Highly transient molecular interactions underlie the stability of kinetochore-microtubule attachment during cell division

Cellular and Molecular Bioengineering

Volumn 6, Issue 4, 2013, Pages 393-405

  Zaytsev, Anatoly V ^a   Ataullakhanov, Fazly I ^b,c,d   Grishchuk, Ekaterina L ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CENTER FOR THEORETICAL PROBLEMS OF PHYSICOCHEMICAL PHARMACOLOGY   (Russian Federation)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

^d Clinical Center of Pediatric Hematology Oncology and Immunology   (Russian Federation)

Author keywords

Affinity; Cooperativity; Mathematical modeling; Microtubule binding; Phosphorylation

Indexed keywords

BINDING PROTEIN; MICROTUBULE BINDING PROTEIN; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; BINDING SITE; CELL DIVISION; CENTROMERE; CONTROLLED STUDY; KINETICS; MATHEMATICAL MODEL; MICROTUBULE; MOLECULAR INTERACTION; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM;

EID: 84890306390     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-013-0309-4     Document Type: Article

References (48)

1. Akiyoshi, B., K. K. Sarangapani, A. F. Powers, C. R. Nelson, S. L. Reichow, H. Arellano-Santoyo, T. Gonen, J. A. Ranish, C. L. Asbury, and S. Biggins. Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468(7323):576-579, 2010.
2. Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter. Molecular Biology of the Cell (5th ed.). New York: Garland Science, pp. 1082-1086, 2008.
3. Alushin, G. M., V. Musinipally, D. Matson, J. Tooley, P. T. Stukenberg, and E. Nogales. Multimodal microtubule binding by the Ndc80 kinetochore complex. Nat. Struct. Mol. Biol. 19(11):1161-1167, 2012.
4. Alushin, G. M., V. H. Ramey, S. Pasqualato, D. A. Ball, N. Grigorieff, A. Musacchio, and E. Nogales. The Ndc80 kinetochore complex forms oligomeric arrays along microtubules. Nature 467(7317):805-810, 2010.
5. Aravamudhan, P., I. Felzer-Kim, and A. P. Joglekar. The budding yeast point centromere associates with two Cse4 molecules during mitosis. Curr. Biol. 23(9):770-774, 2013.
6. Armond, J. W., and M. S. Turner. Force transduction by the microtubule-bound Dam1 ring. Biophys. J. 98(8):1598-1607, 2010.
7. Bakhoum, S. F., G. Genovese, and D. A. Compton. Deviant kinetochore microtubule dynamics underlie chromosomal instability. Curr. Biol. 19(22):1937-1942, 2009.
8. Bakhoum, S. F., S. L. Thompson, A. L. Manning, and D. A. Compton. Genome stability is ensured by temporal control of kinetochore-microtubule dynamics. Nat. Cell Biol. 11(1):27-35, 2009.
9. Cheeseman, I. M., S. Anderson, M. Jwa, E. M. Green, J. Kang, J. R. Yates, 3rd, C. S. Chan, D. G. Drubin, and G. Barnes. Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111(2):163-172, 2002.
10. Cheeseman, I. M., J. S. Chappie, E. M. Wilson-Kubalek, and A. Desai. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127(5):983-997, 2006.
11. Cimini, D., X. Wan, C. B. Hirel, and E. D. Salmon. Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors. Curr. Biol. 16(17):1711-1718, 2006.
12. Civelekoglu-Scholey, G., B. He, M. Shen, X. Wan, E. Roscioli, B. Bowden, and D. Cimini. Dynamic bonds and polar ejection force distribution explain kinetochore oscillations in PtK1 cells. J. Cell Biol. 201(4):577-593, 2013.
13. DeLuca, J. G., W. E. Gall, C. Ciferri, D. Cimini, A. Musacchio, and E. D. Salmon. Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127(5):969-982, 2006.
