The microtubule lattice and plus-end association of Drosophila Mini spindles is spatially regulated to fine-tune microtubule dynamics

Molecular Biology of the Cell

Volumn 22, Issue 22, 2011, Pages 4343-4361

  Currie, Joshua D ^a   Stewman, Shannon ^b   Schimizzi, Gregory ^a   Slep, Kevin C ^a   Ao, Ma ^b   Rogers, Stephen L ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN;

ARTICLE; CELL GROWTH; DROSOPHILA; IN VIVO STUDY; MICROTUBULE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA INTERFERENCE; SPINDLE CELL;

AMINO ACID MOTIFS; ANIMALS; CELL LINE; DROSOPHILA; DROSOPHILA PROTEINS; MICROFILAMENT PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE;

EID: 81755184372     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-06-0520     Document Type: Article

References (61)

1. Akhmanova A, Steinmetz M (2008). Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol.
2. Al-Bassam J, Larsen NA, Hyman AA, Harrison SC (2007). Crystal structure of a TOG domain: conserved features of XMAP215/Dis1-family TOG domains and implications for tubulin binding. Structure 15, 355-362. (Pubitemid 46366718)
3. Al-Bassam J, Kim H, Brouhard G, van Oijen A, Harrison SC, Chang F (2010). CLASP promotes microtubule rescue by recruiting tubulin dimers to the microtubule. Dev Cell 19, 245-258.
4. Bieling P, Kandels-Lewis S, Telley IA, van Dijk J, Janke C, Surrey T (2008). CLIP-170 tracks growing microtubule ends by dynamically recognizing composite EB1/tubulin-binding sites. J Cell Biol 183, 1223-1233.
5. Brittle AL, Ohkura H (2005). Mini spindles, the XMAP215 homologue, suppresses pausing of interphase microtubules in Drosophila. EMBO J 24, 1387-1396. (Pubitemid 40593059)
6. Brouhard GJ, Stear JH, Noetzel TL, Al-Bassam J, Kinoshita K, Harrison SC, Howard J, Hyman AA (2008). XMAP215 is a processive microtubule polymerase. Cell 132, 79-88.
7. Campbell JN, Slep KC (2011). αβ-Tubulin and microtubule-binding assays. Methods Mol Biol 777, 87-97.
8. Charrasse S, Mazel M, Taviaux S, Berta P, Chow T, Larroque C (1995). Characterization of the cDNA and pattern of expression of a new gene over-expressed in human hepatomas and colonic tumors. Eur J Biochem 234, 406-413.
9. Charrasse S, Schroeder M, Gauthier-Rouviere C, Ango F, Cassimeris L, Gard DL, Larroque C (1998). The TOGp protein is a new human microtubule-associated protein homologous to the Xenopus XMAP215. J Cell Sci 111 (Pt 10),1371-1383. (Pubitemid 28274389)
10. Cullen CF, Deák P, Glover DM, Ohkura H (1999). mini spindles: a gene encoding a conserved microtubule-associated protein required for the integrity of the mitotic spindle in Drosophila. J Cell Biol 146, 1005-1018. (Pubitemid 29430443)
11. Cullen CF, Ohkura H (2001). Msps protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nat Cell Biol 3, 637-642. (Pubitemid 32624419)
12. Dzhindzhev NS, Rogers SL, Vale RD, Ohkura H (2005). Distinct mechanisms govern the localisation of Drosophila CLIP-190 to unattached kinetochores and microtubule plus-ends. J Cell Sci 118, 3781-3790. (Pubitemid 41309424)
13. Enke C, Zekert N, Veith D, Schaaf C, Konzack S, Fischer R (2007). Aspergillus nidulans Dis1/XMAP215 protein AlpA localizes to spindle pole bodies and microtubule plus ends and contributes to growth directionality. Eukaryotic Cell 6, 555-562. (Pubitemid 46492343)
14. Garcia MA (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. (Pubitemid 32634347)
15. Gard DL, Becker BE, Josh Romney S (2004). MAPping the eukaryotic tree of life: structure, function, and evolution of the MAP215/Dis1 family of microtubule-associated proteins. Int Rev Cytol 239, 179-272. (Pubitemid 39349485)
16. Gard DL, Kirschner MW (1987). A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end. J Cell Biol 105, 2203-2215. (Pubitemid 18019070)
