Identification of XMAP215 as a microtubule-destabilizing factor in Xenopus egg extract by biochemical purification

Journal of Cell Biology

Volumn 161, Issue 2, 2003, Pages 349-358

  Shirasu Hiza, Mimi ^a,b   Coughlin, Peg ^b   Mitchison, Tim ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Depolymerization; GMPCPP; Microtubule dynamics; Microtubule associated protein; XMAP215

Indexed keywords

GUANOSINE TRIPHOSPHATE DERIVATIVE; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN XMAP215; UNCLASSIFIED DRUG;

ARTICLE; CELL STRUCTURE; DEPOLYMERIZATION; FRACTIONATION; MICROTUBULE; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN POLYMERIZATION; PROTEIN PURIFICATION; XENOPUS;

ANIMALS; BIOLOGICAL ASSAY; CELL EXTRACTS; FEMALE; GUANOSINE TRIPHOSPHATE; MICROTUBULE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MODELS, BIOLOGICAL; OOCYTES; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 0038408571     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200211095     Document Type: Article

References (40)

1. Belmont, L.D., and T.J. Mitchison. 1996. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell. 84:623-631.
2. Belmont, L.D., A.A. Hyman, K.E. Sawin, and T.J. Mitchison. 1990. Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell. 62:579-589.
3. Caplow, M., and J. Shanks. 1996. Evidence that a single monolayer tubulin-GTP cap is both necessary and sufficient to stabilize microtubules. Mol. Biol. Cell. 7:663-675.
4. Caplow, M., R.L. Ruhlen, and J. Shanks. 1994. The free energy for hydrolysis of a microtubule- bound nucleotide triphosphate is near zero: all of the free energy for hydrolysis is stored in the microtubule lattice. J. Cell Biol. 127:779-788.
5. Cassimeris, L., D. Gard, P.T. Tran, and H.P. Erickson. 2001. XMAP215 is a long thin molecule that does not increase microtubule stiffness. J. Cell Sci. 114: 3025-3033.
6. Chretien, D., S.D. Fuller, and E. Karsenti. 1995. Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates. J. Cell Biol. 129:1311-1328.
7. Desai, A., A. Murray, T.J. Mitchison, and C.E. Walczak. 1999a. The use of Xenopus egg extracts to study mitotic spindle assembly and function in vitro. Methods Cell Biol. 61:385-412.
8. Desai, A., S. Verma, T.J. Mitchison, and C.E. Walczak. 1999b. Kin I kinesins are microtubule-destabilizing enzymes. Cell. 96:69-78.
9. Drechsel, D.N., and M.W. Kirschner. 1994. The minimum GTP cap required to stabilize microtubules. Curr. Biol. 4:1053-1061.
10. Garcia, M.A., L. Vardy, N. Koonrugsa, and T. Toda. 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. Garcia, M.A., N. Koonrugsa, and T. Toda. 2002. 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.
12. Gard, D.L., and M.W. Kirschner. 1987. A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus end. J. Cell Biol. 105:2203-2215.
13. Gergely, F., V.M. Draviam, and J.W. Raff. 2003. The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev. 17:336-341.
14. Gliksman, N.R., S.F. Parsons, and E.D. Salmon. 1992. Okadaic acid induces interphase to mitotic-like microtubule dynamic instability by inactivating rescue. J. Cell Biol. 119:1271-1276.
15. Holy, T.E., and S. Leibler. 1994. Dynamic instability of microtubules as an efficient way to search in space. Proc. Natl. Acad. Sci. USA. 91:5682-5685.
16. Hyman, A.A. 1991. Preparation of marked microtubules for the assay of the polarity of microtubule-based motors by fluorescence. J. Cell Sci. Suppl. 14:125-127.
17. Hyman, A.A., S. Salser, D.N. Drechsel, N. Unwin, and T.J. Mitchison. 1992. Role of GTP hydrolysis in microtubule dynamics: information from a slowly hydrolyzable analogue, GMPCPP. Mol. Biol. Cell. 3:1155-1167.
18. Kinoshita, K., I. Arnal, A. Desai, D.N. Drechsel, and A.A. Hyman. 2001. Reconstitution of physiological microtubule dynamics using purified components. Science. 294:1340-1343.
19. Kline-Smith, S.L., and C.E. Walczak. 2002. The microtubule-destabilizing kinesin XKCM1 regulates microtubule dynamic instability in Cells. Mol. Biol. Cell. 13:2718-2731.
