Tension-depenent regulation of microtubule dynamics at kinetochores can explain metaphase congression in yeast

Molecular Biology of the Cell

Volumn 16, Issue 8, 2005, Pages 3764-3775

  Gardner, Melissa K ^a   Pearson, Chad G ^b   Sprague, Brian L ^c   Zarzar, Ted R ^b   Bloom, Kerry ^b   Salmon, E D ^b   Odde, David J ^a  

^a University of Minnesota   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; GREEN FLUORESCENT PROTEIN; PROTEIN CSE4; UNCLASSIFIED DRUG; CDC6 PROTEIN, S CEREVISIAE; CELL CYCLE PROTEIN; CSE4 PROTEIN, S CEREVISIAE; DNA BINDING PROTEIN; NONHISTONE PROTEIN; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CENTROMERE; CHROMOSOME; CHROMOSOME REPLICATION; COMPUTER MODEL; CONTROLLED STUDY; DEPOLYMERIZATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; METAPHASE; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOSIS; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; YEAST; BIOLOGICAL MODEL; CHROMATIN; CYTOLOGY; GENETICS; METABOLISM; MUTATION; SACCHAROMYCES CEREVISIAE; SPECTROFLUOROMETRY;

SACCHAROMYCETALES;

CELL CYCLE PROTEINS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; KINETOCHORES; METAPHASE; MICROTUBULES; MODELS, BIOLOGICAL; MUTATION; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECTROMETRY, FLUORESCENCE;

EID: 23044453524     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-04-0275     Document Type: Article

References (54)