17. Gardner MK, Hunt AJ, Goodson HV, Odde DJ (2008). Microtubule assembly dynamics: new insights at the nanoscale. Curr Opin Cell Biol 20, 64-70.
18. Gergely F, Draviam VM, Raff JW (2003). The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev 17, 336-341. (Pubitemid 36182191)
19. Goshima G, Wollman R, Goodwin SS, Zhang N, Scholey JM, Vale RD, Stuurman N (2007). Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316, 417-421. (Pubitemid 46651486)
20. Guimaraes GJ, Dong Y, McEwen BF, Deluca JG (2008). Kinetochore- microtubule attachment relies on the disordered N-terminal tail domain of Hec1. Curr Biol 18, 1778-1784.
21. He X, Rines DR, Espelin CW, Sorger PK (2001). Molecular analysis of kinetochore-microtubule attachment in budding yeast. Cell 106, 195-206. (Pubitemid 32772630)
22. Howard J, Hyman AA (2003). Dynamics and mechanics of the microtubule plus end. Nature 422, 753-758. (Pubitemid 36514118)
23. Iwasa JH, Mullins RD (2007). Spatial and temporal relationships between actin-filament nucleation, capping, and disassembly. Curr Biol 17, 395-406.
24. Kawamura E, Wasteneys GO (2008). MOR1, the Arabidopsis thaliana homologue of Xenopus MAP215, promotes rapid growth and shrinkage, and suppresses the pausing of microtubules in vivo. J Cell Sci 121, 4114-4123.
25. Kerssemakers JWJ, Munteanu EL, Laan L, Noetzel TL, Janson ME, Dogterom M (2006). Assembly dynamics of microtubules at molecular resolution. Nature 442, 709-712. (Pubitemid 44215328)
26. Kinoshita K (2001). Reconstitution of physiological microtubule dynamics using purified components. Science 294, 1340-1343.
27. Kinoshita K, Habermann B, Hyman AA (2002). XMAP215: a key component of the dynamic microtubule cytoskeleton. Trends Cell Biol 12, 267-273. (Pubitemid 34634175)
28. Kosco KA, Pearson CG, Maddox PS, Wang PJ, Adams IR, Salmon ED, Bloom K, Huffaker TC (2001). Control of microtubule dynamics by Stu2p is essential for spindle orientation and metaphase chromosome alignment in yeast. Mol Biol Cell 12, 2870-2880. (Pubitemid 33051950)
29. Kumar P, Lyle KS, Gierke S, Matov A, Danuser G, Wittmann T (2009). GSK3beta phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J Cell Biol 184, 895-908.
30. Lansbergen G, Akhmanova A (2006). Microtubule plus end: a hub of cellular activities. Traffic 7, 499-507. (Pubitemid 44026748)
31. Lee MJ, Gergely F, Jeffers K, Peak-Chew SY, Raff JW (2001). Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour. Nature Cell Biol 3, 643-649. (Pubitemid 32624420)
32. Li W, Miki T, Watanabe T, Kakeno M, Sugiyama I, Kaibuchi K, Goshima G (2011). EB1 promotes microtubule dynamics by recruiting Sentin in Drosophila cells. J Cell Biol 193, 973-983.
33. Mitchison T, Kirschner M (1984). Dynamic instability of microtubule growth. Nature 312, 237-242.
34. Nakaseko Y, Goshima G, Morishita J, 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. (Pubitemid 32324756)
35. Niethammer P, Kronja I, Kandels-Lewis S, Rybina S, Bastiaens P, Karsenti E (2007). Discrete states of a protein interaction network govern interphase and mitotic microtubule dynamics. PLoS Biol 5, e29.
36. Popov AV, Pozniakovsky A, Arnal I, Antony C, Ashford AJ, Kinoshita K, Tournebize R, Hyman AA, Karsenti E (2001). XMAP215 regulates microtubule dynamics through two distinct domains. EMBO J 20, 397-410. (Pubitemid 32126976)
37. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, Waterman-Storer CM (2003). Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 5, 599-609. (Pubitemid 36818081)
38. Rogers GC, Rusan NM, Peifer M, Rogers SL (2008). A multicomponent assembly pathway contributes to the formation of acentrosomal microtubule arrays in interphase Drosophila cells. Mol Biol Cell 19, 3163-3178.
39. Rogers GC, Rusan NM, Roberts DM, Peifer M, Rogers SL (2009). The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J Cell Biol 184, 225-239.
