Interdependency of Fission Yeast Alp14/TOG and Coiled Coil Protein Alp7 in Microtubule Localization and Bipolar Spindle Formation

Molecular Biology of the Cell

Volumn 15, Issue 4, 2004, Pages 1609-1622

  Sato, Masamitsu ^a   Vardy, Leah ^a,b   Garcia, Miguel Angel ^a,c   Koonrugsa, Nirada ^a   Toda, Takashi ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN ALP14; PROTEIN ALP7; PROTEIN TOG; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; INTERPHASE; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SPINDLE CELL; SPINDLE POLE BODY; YEAST;

BINDING SITES; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENOTYPE; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; KINETOCHORES; LUMINESCENT PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; PLASMIDS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TEMPERATURE; TIME FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

ANIMALIA; SCHIZOSACCHAROMYCES POMBE;

EID: 1642464705     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-11-0837     Document Type: Article

References (51)

1. Bähler, J., Wu, J., Longtine, M.S., Shah, N.G., McKenzie III, A., Steever, A.B., Wach, A., Philippsen, P., and Pringle, J.R. (1998). Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951.
2. Bellanger, J.-M., and Gönczy, P. (2003). TAC-1 and ZYG-9 form a complex that promotes microtubule assembly in C. elegans embryos. Curr. Biol. 13, 1488-1498.
3. Bridge, A.J., Morphew, M., Bartlett, R., and Hagan, I.M. (1998). The fission yeast SPB component Cut12 links bipolar spindle formation to mitotic control. Genes Dev. 12, 927-942.
4. Chen, X.P., Yin, H., and Huffaker, T.C. (1998). The yeast spindle pole body component Spc72p interacts with Stu2p and is required for proper microtubule assembly. J. Cell Biol. 141, 1169-1179.
5. Cullen, C.F., and Ohkura, H. (2001). Msps protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nat. Cell Biol. 3, 637-642.
6. Desai, A., Verma, S., Mitchison, T.J., and Walczak, C.E. (1999). Kin I kinesins are microtubule-destabilizing enzymes. Cell 96, 69-78.
7. Ding, D.-Q., Chikashige, Y., Haraguchi, T., and Hiraoka, Y. (1998). Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells. J. Cell Sci. 111, 701-712.
8. Garcia, M.A., Koonrugsa, N., and Toda, T. (2002a). Spindle-kinetochore attachment requires the combined action of Kin I-like Klp5/6 and Alp14/ Dis1-MAPs in fission yeast. EMBO J. 21, 6015-6024.
9. Garcia, M.A., Koonrugsa, N., and Toda, T. (2002b). Two kinesin-like Kin I family proteins in fission yeast regulate the establishment of metaphase and the onset of anaphase A. Curr. Biol. 12, 610-621.
10. Garcia, M.A., Vardy, L., Koonrugsa, N., and Toda, T. (2001). Fission yeast ch-TOG/XMAP215 homologue Alp14 connects mitotic spindles with the kinetochore and is a component of the Mad2-dependent spindle checkpoint. EMBO J. 20, 3389-3401.
11. 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.
12. Gergely, F., Draviam, V.M., and Raff, J.W. (2003). The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev. 17, 336-341.
13. Gergely, F., Kidd, D., Jeffers, K., Wakefield, J.G., and Raff, J.W. (2000). DTACC: a novel centrosomal protein required for normal spindle function in the early Drosophila embryo. EMBO J. 19, 241-252.
14. Groves, M.R., Hanlon, N., Turowski, P., Hemmings, B.A., and Barford, D. (1999). The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of Its 15 tandemly repeated HEAT motifs. Cell 96, 99-110.
