TOGp regulates microtubule assembly and density during mitosis and contributes to chromosome directional instability

Cell Motility and the Cytoskeleton

Volumn 66, Issue 8, 2009, Pages 535-545

  Cassimeris, Lynne ^a   Becker, Bret ^a   Carney, Bruce ^a  

^a LEHIGH UNIVERSITY   (United States)

Author keywords

Kid; Microtubule associated proteins; Microtubule dynamics; Spindle; TACC3

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CELL PROTEIN; GREEN FLUORESCENT PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NOCODAZOLE; SMALL INTERFERING RNA; TOGP PROTEIN; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; BLEACHING; CELL ADHESION; CELL DENSITY; CELL GROWTH; CELL MOTILITY; CELL POLARITY; CENTROMERE; CHROMATIN; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; CYTOLYSIS; DEPOLYMERIZATION; FEMALE; FLUORESCENCE; GENE DELETION; HELA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; METAPHASE; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOSIS; OSCILLATION; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN PROTEIN INTERACTION;

CHROMOSOMAL INSTABILITY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENT ANTIBODY TECHNIQUE; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; KINETOCHORES; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; RNA, SMALL INTERFERING; TUBULIN;

EID: 67749113756     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20359     Document Type: Article

References (62)

1. Aoki K, Nakaseko Y, Kinoshita K, Goshima G, Yanagida M. 2006. Cdc2 phosphorylation of the fission yeast Dis1 ensures accurate chromosome segregation. Curr Biol 16:1627-1635. (Pubitemid 44251180)
2. Barr AR, Gergely F. 2008. MCAK-independent functions of ch-TOG/XMAP215 in microtubule plus-end dynamics. Mol Cell Biol 28:7199-7211.
3. Becker BE, Romney SJ, Gard DL. 2003. XMAP215, XKCM1, NuMA and cytoplasmic dynein are required for the assembly and organization of the transient microtubule array during maturation of Xenopus oocytes. Dev Biol 261:488-505.
4. Bellanger JM, Gonczy P. 2003. TAC-1 and ZYG-9 form a complex that promotes microtubule assembly in C. elegans embryos. Curr Biol 13:1488-1498. (Pubitemid 37078404)
5. Bonfils C, Bec N, Lacroix B, Harricane M-C, Larroque C. 2007. Kinetic analysis of tubulin assembly in the presence of the microtubule associated proteins TOGp. J Biol Chem 282:5570-5581. (Pubitemid 47093746)
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. Cameron LA, Yang G, Cimini D, Canman JC, Kisurina-Evgenieva O, Khodjakov A, Danuser G, Salmon ED. 2006. Kinesin 5-independent poleward flux of kinetochore microtubules in PtK1 cells. J Cell Biol 173:173-179.
8. Cassimeris L, Morabito J. 2004. TOGp, the human homolog of XMAP215/Dis1, is required for centrosome integrity, spindle pole organization and bipolar spindle assembly. Mol Biol Cell 15:1580-1590. (Pubitemid 38401809)
9. Chen R-H, Waters JC, Salmon ED, Murray AW. 1996. Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores. Science 274:242-246.
10. Cimini D, Cameron LA, Salmon ED. 2004. Anaphase spindle mechanics prevent mis-segregation of merotelically oriented chromosomes. Curr Biol 14:2149-2155.
11. Civelekoglu-Scholey G, Sharp DJ, Mogilner A, Scholey JM. 2006. Model of chromosome motility in Drosophila embryos: Adaptation of a general mechanism for rapid mitosis. Biophys J 90:3966-3982. (Pubitemid 43846114)
12. Conte N, Delaval B, Ginestier C, Ferrand A, Isnardon D, Larroque C, Prigent C, Seraphin B, Jacquemier J, Birnbaum D. 2003. TACC1-chTOG-Aurora A protein complex in breast cancer. Oncogene 22:8102-8116. (Pubitemid 37487301)
13. DeLuca J, Gall WE, Ciferri C, Chimin D, Musacchio A, Salmon ED. 2006. Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127:969-982.
14. Ehrhardt AG, Sluder G. 2005. Spindle pole fragmentation due to proteasome inhibition. J Cell Physiol 204:808-818. (Pubitemid 41099266)
