Reconstitution of dynamic microtubules with drosophila XMAP215, EB1, and sentin

Journal of Cell Biology

Volumn 199, Issue 5, 2012, Pages 849-862

  Li, Wenjing ^a,b   Moriwaki, Takashi ^a   Tani, Tomomi ^b   Watanabe, Takashi ^a   Kaibuchi, Kozo ^a   Goshima, Gohta ^a,b  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EB1 PROTEIN; MICROTUBULE PROTEIN; SENTIN; UNCLASSIFIED DRUG; XMAP215 PROTEIN;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; GROWTH ACCELERATION; INTERPHASE; MICROTUBULE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SPINDLE CELL;

ANIMALS; CELLS, CULTURED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; SPODOPTERA;

DROSOPHILA MELANOGASTER;

EID: 84872002781     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201206101     Document Type: Article

References (39)

1. Akhmanova, A., and M.O. Steinmetz. 2008. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9:309-322. http://dx.doi.org/10.1038/nrm2369
2. Bettencourt-Dias, M., and G. Goshima. 2009. RNAi in Drosophila S2 cells as a tool for studying cell cycle progression. Methods Mol. Biol. 545:39-62. http://dx.doi.org/10.1007/978-1-60327-993-2_3
3. Bieling, P., L. Laan, H. Schek, E.L. Munteanu, L. Sandblad, M. Dogterom, D. Brunner, and T. Surrey. 2007. Reconstitution of a microtubule plusend tracking system in vitro. Nature. 450:1100-1105. http://dx.doi.org/10.1038/nature06386
4. Bieling, P., S. Kandels-Lewis, I.A. Telley, J. van Dijk, C. Janke, and T. Surrey. 2008. CLIP-170 tracks growing microtubule ends by dynamically recognizing composite EB1/tubulin-binding sites. J. Cell Biol. 183:1223-1233. http://dx.doi.org/10.1083/jcb.200809190
5. Bieling, P., I.A. Telley, C. Hentrich, J. Piehler, and T. Surrey. 2010. Fluorescence microscopy assays on chemically functionalized surfaces for quantitative imaging of microtubule, motor, and +TIP dynamics. Methods Cell Biol. 95:555-580. http://dx.doi.org/10.1016/S0091-679X(10)95028-0
6. Brittle, A.L., and H. Ohkura. 2005. Mini spindles, the XMAP215 homologue, suppresses pausing of interphase microtubules in Drosophila. EMBO J. 24:1387-1396. http://dx.doi.org/10.1038/sj.emboj.7600629
7. Brouhard, G.J., J.H. Stear, T.L. Noetzel, J. Al-Bassam, K. Kinoshita, S.C. Harrison, J. Howard, and A.A. Hyman. 2008. XMAP215 is a processive microtubule polymerase. Cell. 132:79-88. http://dx.doi.org/10.1016/j.cell.2007.11.043
8. Desai, A., and T.J. Mitchison. 1997. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13:83-117. http://dx.doi.org/10.1146/annurev.cellbio.13.1.83
9. Dixit, R., B. Barnett, J.E. Lazarus, M. Tokito, Y.E. Goldman, and E.L. Holzbaur. 2009. Microtubule plus-end tracking by CLIP-170 requires EB1. Proc. Natl. Acad. Sci. USA. 106:492-497. http://dx.doi.org/10.1073/pnas.0807614106
10. Gardner, M.K., M. Zanic, C. Gell, V. Bormuth, and J. Howard. 2011. Depolymerizing kinesins Kip3 and MCAK shape cellular microtubule architecture by differential control of catastrophe. Cell. 147:1092-1103. http://dx.doi.org/10.1016/j.cell.2011.10.037
11. Gell, C., V. Bormuth, G.J. Brouhard, D.N. Cohen, S. Diez, C.T. Friel, J. Helenius, B. Nitzsche, H. Petzold, J. Ribbe, et al. 2010. Microtubule dynamics reconstituted in vitro and imaged by single-molecule fluorescence microscopy. Methods Cell Biol. 95:221-245. http://dx.doi.org/10.1016/S0091-679X(10)95013-9
12. Goshima, G. 2010. Assessment of mitotic spindle phenotypes in Drosophila S2 cells. Methods Cell Biol. 97:259-275. http://dx.doi.org/10.1016/S0091-679X(10)97015-5
13. Goshima, G., and R.D. Vale. 2003. The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line.
14. J. Cell Biol. 162:1003-1016. http://dx.doi.org/10.1083/jcb.200303022
15. Goshima, G., and R.D. Vale. 2005. Cell cycle-dependent dynamics and regulation of mitotic kinesins in Drosophila S2 cells. Mol. Biol. Cell. 16:3896-3907. http://dx.doi.org/10.1091/mbc.E05-02-0118
16. Goshima, G., R. Wollman, N. Stuurman, J.M. Scholey, and R.D. Vale. 2005. Length control of the metaphase spindle. Curr. Biol. 15:1979-1988. http://dx.doi.org/10.1016/j.cub.2005.09.054
17. Goshima, G., R. Wollman, S.S. Goodwin, N. Zhang, J.M. Scholey, R.D. Vale, and N. Stuurman. 2007. Genes required for mitotic spindle assembly in Drosophila S2 cells. Science. 316:417-421. http://dx.doi.org/10.1126/science.1141314
18. Howard, J., and A.A. Hyman. 2007. Microtubule polymerases and depolymerases. Curr. Opin. Cell Biol. 19:31-35. http://dx.doi.org/10.1016/j.ceb.2006.12.009