14. Dong, Y., K. J. Vanden Beldt, X. Meng, A. Khodjakov, and B. F. McEwen. The outer plate in vertebrate kinetochores is a flexible network with multiple microtubule interactions. Nat. Cell Biol. 9(5):516-522, 2007.
15. Efremov, A., E. L. Grishchuk, J. R. McIntosh, and F. I. Ataullakhanov. In search of an optimal ring to couple microtubule depolymerization to processive chromosome motions. Proc. Natl. Acad. Sci. U.S.A. 104(48):19017-19022, 2007.
16. Franck, A. D., A. F. Powers, D. T. Gestaut, T. Gonen, T. N. Davis, and C. L. Asbury. Tension applied through the Dam1 complex promotes microtubule elongation providing a direct mechanism for length control in mitosis. Nat. Cell Biol. 9(7):832-837, 2007.
17. Gardner, M. K., C. G. Pearson, B. L. Sprague, T. R. Zarzar, K. Bloom, E. D. Salmon, and D. J. Odde. Tension-dependent regulation of microtubule dynamics at kinetochores can explain metaphase congression in yeast. Mol. Biol. Cell 16:3764-3775, 2005.
18. Grishchuk, E. L., J. R. McIntosh, M. I. Molodtsov, and F. I. Ataullakhanov. Comprehensive Biophysics, Vol. 4. Amsterdam: Elsevier, pp. 93-117, 2012.
19. Hill, A. V. The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J. Physiol. 40:iv-vii, 1910.
20. Hill, T. L. Theoretical problems related to the attachment of microtubules to kinetochores. Proc. Natl. Acad. Sci. U.S.A. 82:4404-4408, 1985.
21. Joglekar, A. P., and A. J. Hunt. A simple, mechanistic model for directional instability during mitotic chromosome movements. Biophys. J. 83(1):42-58, 2002.
22. Johnston, K., A. Joglekar, T. Hori, A. Suzuki, T. Fukagawa, and E. D. Salmon. Vertebrate kinetochore protein architecture: protein copy number. J. Cell Biol. 189(6):937-943, 2010.
23. Jordan, M. A., and K. Kamath. How do microtubule-targeted drugs work? An overview. Curr. Cancer Drug Targets 7(8):730-742, 2007.
24. Lawrimore, J., K. S. Bloom, and E. D. Salmon. Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome. J. Cell Biol. 195(4):573-582, 2011.
25. Liu, J., and J. N. Onuchic. A driving and coupling "Pac-Man" mechanism for chromosome poleward translocation in anaphase A. Proc. Natl. Acad. Sci. U.S.A. 103(49):18432-18437, 2006.
26. McDonald, K. L., E. T. O'Toole, D. N. Mastronarde, and J. R. McIntosh. Kinetochore microtubules in PTK cells. J. Cell Biol. 118(2):369-383, 1992.
27. McEwen, B. F., A. B. Heagle, G. O. Cassels, K. F. Buttle, and C. L. Rieder. Kinetochore fiber maturation in PtK1 cells and its implications for the mechanisms of chromosome congression and anaphase onset. J. Cell Biol. 137(7):1567-1580, 1997.
28. McIntosh, J. R., E. L. Grishchuk, M. K. Morphew, A. K. Efremov, K. Zhudenkov, V. A. Volkov, I. M. Cheeseman, A. Desai, D. N. Mastronarde, and F. I. Ataullakhanov. Fibrils connect microtubule tips with kinetochores: a mechanism to couple tubulin dynamics to chromosome motion. Cell 135(2):322-333, 2008.
29. McIntosh, J. R., E. L. Grishchuk, and R. R. West. Chromosome-microtubule interactions during mitosis. Annu. Rev. Cell Dev. Biol. 18:193-219, 2002.
30. McIntosh, J. R., E. O'Toole, K. Zhudenkov, M. Morphew, C. Schwartz, F. I. Ataullakhanov, and E. L. Grishchuk. Conserved and divergent features of kinetochores and spindle microtubule ends from five species. J. Cell Biol. 200(4):459-474, 2013.
31. Molodtsov, M. I., E. L. Grishchuk, A. K. Efremov, J. R. McIntosh, and F. I. Ataullakhanov. Force production by depolymerizing microtubules. Proc. Natl. Acad. Sci. U.S.A. 102(12):4353-4358, 2005.