15. + gene. Nature 347, 563-566.
16. Hagan, I., and Yanagida, M. (1992). Kinesin-related cut7 protein associates with mitotic and meiotic spindles in fission yeast. Nature 356, 74-76.
17. + associates with the fission yeast spindle pole body and is essential for viability. J. Cell Biol. 129, 1033-1047.
18. Hagan, I.M. (1998). The fission yeast microtubule cytoskeleton. J. Cell Sci. 111, 1603-1612.
19. Hiraoka, Y., Toda, T., and Yanagida, M. (1984). The NDA3 gene of fission yeast encodes β-tubulin: a cold-sensitive nda3 mutation reversibly blocks spindle formation and chromosome movement in mitosis. Cell 39, 349-358.
20. Kinoshita, K., Amal, I., Desai, A., Drechsel, D.N., and Hyman, A.A. (2001). Reconstitution of physiological microtubule dynamics using purified components. Science 294, 1340-1343.
21. Kinoshita, K., Habermann, B., and Hyman, A.A. (2002). XMAP 215, a key component of the dynamic microtubule cytoskeleton. Trends Cell Biol. 6, 267-273.
22. Kosco, K.A., Pearson, C.G., Maddox, P.S., Wang, P.J., Adams, I.R., Salmon, E.D., Bloom, K., and Huffaker, T.C. (2001). Control of microtubule dynamics by stu2p is essential for spindle orientation and metaphase chromosome alignment in yeast. Mol. Biol. Cell 12, 2870-2880.
23. Le Bot, N., Tsai, M.-C., Andrews, R.K., and Ahringer, J. (2003). TAC-1, a regulator of microtubule length in the C. elegans embryo. Curr. Biol. 13, 1499-1505.
24. Lee, M.J., Gergely, F., Jeffers, K., Peak-Chew, S.Y. and Raff, J.W. (2001). Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour. Nat. Cell Biol. 3, 643-649.
25. Matthews, L.R., Carter, P., Thierry-Mieg, D., and Kemphues, K. (1998). ZYG-9, a Caenorhabditis elegans protein required for microtubule organization and function, is a component of meiotic and mitotic spindle poles. J. Cell Biol. 141, 1159-1168.
26. Moreno, S., Klar, A., and Nurse, P. (1991). Molecular genetic analyses of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 773-782.
27. dis1, which is required for sister chromatid separation, is a novel microtubule and spindle pole body-associating protein phosphorylated at the Cdc2 target sites. Genes Dev. 9, 1572-1585.
28. Nabeshima, K., Nakagawa, T., Straight, A.F., Murray, A., Chikashige, Y., Yamashita, Y.M., Hiraoka, Y., and Yanagida, M. (1998). Dynamics of centromeres during metaphase-anaphase transition in fission yeast: Dis1 is implicated in force balance in metaphase bipolar spindle. Mol. Biol. Cell 9, 3211-3225.
29. Nabetani, A., Koujin, T., Tsutsumi, C., Haraguchi, T., and Hiraoka, Y. (2001). A conserved protein, Nuf2, is implicated in connecting the centromere to the spindle during chromosome segregation: a link between the kinetochore function and the spindle checkpoint. Chromosoma 110, 322-334.
30. Nakaseko, Y., Goshima, G., Morishita, J., and Yanagida, M. (2001). M phase-specific kinetochore proteins in fission yeast microtubule-associating Dis1 and Mtc1 display rapid separation and segregation during anaphase. Curr. Biol. 11, 537-549.
31. dis1: regions implicated in regulated localization and microtubule interaction. Genes Cells 1, 633-644.
32. Neuwald, A.F., and Hirano, T. (2000). HEAT repeats associated with condensins, cohesins, and other complexes Involved in chromosome-related functions. Genome Res. 10, 1445-1452.
33. Ohkura, H., Garcia, M.A., and Toda, T. (2001). Dis1/TOG universal microtubule adaptors-one MAP for all? J. Cell Sci. 114, 3805-3812.