15. Elowe S, Hummer S, Uldschmid A, Li X, Nigg EA. 2007. Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev 21:2205-2219. (Pubitemid 47360842)
16. Gadde S, Heald R. 2004. Mechanisms and molecules of the mitotic spindle. Curr Biol 14:R797-R805.
17. Garcia MA, Vardy L, Koonrugsa N, 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. (Pubitemid 32634347)
18. Garcia MA, Koonrugsa N, Toda T. 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. (Pubitemid 35415320)
19. Gard DL, Becker BE, Romney SJ. 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.
20. Gardner M, Odde DJ. 2006. Modeling of chromosome motility during mitosis. Curr Opin Cell Bio 18:639-647.
21. Gerlich D, Hirota T, Koch B, Peters JM, Ellenberg J. 2006. Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr Biol 16:333-344. (Pubitemid 43259343)
22. Gergely F, Karlson C, Still I, Cowell J, Kilmartin J, Raff JW. 2000a. The TACC domain identifies a family of centrosomal proteins that can interact with microtubules. Proc Natl Acad Sci USA 97:14352-14357. (Pubitemid 32016579)
23. Gergely F, Kidd D, Jeffers K, Wakefield JG, Raff JW. 2000b. DTACC a novel centrosomal protein required for normal spindle function in the early Drosophila embryo. EMBO J 19:241-252. (Pubitemid 30042706)
24. Gergely F, Daviam 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)
25. Goshima G, Nedelec F, Vale RD. 2005. Mechanisms for focusing mitotic spindle poles by minus end-directed motor proteins. J Cell Biol 171:229-240. (Pubitemid 41540016)
26. Gordon MB, Howard L, Compton DA. 2001. Chromosome movement in mitosis requires microtubule anchorage at spindle poles. J Cell Biol 152:425-434 (Pubitemid 34280228)
27. Graf R, Daunderer C, Schliwa M. 2000. Dictyostelium DdCP224 is a microtubule-associated protein and a permanent centrosomal resident involved in centrosome duplication. J Cell Sci 113:1747-1758. (Pubitemid 30333124)
28. 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.
29. He X, Rines DR, Espelin CW, Sorger PK. 2001. Molecular analysis of kinetochore-microtubule attachment in budding yeast. Cell 106:195-206. (Pubitemid 32772630)
30. Holmfeldt P, Stenmark S, Gullberg M. 2004. Differential functional interplay of TOGp/XMAP215 and KinI kinesin MCAK during interphase and mitosis. EMBO J 23:627-637. (Pubitemid 38282394)
31. Howell BJ, McEwen BF, Canman JC, Hoffman DB, Farrar EM, Rieder CL, Salmon ED. 2001. Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J Cell Biol 155:1159-1172.
32. Kapoor TM, Compton DA. 2002. Searching for the middle ground: Mechanisms of chromosome alignment during mitosis. J Cell Biol 157:551-556.
33. Khodjakov A, Rieder CL. 1996. Kinetochores moving away from their associated pole do not exert a significant pushing force on the chromosome. J Cell Biol 135:315-327. (Pubitemid 26359328)
34. Kinoshita K, Noetzel TL, Pelletier L, Mechtler K, Drechsel DN, Schwager ML, Raff JW, Hyman AA. 2005. Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis. J Cell Biol 170:1047-1055. (Pubitemid 41362637)
35. Kline-Smith SL, Khodajkov A, Hergert P, Walczak CE. 2004. Depletion of centromeric MCAK leads to chromosome congression and segregation defects due to improper kinetochore attachments. Mol Biol Cell 15:1146-1159. (Pubitemid 38316223)
36. 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)
37. Lee MJ, Gergely F, Jeffers K, Peak-Chew S, Raff JW. 2001. Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behavior. Nat Cell Biol 3:643-649. (Pubitemid 32624420)
38. Levesque AA, Compton DA. 2001. The chromokinesin Kid is necessary for chromosome arm orientation and oscillation, but not congression, on mitotic spindles. J Cell Biol 154:1135-1146.