32. Nicklas, R. B. Chromosome velocity during mitosis as a function of chromosome size and position. J. Cell Biol. 25:119-135, 1965.
33. Powers, A. F., A. D. Franck, D. R. Gestaut, J. Cooper, B. Gracyzk, R. R. Wei, L. Wordeman, T. N. Davis, and C. L. Asbury. The Ndc80 kinetochore complex forms load-bearing attachments to dynamic microtubule tips via biased diffusion. Cell 136(5):865-875, 2009.
34. Rank, K. C., and I. Rayment. Functional asymmetry in kinesin and dynein dimers. Biol. Cell 105(1):1-13, 2013.
35. Santaguida, S., and A. Musacchio. The life and miracles of kinetochores. EMBO J. 28(17):2511-2531, 2009.
36. Schmidt, J. C., H. Arthanari, A. Boeszoermenyi, N. M. Dashkevich, E. M. Wilson-Kubalek, N. Monnier, M. Markus, M. Oberer, R. A. Milligan, M. Bathe, G. Wagner, E. L. Grishchuk, and I. M. Cheeseman. The kinetochore-bound Ska1 complex tracks depolymerizing microtubules and binds to curved protofilaments. Dev. Cell 23(5):968-980, 2012.
37. Shen, Q. T., P. P. Hsiue, C. V. Sindelar, M. D. Welch, K. G. Campellone, and H. W. Wang. Structural insights into WHAMM-mediated cytoskeletal coordination during membrane remodeling. J. Cell Biol. 199(1):111-124, 2012.
38. Shivaraju, M., J. R. Unruh, B. D. Slaughter, M. Mattingly, J. Berman, and J. L. Gerton. Cell-cycle-coupled structural oscillation of centromeric nucleosomes in yeast. Cell 150(2):304-316, 2012.
39. Shtylla, B., and J. P. Keener. A mechanomolecular model for the movement of chromosomes during mitosis driven by a minimal kinetochore bicyclic cascade. J. Theor. Biol. 263(4):455-470, 2010.
40. Thompson, S. L., S. F. Bakhoum, and D. A. Compton. Mechanisms of chromosomal instability. Curr. Biol. 20(6):R285-R295, 2010.
41. Umbreit, N. T., D. R. Gestaut, J. F. Tien, B. S. Vollmar, T. Gonen, C. L. Asbury, and T. N. Davis. The Ndc80 kinetochore complex directly modulates microtubule dynamics. Proc. Natl. Acad. Sci. U.S.A. 109(40):16113-16118, 2012.
42. Volkov, V. A., A. V. Zaytsev, N. Gudimchuk, P. M. Grissom, A. L. Gintsburg, F. I. Ataullakhanov, J. R. McIntosh, and E. L. Grishchuk. Long tethers provide high-force coupling of the Dam1 ring to shortening microtubules. Proc. Natl. Acad. Sci. U.S.A. 110(19):7708-7713, 2013.
43. Wan, X., R. P. O'Quinn, H. L. Pierce, A. P. Joglekar, W. E. Gall, J. G. DeLuca, C. W. Carroll, S. T. Liu, T. J. Yen, B. F. McEwen, P. T. Stukenberg, A. Desai, and E. D. Salmon. Protein architecture of the human kinetochore microtubule attachment site. Cell 137(4):672-684, 2009.
44. Westermann, S., H. W. Wang, A. Avila-Sakar, D. G. Drubin, E. Nogales, and G. Barnes. The Dam1 kinetochore ring complex moves processively on depolymerizing microtubule ends. Nature 440(7083):565-569, 2006.
45. Wilson-Kubalek, E. M., I. M. Cheeseman, C. Yoshioka, A. Desai, and R. A. Milligan. Orientation and structure of the Ndc80 complex on the microtubule lattice. J. Cell Biol. 182(6):1055-1061, 2008.
46. Wollman, R., G. Civelekoglu-Scholey, J. M. Scholey, and A. Mogilner. Reverse engineering of force integration during mitosis in the Drosophila embryo. Mol. Syst. Biol. 4:195, 2008.
47. Zhai, Y., P. J. Kronebusch, and G. G. Borisy. Kinetochore microtubule dynamics and the metaphase-anaphase transition. J. Cell Biol. 131(3):721-734, 1995.
48. Zinkowski, R. P., J. Meyne, and B. R. Brinkley. The centromere- kinetochore complex: a repeat subunit model. J. Cell Biol. 113(5):1091-1110, 1991.