20. Mandelkow, E.M., E. Mandelkow, and R.A. Milligan. 1991. Microtubule dynamics and microtubule caps: a time-resolved cryo-electron microscopy study. J. Cell Biol. 114:977-991.
21. Maney, T., M. Wagenbach, and L. Wordeman. 2001. Molecular dissection of the microtubule depolymerizing activity of mitotic centromere-associated kinesin. J. Biol. Chem. 276:34753-34758.
22. McNally, F.J., and R.D. Vale. 1993. Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell. 75:419-429.
23. Mitchison, T.J. 1993. Localization of an exchangeable GTP binding site at the plus end of microtubules. Science. 261:1044-1047.
24. Miyamoto, D., Z. Perlman, T. Mitchison, and M. Shirasu-Hiza. 2002. Dynamics of the mitotic spindle - potential therapeutic targets. In Progress in Cell Cycle Research. Vol. 5. L. Meijer, A. Jezequel, and M. Roberge, editors. Plenum Press, New York. 349-360.
25. Nakaseko, Y., G. Goshima, J. Morishita, and M. Yanagida. 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.
26. Ohkura, H., M.A. Garcia, and T. Toda. 2001. Dis1/TOG universal microtubule adaptors - one MAP for all? J. Cell Sci. 114:3805-3812.
27. Popov, A.V., A. Pozniakovsky, I. Arnal, C. Antony, A.J. Ashford, K. Kinoshita, R. Tournebize, A.A. Hyman, and E. Karsenti. 2001. XMAP215 regulates microtubule dynamics through two distinct domains. EMBO J. 20:397-410.
28. Rusan, N.M., C.J. Fagerstrom, A.M. Yvon, and P. Wadsworth. 2001. Cell cycledependent changes in microtubule dynamics in living cells expressing green fluorescent protein-α tubulin. Mol. Biol. Cell. 12:971-980.
29. Shelden, E., and P. Wadsworth. 1993. Observation and quantification of individual microtubule behavior in vivo: microtubule dynamics are cell type specific. J. Cell Biol. 120:935-945.
30. Simon, J.R., and E.D. Salmon. 1990. The structure of microtubule ends during the elongation and shortening phases of dynamic instability examined by negative-stain electron microscopy. J. Cell Sci. 96(Pt 4):571-582.
31. Spittle, C., S. Charrasse, C. Larroque, and L. Cassimeris. 2000. The interaction of TOGp with microtubules and tubulin. J. Biol. Chem. 275:20748-20753.
32. Takada, S., T. Shibata, Y. Hiraoka, and H. Masuda. 2000. Identification of ribonucleotide reductase protein R1 as an activator of microtubule nucleation in Xenopus egg mitoric extracts. Mol. Biol. Cell. 11:4173-4187.
33. Tirnauer, J.S., S. Grego, E.D. Salmon, and T.J. Mitchison. 2002. EB1-microtubule interactions in Xenopus egg extracts: role of EB1 in microtubule stabilization and mechanisms of targeting to microtubules. Mol. Biol. Cell. 13: 3614-3626.
34. Tirnauer, J.S., E. O'Toole, L. Berrueta, B.E. Bierer, and D. Pellman. 1999. Yeast Bim1p promores the G1-specific dynamics of microtubules. J. Cell Biol. 145:993-1007.
35. Tournebize, R., A. Popov, K. Kinoshita, A.J. Ashford, S. Rybina, A. Pozniakovsky, T.U. Mayer, C.E. Walczak, E. Karsenti, and A.A. Hyman. 2000. Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nat. Cell Biol. 2:13-19.
36. Tran, P.T., R.A. Walker, and E.D. Salmon. 1997. A metastable intermediate state of microtubule dynamic instability that differs significantly between plus and minus ends. J. Cell Biol. 138:105-117.
37. van Breugel, M., D. Drechsel, and A. Hyman. 2003. Stu2p, the budding yeast member of the conserved Dis1/XMAP215 family of microtubule-associated proteins is a plus end-binding microtubule destabilizer. J. Cell Biol. 161: 359-369.
38. Vasquez, R.J., D.L. Gard, and L. Cassimeris. 1994. XMAP from Xenopus eggs promotes rapid plus end assembly of microtubules and rapid microtubule polymer turnover. J. Cell Biol. 127:985-993.
39. Walczak, C.E., T.J. Mitchison, and A. Desai. 1996. XKCM1: a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell. 84:37-47.
40. Walker, R.A., E.T. O'Brien, N.K. Pryer, M.F. Soboeiro, W.A. Voter, H.P. Erickson, and E.D. Salmon. 1988. Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J. Cell Biol. 107:1437-1448.