVERSITY OF HAWAII   (United States)

Author keywords

Centrosome; Drosophila; Microtubule; P element; Phosphorylation; Protein phosphatase

Indexed keywords

MESSENGER RNA; PHOSPHOPROTEIN PHOSPHATASE; TUBULIN;

AMINO ACID SEQUENCE; ARTICLE; CELL DIVISION; CENTROSOME; CONFORMATIONAL TRANSITION; DROSOPHILA MELANOGASTER; EMBRYO; MICROTUBULE; MITOSIS SPINDLE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CENTROSOME; CONSERVED SEQUENCE; DNA, COMPLEMENTARY; DROSOPHILA; FLUORESCENT ANTIBODY TECHNIQUE; GENES, INSECT; HOMOZYGOTE; MAMMALS; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PHENOTYPE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID;

DROSOPHILA MELANOGASTER; HEXAPODA; INVERTEBRATA; MELANOGASTER;

EID: 0031799965     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Alexandre, H., van Cauwenberge, A., Tsukitani, Y. and Mulnard, J. (1991). Pleiotropic effect of okadaic acid on maturing mouse oocytes. Development 112, 971-980.
2. Andersen, S. S., Buendia, B., Dominguez, J. E., Sawyer, A. and Karsenti, E. (1994). Effect on microtubule dynamics of XMAP230, a microtubule-associated protein present in Xenopus laevis eggs and dividing cells. J. Cell Biol. 127, 1289-1299.
3. Armstrong, C. G., Mann, D. J., Berndt, N. and Cohen, P. T. W. (1995). Drosophila PPY. a male specific protein serine/threonine phosphatase localised in somatic cells of the testis. J. Cell Sci. 108, 3367-3375.
4. Arndt, K. T., Styles, C. A. and Fink, G. R. (1989). A suppressor of HlS4 transcription defect encodes a protein with homology to the catalytic subunit of protein phosphatases. Cell 56, 527-537.
5. cdc2 is located in both nucleus and cytoplasm: part is centrosomally associated at G2/M and enters vesicles at anaphase. EMBO J. 8, 3985-3995.
6. Barton, G. J., Cohen, P. T. W. and Barford, D. (1994). Conservation analysis and structure prediction of the protein serine/threonine phosphatases: sequence similarity with diadenosine tetraphosphatase from E. coli suggests homology to the protein phosphatases. Eur. J. Biochem. 220, 225-237.
7. Belmont, L., Hymann, A. A., Sawin, K. D. and Mitchison, T. (1990). Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell 62, 579-589.
8. 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.
9. Black, S., Andrews, P. D., Sneddon, A. A. and Stark, M. J. R. (1995). A regulated MET3-GLC7 gene fusion provides evidence of a mitotic role for Saccharomyces cerevisiae protein phosphatase 1. Yeast 11, 747-759.
10. Brewis, N. D. and Cohen, P. T. W. (1992). Protein phosphatase X has been highly conserved during mammalian evolution. Biochim. Biophys. Acta 1171, 231-233.
11. Brewis, N. D., Street, A. J., Prescott, A. R. and Cohen, P. T. W. (1993). PPX, a novel protein serine/threonine phosphatase localized to centrosomes. EMBO J. 12, 987-996.
12. 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.
13. Centonze, V. E. and Borisy, G. G. (1990). Nucleation of microtubules from mitotic centrosomes is modulated by a phosphorylated epitope. J. Cell Sci. 95, 405-411.
14. Cohen, P. T. W. (1997). Novel protein serine/threonine phosphatases variety is the spice of life. Trends Biochem. Sci. 22, 245-251.
15. Debec, A., Kalpin, R. F., Saily, D. R., McCallum, P. D., Rothwell, W. F. and Sullivan, W. (1996). Live analysis of free centrosomes in normal and aphidicolin-treated Drosophila embryos. J. Cell Biol. 134, 103-115.
16. Dombrádi, V., Mann, D. J., Saunders, R. D. C. and Cohen, P. T. W. (1993). Cloning of the fourth functional gene for protein phosphatase 1 in Drosophila melanogaster from its chromosomal localisation. Eur. J. Biochem. 212, 177-183.
17. Félix, M.-A., Antony, C., Wright, M. and Maro, B. (1994). Centrosome assembly in vitro: role of γ-tubulin recruitment in Xenopus sperm aster formation. J. Cell Biol. 124, 19-31.
18. Fuller, S. D., Kenny, J. M. and Karsenti, E. (1992). Centrosomes. Curr. Opin. Struct. Biol. 2, 264-274.
19. Heald, R., Tournebize, R., Blank, T., Sandaltzopoulos, R., Becker, P., Hyman, A. and Karsenti, E. (1996). Self-organisation of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382, 420-425.
20. Heald, R., Townebize, R., Habermann, A., Karsenti, E. and Hyman, A. (1997). Spindle assembly in Xenopus egg extracts: respective roles of centrosomes and microtubule self-organization. J. Cell Biol. 138, 615-628.
21. Horio, T., Uzawa, S., Jung, M. K., Oakley, B. R., Tanaka, K. and Yanagida, M. (1991). The fission yeast γ-tubulin is essential for mitosis and is localized at the microtubule organising centres. J. Cell Sci. 99, 693-700.
22. Joshi, H. C., Palacios, M. J., McNamara, L. and Cleveland, D. W. (1992). γ-Tubulin is a centrosomal protein required for cell cycle-dependent microtubule nucleation. Nature 356, 80-83.
