Molecular mechanisms of kinetochore capture by spindle microtubules

Nature

Volumn 434, Issue 7036, 2005, Pages 987-994

  Tanaka, Kozo ^a   Mukae, Naomi ^a   Dewar, Hilary ^a   Van Breugel, Mark ^b   James, Euan K ^a   Prescott, Alan R ^a   Antony, Claude ^c   Tanaka, Tomoyuki U ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOMES; CRYSTAL ORIENTATION; KINEMATICS; PROTEINS; TUBES (COMPONENTS); VISUALIZATION;

CHROMOSOME SEGREGRATION; KINETOCHORE CAPTURE; MOLECULAR MECHANISMS; SACCHAROMYCES;

MOLECULAR DYNAMICS;

GUANINE NUCLEOTIDE EXCHANGE FACTOR; KAR3 PROTEIN; KINESIN; RAN PROTEIN; UNCLASSIFIED DRUG; KAR3 PROTEIN, S CEREVISIAE; MICROTUBULE ASSOCIATED PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; STU2 PROTEIN, S CEREVISIAE;

BIOLOGY;

ARTICLE; CENTROMERE; CHROMOSOME SEGREGATION; MICROTUBULE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SPINDLE CELL; SPINDLE POLE BODY; CELL CYCLE; CHROMOSOME; CYTOLOGY; METABOLISM; MITOSIS SPINDLE; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

BIOLOGICAL TRANSPORT; CELL CYCLE; CHROMOSOME SEGREGATION; CHROMOSOMES, FUNGAL; KINESIN; KINETOCHORES; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; RAN GTP-BINDING PROTEIN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 17844391253     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/nature03483     Document Type: Article

References (50)