1. Biggins, S., and Murray, A. W. (2001). The budding yeast protein kinase Tpll/Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev. 15, 3118-3129.
2. Biggins, S., and Walczak, C. E. (2003). Captivating capture: how microtubules attach to kinetochores. Curr. Biol. 13, R449-460.
3. Brower-Toland, B. D., Smith, C. L., Yeh, R. C., Lis, J. T., Peterson, C. L., and Wang, M. D. (2002). Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. Proc. Natl. Acad. Sci. USA 99, 1960-1965.
4. Brown, G. C, and Kholodenko, B. N. (1999). Spatial gradients of cellular phospho-proteins. FEBS Lett. 457, 452-454.
5. Caplow, M., and Shanks, J. (1996). Evidence that a single monolayer tubulin-GTP cap is both necessary and sufficient to stabilize microtubules. Mol. Biol. Cell 7, 663-675.
6. Carminati, J. L., and Stearns, T. (1997). Microtubules orient the mitotic spindle in yeast through dynein-dependent interactions with the cell cortex. J. Cell Biol. 138, 629-641.
7. Cheeseman, I. M., Drubin, D. G., and Barnes, G. (2002). Simple centromere, complex kinetochore: linking spindle microtubules and centromeric DNA in budding yeast. J. Cell Biol. 157, 199-203.
8. Chen, Y., Baker, R. E., Keith, K. C., Harris, K., Stoler, S., and Fitzgerald-Hayes, M. (2000). The N terminus of the centromere H3-like protein Cse4p performs an essential function distinct from that of the histone fold domain. Mol. Cell. Biol. 20, 7037-7048.
9. Cimini, D., Cameron, L. A., and Salmon, E. D. (2004). Anaphase spindle mechanics prevent mis-segregation of merotelically oriented chromosomes. Curr. Biol. 14, 2149-2155.
10. Cleveland, D. W., Mao, Y., and Sullivan, K. F. (2003). Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112, 407-421.
11. Dewar, H., Tanaka, K., Nasmyth, K., and Tanaka, T. U. (2004). Tension between two kinetochores suffices for their bi-orientation on the mitotic spindle. Nature 428, 93-97.
12. Goshima, G., and Yanagida, M. (2001). Time course analysis of precocious separation of sister centromeres in budding yeast: continuously separated or frequently reassociated? Genes Cells 6, 765-773.
13. Guacci, V., Hogan, E., and Koshland, D. (1997). Centromere position in budding yeast: evidence for anaphase A. Mol. Biol. Cell 8, 957-972.
14. Gupta, M. L., Jr., Bode, C. J., Thrower, D. A., Pearson, C. G., Suprenant, K. A., Bloom, K. S., and Himes, R. H. (2002). beta-Tubulin C354 mutations that severely decrease microtubule dynamics do not prevent nuclear migration in yeast. Mol. Biol. Cell 13, 2919-2932.
15. He, X., Asthana, S., and Sorger, P. K. (2000). Transient sister chromarid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell 101, 763-775.
16. He, X., Rines, D. R., Espelin, C. W., and Sorger, P. K. (2001). Molecular analysis of kinetochore-microtubule attachment in budding yeast. Cell 106, 195-206.
17. Howard, J., and Hyman, A. A. (2003). Dynamics and mechanics of the microtubule plus end. Nature 422, 753-758.
18. Inoue, S., and Salmon, E. D. (1995). Force generation by microtubule assembly/disassembly in mitosis and related movements. Mol. Biol. Cell 6, 1619-1640.
19. Kalab, P., Weis, K., and Heald, R. (2002). Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 295, 2452-2456.
20. Kosco, K., A., Pearson, C. G., Maddox, P. S., Wang, P. J., Adams, I. R., Salmon, E. D., Bloom, K., and Huffaker, T. C. (2001). Control of microtubule dynamics by Stu2p is essential for spindle orientation and metaphase chromosome alignment in yeast. Mol. Biol. Cell 12, 2870-2880.
21. Krishnan, V., Nirantar, S., Crasta, K., Cheng, A. Y., and Surana, U. (2004). DNA replication checkpoint prevents precocious chromosome segregation by regulating spindle behavior. Mol. Cell 16, 687-700.
22. Maddox, P., Bloom, K., and Salmon, E. D. (2000). Polarity and dynamics of microtubule assembly in the budding yeast Saccharomyces cerevisiae. Nat. Cell Biol. 2, 36-41.
23. Maddox, P., Straight, A., Coughlin, P., Mitchison, T. J., and Salmon, E. D. (2003). Direct observation of microtubule dynamics at kinetochores in Xenopus extract spindles: implications for spindle mechanics. J. Cell Biol. 162, 377-382.
24. McIntosh, J. R. (2005). Rings around kinetochore microtubules in yeast. Nat. Struct. Mol. Biol. 12, 210-212.
25. Meluh, P. B., Yang, P., Glowczewski, L., Koshland, D., and Smith, M. M. (1998). Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94, 607-613.
26. Miranda, J. J., De Wulf, P., Sorger, P. K., and Harrison, S. C. (2005). The yeast DASH complex forms closed rings on microtubules. Nat. Struct. Mol. Biol. 12, 138-143.
27. Nasmyth, K. (2002). Segregating sister genomes: the molecular biology of chromosome separation. Science 297, 559-565.
28. Nicklas, R. B. (1988). The forces that move chromosomes in mitosis. Annu. Rev. Biophys. Biophys. Chem. 17, 431-449.