40. Rogers SL, Rogers GC, Sharp DJ, Vale RD (2002). Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J Cell Biol 158, 873-884. (Pubitemid 35001079)
41. Rogers SL, Rogers GC (2008). Culture of Drosophila S2 cells and their use for RNAi-mediated loss-of-function studies and immunofluorescence microscopy. Nat Protoc 3, 606-611. (Pubitemid 351516756)
42. Sato M, Vardy L, Angel Garcia M, Koonrugsa N, Toda T (2004). Interdependency of fission yeast Alp14/TOG and coiled coil protein Alp7 in microtubule localization and bipolar spindle formation. Mol Biol Cell 15, 1609-1622. (Pubitemid 38401812)
43. Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, Davidson MW, Tsien RY (2008). Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods 5, 545-551. (Pubitemid 351761763)
44. Shirasu-Hiza M, (2003). Identification of XMAP215 as a microtubule-destabilizing factor in Xenopus egg extract by biochemical purification. J Cell Biol 161, 349-358.
45. Slep KC (2009). The role of TOG domains in microtubule plus end dynamics. Biochem Soc Trans 37, 1002-1006.
46. Slep KC, Vale RD (2007). Structural basis of microtubule plus end tracking by XMAP215, CLIP-170, and EB1. Mol Cell 27, 976-991. (Pubitemid 47488185)
47. Spittle C, Charrasse S, Larroque C, Cassimeris L (2000). The interaction of TOGp with microtubules and tubulin. J Biol Chem 275, 20748-20753. (Pubitemid 30457664)
48. Srayko M, Quintin S, Schwager A, Hyman AA (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. (Pubitemid 37078406)
49. Stone MC, Roegiers F, Rolls MM (2008). Microtubules have opposite orientation in axons and dendrites of Drosophila neurons. Mol Biol Cell 19, 4122-4129.
50. Subramanian R, Wilson-Kubalek EM, Arthur CP, Bick MJ, Campbell EA, Darst SA, Milligan RA, Kapoor TM (2010). Insights into antiparallel microtubule crosslinking by PRC1, a conserved nonmotor microtubule binding protein. Cell 142, 433-443.
51. Tanaka K, Mukae N, Dewar H, van Breugel M, James EK, Prescott AR, Antony C, Tanaka TU (2005). Molecular mechanisms of kinetochore capture by spindle microtubules. Nature 434, 987-994. (Pubitemid 40586041)
52. van Breugel M, Drechsel D, Hyman A (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. (Pubitemid 36529853)
53. van der Vaart B, Akhmanova A, Straube A (2009). Regulation of microtubule dynamic instability. Biochem Soc Trans 37, 1007-1013.
54. van der Vaart B et al. (2011). SLAIN2 links microtubule plus end-tracking proteins and controls microtubule growth in interphase. J Cell Biol 193, 1083-1099.
55. Vaughan KT (2005). TIP maker and TIP marker; EB1 as a master controller of microtubule plus ends. J Cell Biol 171, 197-200.
56. Widlund PO, Stear JH, Pozniakovsky A, Zanic M, Reber S, Brouhard GJ, Hyman AA, Howard J (2011). XMAP215 polymerase activity is built by combining multiple tubulin-binding TOG domains and a basic lattice-binding region. Proc Natl Acad Sci USA 108, 2741-2746.
57. Wittmann T, Bokoch GM, Waterman-Storer CM (2003). Regulation of leading edge microtubule and actin dynamics downstream of Rac1. J Cell Biol 161, 845-851. (Pubitemid 36718418)
58. Wittmann T, Bokoch GM, Waterman-Storer CM (2004). Regulation of microtubule destabilizing activity of Op18/stathmin downstream of Rac1. J Biol Chem 279, 6196-6203. (Pubitemid 38220653)
59. Wittmann T, Waterman-Storer CM (2005). Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3beta in migrating epithelial cells. J Cell Biol 169, 929-939. (Pubitemid 41002869)
60. Wolyniak MJ, Blake-Hodek K, Kosco K, Hwang E, You L, Huffaker TC (2006). The regulation of microtubule dynamics in Saccharomyces cerevisiae by three interacting plus-end tracking proteins. Mol Biol Cell 17, 2789-2798. (Pubitemid 43825514)
61. Zhang D et al. (2011). Drosophila katanin is a microtubule depolymerase that regulates cortical-microtubule plus-end interactions and cell migration. Nat Cell Biol 13, 361-370.