19. Kerssemakers, J.W., E.L. Munteanu, L. Laan, T.L. Noetzel, M.E. Janson, and M. Dogterom. 2006. Assembly dynamics of microtubules at molecular resolution. Nature. 442:709-712. http://dx.doi.org/10.1038/nature04928
20. 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. http://dx.doi.org/10.1126/science.1064629
21. Komarova, Y., C.O. De Groot, I. Grigoriev, S.M. Gouveia, E.L. Munteanu, J.M. Schober, S. Honnappa, R.M. Buey, C.C. Hoogenraad, M. Dogterom, et al. 2009. Mammalian end binding proteins control persistent microtubule growth. J. Cell Biol. 184:691-706. http://dx.doi.org/10.1083/jcb.200807179
22. Lemos, C.L., P. Sampaio, H. Maiato, M. Costa, L.V. Omel'yanchuk, V. Liberal, and C.E. Sunkel. 2000. Mast, a conserved microtubule-associated protein required for bipolar mitotic spindle organization. EMBO J. 19:3668-3682. http://dx.doi.org/10.1093/emboj/19.14.3668
23. Li, W., T. Miki, T. Watanabe, M. Kakeno, I. Sugiyama, K. Kaibuchi, and G. Goshima. 2011. EB1 promotes microtubule dynamics by recruiting Sentin in Drosophila cells. J. Cell Biol. 193:973-983. http://dx.doi.org/10.1083/jcb.201101108
24. Manna, T., S. Honnappa, M.O. Steinmetz, and L. Wilson. 2008. Suppression of microtubule dynamic instability by the +TIP protein EB1 and its modulation by the CAP-Gly domain of p150glued. Biochemistry. 47:779-786. http://dx.doi.org/10.1021/bi701912g
25. Maurer, S.P., P. Bieling, J. Cope, A. Hoenger, and T. Surrey. 2011. GTPgammaS microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs). Proc. Natl. Acad. Sci. USA. 108:3988-3993. http://dx.doi.org/10.1073/pnas.1014758108
26. Maurer, S.P., F.J. Fourniol, G. Bohner, C.A. Moores, and T. Surrey. 2012. EBs recognize a nucleotide-dependent structural cap at growing microtubule ends. Cell. 149:371-382. http://dx.doi.org/10.1016/j.cell.2012.02.049
27. Mennella, V., G.C. Rogers, S.L. Rogers, D.W. Buster, R.D. Vale, and D.J. Sharp. 2005. Functionally distinct kinesin-13 family members cooperate to regulate microtubule dynamics during interphase. Nat. Cell Biol. 7:235-245. http://dx.doi.org/10.1038/ncb1222
28. Montenegro Gouveia, S., K. Leslie, L.C. Kapitein, R.M. Buey, I. Grigoriev, M. Wagenbach, I. Smal, E. Meijering, C.C. Hoogenraad, L. Wordeman, et al. 2010. In vitro reconstitution of the functional interplay between MCAK and EB3 at microtubule plus ends. Curr. Biol. 20:1717-1722. http://dx.doi.org/10.1016/j.cub.2010.08.020
29. Niethammer, P., I. Kronja, S. Kandels-Lewis, S. Rybina, P. Bastiaens, and E. Karsenti. 2007. Discrete states of a protein interaction network govern interphase and mitotic microtubule dynamics. PLoS Biol. 5:e29. http://dx.doi.org/10.1371/journal.pbio.0050029
30. Rogers, S.L., G.C. Rogers, D.J. Sharp, and R.D. Vale. 2002. Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J. Cell Biol. 158:873-884. http://dx.doi.org/10.1083/jcb.200202032
31. Short, B. 2011. New TIPs for successfully growing microtubules. J. Cell Biol. 193:955. http://dx.doi.org/10.1083/jcb.1936if
32. Slep, K.C. 2010. Structural and mechanistic insights into microtubule endbinding proteins. Curr. Opin. Cell Biol. 22:88-95. http://dx.doi.org/10.1016/j.ceb.2009.10.009
33. Sousa, A., R. Reis, P. Sampaio, and C.E. Sunkel. 2007. The Drosophila CLASP homologue, Mast/Orbit regulates the dynamic behaviour of interphase microtubules by promoting the pause state. Cell Motil. Cytoskeleton. 64:605-620. http://dx.doi.org/10.1002/cm.20208
34. 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. http://dx.doi.org/10.1091/mbc.02-04-0210
35. van der Vaart, B., C. Manatschal, I. Grigoriev, V. Olieric, S.M. Gouveia, S. Bjelic, J. Demmers, I. Vorobjev, C.C. Hoogenraad, M.O. Steinmetz, and A. Akhmanova. 2011. SLAIN2 links microtubule plus end-tracking proteins and controls microtubule growth in interphase. J. Cell Biol. 193:1083-1099. http://dx.doi.org/10.1083/jcb.201012179
36. Vitre, B., F.M. Coquelle, C. Heichette, C. Garnier, D. Chrétien, and I. Arnal. 2008. EB1 regulates microtubule dynamics and tubulin sheet closure in vitro. Nat. Cell Biol. 10:415-421. http://dx.doi.org/10.1038/ncb1703
37. 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. http://dx.doi.org/10.1083/jcb.107.4.1437
38. Zanic, M., J.H. Stear, A.A. Hyman, and J. Howard. 2009. EB1 recognizes the nucleotide state of tubulin in the microtubule lattice. PLoS ONE. 4:e7585. http://dx.doi.org/10.1371/journal.pone.0007585
39. Zhu, Z.C., K.K. Gupta, A.R. Slabbekoorn, B.A. Paulson, E.S. Folker, and H.V. Goodson. 2009. Interactions between EB1 and microtubules: dramatic effect of affinity tags and evidence for cooperative behavior. J. Biol. Chem. 284:32651-32661. http://dx.doi.org/10.1074/jbc.M109.013466