39. Matthews LR, Carter P, Thierry-Mieg D, Kemphues K. 1998. ZYG-9. A Caenorhabditis elegans protein required for microtubule organization and function, is a component of meitotic and mitotic spindle poles. J Cell Biol 141:1159-1168. (Pubitemid 28265610)
40. Meraldi P, Draviam VM, Sorger PK. 2004. Timing and checkpoints in the regulation of mitotic progression. Dev Cell 7:45-60. (Pubitemid 39172687)
41. Musacchio A, Salmon ED. 2007. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8:379-393.
42. Nakaseko Y, Goshima G, Morishia 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)
43. O'Connell CB, Khodajakov AL. 2007. Cooperative mechanisms of mitotic spindle formation. J Cell Sci 120:1717-1722.
44. Piehl M, Cassimeris L. 2003. Organization and dynamics of growing microtubule plus ends during early mitosis. Mol Biol Cell 14:916-925. (Pubitemid 36337442)
45. Popov AV, Karsenti E. 2003. Stu2p and XMAP215: Turncoat microtubule-associated proteins?. Trends in Cell Biol 13:547-550. (Pubitemid 37311392)
46. Popov AV, Severin F, Karsenti E. 2002. XMAP215 is required for the microtubule-nucleating activity of centrosomes. Curr Biol 12:1326-1330. (Pubitemid 34869884)
47. Rieder CL. 1981. The structure of the cold-stable kinetochore fiber in metaphase PtK1 cells. Chromosoma 84:145-158.
48. Salmon ED, Wadsworth P. 1986. Fluorescence studies of tubulin and microtubule dynamics in living cells. In: Taylor DL, Waggoner AS, Murphy RF, Lanni F, Birge RR, editors. Applications of Fluorescence in the Biomedical Sciences. New York: Alan R Liss. p 377-403.
49. Saxton WM, Stemple DL, Leslie RJ, Salmon ED, Zavortink M, McIntosh JR. 1984. Tubulin dynamics in cultured mammalian cells. J Cell Biol 99:2175-2186. (Pubitemid 15181881)
50. Shirasu-Hiza M, Coughlin P, Mitchison T. 2003. Identification of XMAP215 as a microtubule-destabilizing factor in Xenopus egg extract by biochemical purification. J Cell Biol 161:349-358. (Pubitemid 36529852)
51. Skibbens RV, Skeen VP, Salmon ED. 1993. Directional instability of kinetochore motility during chromosome congression and segregation in mitotic newt lung cells. J Cell Biol 122:859-875.
52. Sryako 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)
53. Stumpff J, von Dassow G, Wagenbach M, Asbury C, Wordeman L. 2008. The kinesin-8 motor Kif18a suppresses kinetochore movements to control mitotic chromosome alignment. Dev Cell 14:252-262. (Pubitemid 351189173)
54. Tokai-Nishizumi N, Ohsugi M, Suzuki E, Yamamoto T. 2005. The chromokinesin Kid is required for maintenance of proper metaphase spindle size. Mol Biol Cell 16:5455-5463. (Pubitemid 41566853)
55. Tournebize R, Popov A, Kinoshita K, Ashford AJ, Rybina S, Pozniakovsky A, Mayer TU, Walczak CE, Karsenti E, Hyman AA. 2000. Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nature Cell Biol 2:13-19. (Pubitemid 30785937)
56. Tulu US, Fagerstrom C, Ferenz NP, Wadsworth P. 2006. Molecular requirements for kinetochore-associated microtubule formation in mammalian cells. Curr Biol 16:536-541. (Pubitemid 43343717)
57. 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)
58. Vasquez RJ, Gard DL, Cassimeris L. 1994. XMAP from Xenopus eggs promotes rapid plus end assembly of microtubules and rapid microtubule polymer turnover. J Cell Biol 127:985-993. (Pubitemid 24355987)
59. Wadsworth P, Khodjakov A. 2004. E. pluribus unum: Towards a universal mechanism for spindle assembly. Trends Cell Biol 14:413-419. (Pubitemid 39092698)
60. Wang PJ, Huffaker TC. 1997. Stu2p: A microtubule-binding protein that is an essential component of the yeast spindle pole body. J Cell Biol 139:1271-1280.
61. Wordeman L, Wagenbach M, von Dassow G. 2008. MCAK facilitates chromosome movement by promoting kinetochore microtubule turnover. J Cell Biol 179:869-879. (Pubitemid 350223485)
62. Zhai Y, Kronebusch PJ, Borisy GG. 1995. Kinetochore microtubule dynamics and the metaphase-anaphase transition. J Cell Biol 131:721-734.