34. Pearson, C.G., Maddox, P.S., Zarzar, T.R., Salmon, E.D., and Bloom, K. (2003). Yeast kinetochores do not stabilize Stu2p-dependent spindle microtubule dynamics. Mol. Biol. Cell 14, 4181-4195.
35. Pereira, G., Grueneberg, U., Knop, M., and Schiebel, E. (1999). Interaction of the yeast γ-tubulin complex-binding protein Spc72p with Kar1p is essential for microtubule function during karyogamy. EMBO J. 18, 4180-4195.
36. Radcliffe, P., Hirata, D., Childs, D., Vardy, L., and Toda, T. (1998). Identification of novel temperature-sensitive lethal alleles in essential β-tubulin and nonessential a2-tubulin genes as fission yeast polarity mutants. Mol. Biol. Cell 9, 1757-1771.
37. Raff, J.W. (2002). Centrosomes and cancer: lessons from a TACC. Trends Cell Biol. 12, 222-225.
38. Sato, M., Vardy, L., Koonrugsa, N., Tournier, S., Millar, J.B.A., and Toda, T. (2003). Deletion of Mia1/Alp7 activates Mad2-dependent spindle assembly checkpoint in fission yeast. Nat. Cell Biol. 5, 764-766.
39. Sato, M., Watanabe, Y., Akiyoshi, Y., and Yamamoto, M. (2002). 14-3-3 protein interferes with the binding of RNA to the phosphorylated form of fission yeast meiotic regulator Mei2p. Curr. Biol. 12, 141-145.
40. Severin, F., Habermann, B., Huffaker, T., and Hyman, T. (2001). Stu2 promotes mitotic spindle elongation in anaphase. J. Cell Biol. 153, 435-442.
41. Shirasu-Hiza, M., Coughlin, P., and Mitchison, T. (2003). Identification of XMAP215 as a microtubule-destabilizing factor in Xenopus egg extract by biochemical purification. J. Cell Biol. 161, 349-358.
42. Souès, S., and Adams, I.R. (1998). SPC 72, a spindle pole component required for spindle orientation in the yeast Saccharomyces cerevisiae. J. Cell Sci. 111, 2809-2818.
43. Srayko, M., Quintin, S., Schwager, A., and Hyman, A.A. (2003). Caenorhabditis elegans TAC-1 and ZYG-9 form a complex that is essential for long astral and spindle microtubules. Curr. Biol. 13, 1506-1511.
44. 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.
45. Usui, T., Maekawa, H., Pereira, G., and Schiebel, E. (2003). The XMAP215 homologue Stu2 at yeast spindle pole bodies regulates microtubule dynamics and anchorage. EMBO J. 22, 4779-4793.
46. van Breugel, M., Drechsel, D., and Hyman, A. (2003). Stu2p, the budding yeast member of the conserved Dis1/XMAP215 family of microtubule-proteins is a plus end-binding microtubule destabilizer. J. Cell Biol. 161, 359-369.
47. Vardy, L., and Toda, T. (2000). The fission yeast γ-tubulin complex is required in G1 phase and is a component of the spindle-assembly checkpoint. EMBO J. 19, 6098-6111.
48. Walczak, C.E., Gan, E.C., Desai, A., Mitchison, T.J., and Kline-Smith, S.L. (2002). The microtubule-destabilizing kinesin XKCM1 is required for chromosome positioning during spindle assembly. Curr. Biol. 12, 1885-1889.
49. Wang, P.J., and Huffaker, T.C. (1997). Stu2p: a microtubule-binding protein that is essential component of the yeast spindle pole body. J. Cell Biol. 139, 1271-1280.
50. +: a gene required for cell cycle-dependent spindle pole body anchoring in the nuclear envelope and bipolar spindle formation in Schizosaccharomyces pombe. Mol. Biol. Cell 9, 2839-2855.
51. Zeng, X., Kahana, J.A., Silver, P.A., Morphew, M.K., McIntosh, J.R., Fitch, I.T., Carbon, J., and Saunders, W.S. (1999). Slk19p is a centromere protein that functions to stabilize mitotic spindles. J. Cell Biol. 146, 415-426.