29. Nicklas, R. B., and Ward, S. C. (1994). Elements of error correction in mitosis: microtubule capture, release, and tension. J. Cell Biol. 126, 1241-1253.
30. Nicklas, R. B., Waters, J. C., Salmon, E. D., and Ward, S. C. (2001). Checkpoint signals in grasshopper meiosis are sensitive to microtubule attachment, but tension is still essential. J. Cell Sci. 114, 4173-4183.
31. O'Toole, E. T., Winey, M., and McIntosh, J. R. (1999). High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 10, 2017-2031.
32. Pearson, C. G., Maddox, P. S., Salmon, E. D., and Bloom, K. (2001). Budding yeast chromosome structure and dynamics during mitosis. J. Cell Biol. 152, 1255-1266.
33. Pearson, C. G., Maddox, P., S., Zarzar, T. R., Salmon, E. D., and Bloom, K. (2003). Yeast kinetochores do not stabilize Stu2p-dependent spindle microtubule dynamics. Mol. Biol. Cell 14, 4181-4195.
34. Pearson, C. G., Yeh, E., Gardner, M., Odde, D., Salmon, E. D., and Bloom, K. (2004). Stable kinetochore-microtubule attachment constrains centromere positioning in metaphase. Curr. Biol. 14, 1962-1967.
35. Peterson, J. B., and Ris, H. (1976). Electron-microscopic study of the spindle and chromosome movement in the yeast Saccharomyces cerevisiae. J. Cell Sci. 22, 219-242.
36. Rieder, C. L., and Salmon, E. D. (1994). Motile kinetochores and polar ejection forces dictate chromosome position on the vertebrate mitotic spindle. J. Cell Biol. 124, 223-233.
37. Rieder, C. L., and Salmon, E. D. (1998). The vertebrate cell kinetochore and its roles during mitosis. Trends Cell Biol. 8, 310-318.
38. Scholey, J. M., Brust-Mascher, I., and Mogilner, A. (2003). Cell division. Nature 422, 746-752.
39. Shaw, S. L., Yeh, E., Maddox, P., Salmon, E. D., and Bloom, K. (1997). Astral microtubule dynamics in yeast: a microtubule-based searching mechanism for spindle orientation and nuclear migration into the bud. J. Cell Biol. 139, 985-994.
40. Skibbens, R. V., Rieder, C. L., and Salmon, E. D. (1995). Kinetochore motility after severing between sister centromeres using laser microsurgery: evidence that kinetochore directional instability and position is regulated by tension. J. Cell Sci. 108, 2537-2548.
41. Skibbens, R. V., and Salmon, E. D. (1997). Micromanipulation of chromosomes in mitotic vertebrate tissue cells: tension controls the state of kinetochore movement. Exp. Cell Res. 235, 314-324.
42. Skibbens, R. V., Skeen, V. P., and Salmon, E. D. (1993). Directional instability of kinetochore motility during chromosome congression and segregation in mitotic newt lung cells: a push-pull mechanism. J. Cell Biol. 122, 859-875.
43. Sprague, B. L., Pearson, C. G., Maddox, P. S., Bloom, K. S., Salmon, E. D., and Odde, D. J. (2003). Mechanisms of microtubule-based kinetochore positioning in the yeast metaphase spindle. Biophys. J. 84, 1-18.
44. Stern, B. M., and Murray, A. W. (2001). Lack of tension at kinetochores activates the spindle checkpoint in budding yeast. Curr. Biol. 11, 1462-1467.
45. Straight, A. F. (1997). Cell cycle: checkpoint proteins and kinetochores. Curr. Biol. 7, R613.
46. Tanaka, T., Fuchs, J., Loidl, J., and Nasmyth, K. (2000). Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation. Nat. Cell Biol. 2, 492-499.
47. Tirnauer, J. S., O'Toole, E. O., Berrueta, L., Bierer, B. E., and Pellman, D. (1999). Yeast Bim1p promotes the G1-specific dynamics of microtubules. J. Cell Biol. 145, 993-1007.
48. Tirnauer, J. S., Salmon, E. D., and Mitchison, T. J. (2004). Microtubule plus-end dynamics in Xenopus egg extract spindles. Mol. Biol. Cell 15, 1776-1784.
49. Van Breugel, M., Drechsel, D., and Hyman, A. (2003). Stu2p, the budding yeast member of the conserved Dis1/XMAP215 family of microtubule-associated proteins is a plus end-binding microtubule destabilizes J. Cell Biol. 161, 359-369.
50. VanBuren, V., Odde, D. J., and Cassimeris, L. (2002). Estimates of lateral and longitudinal bond energies within the microtubule lattice. Proc. Natl. Acad. Sci. USA 99, 6035-6040
51. [correction published in Proc. Natl. Acad. Sci. USA (2004). 102, 14989].
52. Westermann, S., Avila-Sakar, A., Wang, H. W., Niederstrasser, H., Wong, J., Drubin, D. G., Nogales, E., and Barnes, G. (2005). Formation of a dynamic kinetochore-microtubule interface through assembly of the Dam1 ring complex. Mol. Cell 17, 277-290.
53. Winey, M., Mamay, C. L., O'Toole, E. T., Mastronarde, D. N., Giddings, T. H., Jr., McDonald, K. L., and McIntosh, J. R. (1995). Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle. J. Cell Biol. 129, 1601-1615.
54. Zhou, J., Yao, J., and Joshi, H. C. (2002). Attachment and tension in the spindle assembly checkpoint. J. Cell Sci. 115, 3547-3555.