23. Kaiser, K. and Goodwin, S. F. (1990). 'Site-selected' transposon mutagenesis of Drosophila. Proc. Nat. Acad. Sci. USA 87, 1686-1690.
24. Kalnins, V. I. (1992). The Centrosome. Academic Press, San Diego.
25. Keeling, P. J. and Logsdon, J. M. (1996). Highly divergent Caenorhabditis and Saccharomyces tubulins evolved recently from genes encoding γ-tubulin. Trends Cell Biol. 6, 375.
26. Kellogg, D. R., Mitchison, T. J. and Alberts, B. M. (1988). Behaviour of microtubules and actin filaments in living Drosophila embryos. Development 103, 675-686.
27. Kellogg, D. R., Moritz, M. and Alberts, B. M. (1994). The centrosome and cellular organisation. Annu. Rev. Biochem. 63, 639-674.
28. Kellogg, D. R., Oegema, K., Raff, J., Schneider, K. and Alberts, B. M. (1995). CP60: a microtubule-associated protein that is localised to the centrosome in a cell cycle-specific manner. Mol. Biol. Cell 6, 1673-1684.
29. Kidd, D. and Raff, J. W. (1997). LK6, a short lived protein kinase in Drosophila that can associate with microtubules and centrosomes. J. Cell Sci. 110, 209-219.
30. Lindsley, D. L. and Zimm, G. G. (1992). The Genome of Drosophila melanogaster. Academic Press, San Diego.
31. Matsukage, A., Hirose, F., Hayashi, Y., Hamada, K. and Yamaguchi, M. (1995). The DRE sequence TATCGATA, a putative promoter-activating element for Drosophila melanogaster cell-proliferation-related genes. Gene 166, 233-236.
32. Moritz, M., Braunfeld, M. B., Fung, J. C., Sedat, J. W., Alberts, B. and Agard, D. A. (1995a). Three-dimensional structural characterization of centrosomes from early Drosophila embryos. J. Cell Biol. 130, 1149-1159.
33. Moritz, M., Braunfeld, M. B., Sedat, J. W., Alberts, B. M. and Agard, D. A. (1995b). Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature 378, 638-640.
34. O'Hare, K. and Rubin, G. M. (1983). Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell 34, 25-35.
35. Oakley, B. R., Oakley, C. E., Yoon, Y. and Yung, M. K. (1990). γ-Tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell 61, 1289-1301.
36. cdc2 kinase to microtubules and is a pontential regulator of M-phase microtubule dynamics. J. Cell Biol. 128, 849-862.
37. Orgad, S., Brewis, N. D., Alphey, L., Axton, J. M., Dudai, Y. and Cohen, P. T. W. (1990). The structure of protein phosphatase 2A is as highly conserved as that of protein phosphatase 1. FEBS Lett. 275, 44-48.
38. Pagano, M., Pepperkok, R., Verde, F., Ansorge, W. and Draetta, G. (1992). Cyclin A is required at two points in the human cell cycle. EMBO J. 346, 760-763.
39. Picard, A., Capony, J. P., Brautigan, D. L. and Dorée, M. (1989). Involvement of protein phosphatases 1 and 2A in the control of M phase-promoting factor activity in starfish. J. Cell Biol. 109, 3347-3354.
40. Rime, H. and Ozon, R. (1990). Protein phosphatases are involved in the in vivo activation of histone H1 kinase in mouse oocytcs. Dev. Biol. 141, 115-122.
41. Ronne, H., Carlberg, M., Hu, G.-Z. and Nehlin, J. O. (1991). Protein phosphatase 2A in Saccharomyces cerevisiae: effects on cell growth and bud morphogenesis. Mol. Cell. Biol. 11, 4876-4884.
42. Shiina, N., Moriguchi, 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.
43. Snaith, H. A., Armstrong, C. A., Guo, Y., Kaiser, K. and Cohen, P. T. W. (1996). Deficiency of protein phosphatase 2A uncouples the nuclear and centrosome cycles and prevents attachment of microtubules to the kinetchore in Drosophila embryos. J. Cell Sci. 109, 3001-3012.
44. Stearns, T. and Kirschner, M. (1994). In vitro reconstitution of centrosome assembly and function: the role of γ-tubulin. Cell 76, 623-637.
45. Sunkel, C. E., Gomes, R., Sampaio, P., Perdigão, J. and González, C. (1995). γ-Tubulin is required for the structure and function of the microtubule organising centre in Drosophila neuroblasts. EMBO J. 14, 28-36.
46. Tournebize, R., Andersen, S. S. L., Verde, F., Dorée, M., Karsenti, E. and Hyman, A. A. (1997). Distinct roles of PP1 and PP2A-like phosphatases in control of microtubule dynamics during mitosis. EMBO J. 16, 5537-5549.
47. Vandré, 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.
48. Verde, F., Labbé, J. C., Dorée, M. and Karsenti, E. (1990). Regulation of microtubule dynamics by cdc2 protein kinase in cell-free extracts of Xenopus eggs. Nature 343, 233-238.
49. Whitfield, W. G., Chaplin, M. A., Oegema, K., Parry, H. and Glover, D. M. (1995). The 190 kDa centrosome-associated protein of Drosophila melanogaster contains four zinc finger motifs and binds to specific sites on polytene chromosomes. J. Cell Sci. 108, 3377-3387.
50. Zheng, Y., Wong, M. L., Alberts, B. and Mitchison, T. (1995). Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature 378, 578-583.