1. McIntosh, J. R., Grishchuk, E. L. & West, R. R. Chromosome- microtubule interactions during mitosis. Annu. Rev. Cell Dev. Biol. 18, 193-219 (2002).
2. Rieder, C. L. & Alexander, S. P. Kinetochores are transported poleward along a single astral microtubule during chromosome attachment to the spindle in newt lung cells. J. Cell Biol. 110, 81-95 (1990).
3. Hayden, J. H., Bowser, S. S. & Rieder, C. L. Kinetochores capture astral microtubules during chromosome attachment to the mitotic spindle: direct visualization in live newt lung cells. J. Cell Biol. 111, 1039-1045 (1990).
4. Merdes, A. & De Mey, J. The mechanism of kinetochore-spindle attachment and polewards movement analyzed in PtK2 cells at the prophase-prometaphase transition. Eur. J. Cell Biol. 53, 313-325 (1990).
5. Goshima, G. & Yanagida, M. Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast. Cell 100, 619-633 (2000).
6. He, X., Asthana, S. & Sorger, P. K. Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell 101, 763-775 (2000).
7. Tanaka, T., Fuchs, J., Loidl, J. & Nasmyth, K. Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation. Nature Cell Biol. 2, 492-499 (2000).
8. Pearson, C. G., Maddox, P. S., Salmon, E. D. & Bloom, K. Budding yeast chromosome structure and dynamics during mitosis. J. Cell Biol. 152, 1255-1266 (2001).
9. Winey, M. & O'Toole, E. T. The spindle cycle in budding yeast. Nature Cell Biol. 3, E23-E27 (2001).
10. Tanaka, T. U. et al. Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108, 317-329 (2002).
11. Tanaka, T. U. Chromosome bi-orientation on the mitotic spindle. Phil. Trans. R. Soc. Lond. B (in the press); doi:10.1098/rstb.2004.1612.
12. Hill, A. & Bloom, K. Genetic manipulation of centromere function. Mol. Cell. Biol. 7, 2397-2405 (1987).
13. Michaelis, C., Ciosk, R. & Nasmyth, K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35-45 (1997).
14. Nasmyth, K., Peters, J. M. & Uhlmann, F. Splitting the chromosome: cutting the ties that bind sister chromatids. Science 288, 1379-1385 (2000).
15. O'Toole, E. T., Winey, M. & McIntosh, J. R. High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 10, 2017-2031 (1999).
16. Gupta, M. L. Jr et al. β-Tubulin C354 mutations that severely decrease microtubule dynamics do not prevent nuclear migration in yeast. Mol. Biol. Cell 13, 2919-2932 (2002).
17. McAinsh, A. D., Tytell, J. D. & Sorger, P. K. Structure, function, and regulation of budding yeast kinetochores. Annu. Rev. Cell Dev. Biol. 19, 519-539 (2003).
18. Dewar, H., Tanaka, K., Nasmyth, K. & Tanaka, T. U. Tension between two kinetochores suffices for their bi-orientation on the mitotic spindle. Nature 428, 93-97 (2004).
19. Akhmanova, A. & Hoogenraad, C. C. Microtubule plus-end-tracking proteins: mechanisms and functions. Curr. Opin. Cell Biol. 17, 47-54 (2005).
20. Corbett, A. H. & Silver, P. A. Nucleocytoplasmic transport of macromolecules. Microbiol. Mol. Biol. Rev. 61, 193-211 (1997).
21. Hetzer, M., Gruss, O. J. & Mattaj, I. W. The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly. Nature Cell Biol 4, E177-E184 (2002).
22. Quimby, B. B. & Dasso, M. The small GTPase Ran: interpreting the signs. Curr. Opin. Cell Biol. 15, 338-344 (2003).
23. Wilde, A. et al. Ran stimulates spindle assembly by altering microtubule dynamics and the balance of motor activities. Nature Cell Biol. 3, 221-227 (2001).
24. Carazo-Salas, R. E., Gruss, O. J., Mattaj, I. W. & Karsenti, E. Ran-GTP coordinates regulation of microtubule nucleation and dynamics during mitotic-spindle assembly. Nature Cell Biol. 3, 228-234 (2001).
25. Biggins, S. et al. The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev. 13, 532-544 (1999).
26. Cheeseman, I. M., Enquist-Newman, M., Muller-Reichert, T., Drubin, D. G. & Barnes, G. Mitotic spindle integrity and kinetochore function linked by the Duo1p/Dam1p complex. J. Cell Biol. 152, 197-212 (2001).
27. He, X., Rines, D. R., Espelin, C. W. & Sorger, P. K. Molecular analysis of kinetochore-microtubule attachment in budding yeast. Cell 106, 195-206 (2001).
28. Janke, C., Ortiz, J., Tanaka, T. U., Lechner, J. & Schiebel, E. Four new subunits of the Dam1-Duo1 complex reveal novel functions in sister kinetochore biorientation. EMBO J. 21, 181-193 (2002).
29. Li, Y. et al. The mitotic spindle is required for loading of the DASH complex onto the kinetochore. Genes Dev. 16, 183-197 (2002).
30. Maddox, P. S., Bloom, K. S. & Salmon, E. D. The polarity and dynamics of microtubule assembly in the budding yeast Saccharomyces cerevisiae. Nature Cell Biol. 2, 36-41 (2000).
31. Tirnauer, I. S., O'Toole, E., Berrueta, L., Bierer, B. E. & Pellman, D. Yeast Bim1p promotes the G1-specific dynamics of microtubules. J. Cell Biol. 145, 993-1007 (1999).
32. van Breugel, M., Drechsel, D. & Hyman, A. 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 (2003).
33. Lin, H. et al. Polyploids require Bik1 for kinetochore-microtubule attachment. J. Cell Biol. 155, 1173-1184 (2001).
34. Carvalho, P., Gupta, M. L. Jr, Hoyt, M. A. & Pelhnan, D. Cell cycle control of kinesin-mediated transport of Bik1 (CLIP-170) regulates microtubule stability and dynein activation. Dev. Cell 6, 815-829 (2004).
35. Hildebrandt, E. R. & Hoyt, M. A. Mitotic motors in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1496, 99-116 (2000).
36. Saunders, W. S., Koshland, D., Eshel, D., Gibbons, I. R. & Hoyt, M. A. Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation. J. Cell Biol. 128, 617-624 (1995).
37. Meluh, P. B. & Rose, M. D. KAR3, a kinesin-related gene required for yeast nuclear fusion. Cell 60, 1029-1041 (1990).
38. Maddox, P. S., Stemple, J. K., Satterwhite, L., Salmon, E. D. & Bloom, K. The minus end-directed motor Kar3 is required for coupling dynamic microtubule plus ends to the cortical shmoo tip in budding yeast. Curr. Biol. 13, 1423-1428 (2003).
39. Muller-Reichert, T. et al. Analysis of the distribution of the kinetochore protein Ndc10p in Saccharomyces cerevisiae using 3-D modeling of mitotic spindles. Chromosoma 111, 417-428 (2003).
40. Adams, I. R. & Kilmartin, J. V. Spindle pole body duplication: a model for centrosome duplication? Trends Cell Biol. 10, 329-335 (2000).
41. Cheeseman, I. M. et al. Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase 1p11p. Cell 111, 163-172 (2002).
42. Westermann, S. et al. Architecture of the budding yeast kinetochore reveals a conserved molecular core. J. Cell Biol. 163, 215-222 (2003).
43. Nekrasov, V. S., Smith, M. A., Peak-Chew, S. & Kilmartin, J. V. Interactions between centromere complexes in Saccharomyces cerevisiae. Mol. Biol. Cell 14, 4931-4946 (2003).
44. De Wulf, P., McAinsh, A. D. & Sorger, P. K. Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev. 17, 2902-2921 (2003).
45. Miranda, J. L., De Wulf, P., Sorger, P. & Harrison, S. C. The yeast DASH complex forms closed rings on microtubules. Nature Struct. Mol. Biol. 12, 138-143 (2005).
46. Westermann, S. et al. Formation of a dynamic kinetochore-microtubule interface through assembly of the Dam1 ring complex. Mol. Cell 17, 277-290 (2005).
47. Pickett-Heaps, J. D. Cell division in diatoms. Int. Rev. Cytol. 128, 63-107 (1991).
48. Carazo-Salas, R. E. & Karsenti, E. Long-range communication between chromatin and microtubules in Xenopus egg extracts. Curr. Biol. 13, 1728-1733 (2003).
49. Alexander, S. P. & Rieder, C. L. Chromosome motion during attachment to the vertebrate spindle: initial saltatory-like behavior of chromosomes and quantitative analysis of force production by nascent kinetochore fibers. J. Cell Biol. 113, 805-815 (1991).
50. King, J. M., Hays, T. S. & Nicklas, R. B. Dynein is a transient kinetochore component whose binding is regulated by microtubule attachment, not tension. J. Cell Biol. 151, 739-748 (2000).