Pivoting of microtubules around the spindle pole accelerates kinetochore capture

Nature Cell Biology

Volumn 15, Issue 1, 2013, Pages 82-87

  Kalinina, Iana ^a,d   Nandi, Amitabha ^b,e   Delivani, Petrina ^a   Chacón, Mariola R ^a   Klemm, Anna H ^a   Ramunno Johnson, Damien ^a   Krull, Alexander ^a   Lindner, Benjamin ^b,d,f   Pavin, Nenad ^a,b,c   Tolić Nørrelykke, Iva M ^a  

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

^b MAX PLANCK INSTITUT FÜR PHYSIK KOMPLEXER SYSTEME   (Germany)

^c UNIVERSITY OF ZAGREB   (Croatia)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^e YALE UNIVERSITY   (United States)

^f BERNSTEIN CENTER FOR COMPUTATIONAL NEUROSCIENCE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE;

ARTICLE; CELLULAR PARAMETERS; CENTROMERE; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; COLD STRESS; CONTROLLED STUDY; CYTOLOGY; KINETOCHORE CAPTURE; METAPHASE; MICROTUBULE; MICROTUBULE ASSEMBLY; MICROTUBULE LENGTH; MICROTUBULE PIVOTING MOTION; MITOSIS; MOLECULAR INTERACTION; NONHUMAN; POLAR MICROTUBULE; PRIORITY JOURNAL; SCHIZOSACCHAROMYCES POMBE; SPINDLE POLE BODY; TEMPERATURE; THEORETICAL MODEL;

ADENOSINE TRIPHOSPHATE; ADENYLYL IMIDODIPHOSPHATE; CHROMOSOMES, FUNGAL; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GREEN FLUORESCENT PROTEINS; KINETICS; KINETOCHORES; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; RECOMBINANT FUSION PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TIME-LAPSE IMAGING;

SCHIZOSACCHAROMYCETACEAE;

EID: 84871716786     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2640     Document Type: Article

References (39)

1. Cheeseman, I. M. & Desai, A. Molecular architecture of the kinetochore-microtubule interface. Nat. Rev. Mol. Cell Biol. 9, 33-46 (2008).
2. Mitchison, T. J. & Kirschner, M. W. Properties of the kinetochore in vitro. II. Microtubule capture and ATP-dependent translocation. J. Cell Biol. 101, 766-777 (1985).
3. Hill, T. L. Theoretical problems related to the attachment of microtubules to kinetochores. Proc. Natl Acad. Sci. USA 82, 4404-4408 (1985).
4. Holy, T. E. & Leibler, S. Dynamic instability of microtubules as an ef-cient way to search in space. Proc. Natl Acad. Sci. USA 91, 5682-5685 (1994).
5. Carazo-Salas, R. E. et al. Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature 400, 178-181 (1999).
6. Wollman, R. et al. Ef-cient chromosome capture requires a bias in the ̀search-andcapture' process during mitotic-spindle assembly. Curr. Biol. 15, 828-832 (2005).
7. Witt, P. L., Ris, H. & Borisy, G. G. Origin of kinetochore microtubules in Chinese hamster ovary cells. Chromosoma 81, 483-505 (1980).
8. Kitamura, E. et al. Kinetochores generate microtubules with distal plus ends: their roles and limited lifetime in mitosis. Dev. Cell 18, 248-259 (2010).
9. Paul, R. et al. Computer simulations predict that chromosome movements and rotations accelerate mitotic spindle assembly without compromising accuracy. Proc. Natl Acad. Sci. USA 106, 15708-15713 (2009).
10. Burbank, K. S., Groen, A. C., Perlman, Z. E., Fisher, D. S. & Mitchison, T. J. A new method reveals microtubule minus ends throughout the meiotic spindle. J. Cell Biol. 175, 369-375 (2006).
11. Mahoney, N. M., Goshima, G., Douglass, A. D. & Vale, R. D. Making microtubules and mitotic spindles in cells without functional centrosomes. Curr. Biol. 16, 564-569 (2006).
12. Mogilner, A. & Craig, E. Towards a quantitative understanding of mitotic spindle assembly and mechanics. J. Cell Sci. 123, 3435-3445 (2010).
13. O'Connell, C. B. & Khodjakov, A. L. Cooperative mechanisms of mitotic spindle formation. J. Cell Sci. 120, 1717-1722 (2007).
14. Duncan, T. & Wakefield, J. G. 50 ways to build a spindle: the complexity of microtubule generation during mitosis. Chromosome Res. 19, 321-333 (2011).
15. Funabiki, H., Hagan, I., Uzawa, S. & Yanagida, M. Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J. Cell Biol. 121, 961-976 (1993).
16. Sagolla, M. J., Uzawa, S. & Cande, W. Z. Individual microtubule dynamics contribute to the function of mitotic and cytoplasmic arrays in fission yeast. J. Cell Sci. 116, 4891-4903 (2003).
17. Zimmerman, S., Daga, R. R. & Chang, F. Intra-nuclear microtubules and a mitotic spindle orientation checkpoint. Nat. Cell Biol. 6, 1245-1246 (2004).
18. Gachet, Y. et al. Sister kinetochore recapture in fission yeast occurs by two distinct mechanisms, both requiring Dam1 and Klp2. Mol. Biol. Cell 19, 1646-1662 (2008).
19. Grishchuk, E. L. & McIntosh, J. R. Microtubule depolymerization can drive poleward chromosome motion in fission yeast. EMBO J. 25, 4888-4896 (2006).
20. Tanaka, K. et al. Molecular mechanisms of kinetochore capture by spindle microtubules. Nature 434, 987-994 (2005).
21. Beinhauer, J. D., Hagan, I. M., Hegemann, J. H. & Fleig, U. Mal3, the fission yeast homologue of the human APC-interacting protein EB-1 is required for microtubule integrity and the maintenance of cell form. J. Cell Biol. 139, 717-728 (1997).
22. Busch, K. E. & Brunner, D. The microtubule plus end-tracking proteins mal3p and tip1p cooperate for cell-end targeting of interphase microtubules. Curr. Biol. 14, 548-559 (2004).
23. Berg, H. C. Random Walks in Biology (Princeton Univ. Press, 1993).
24. Masuda, H., Hirano, T., Yanagida, M. & Cande, W. Z. In vitro reactivation of spindle elongation in fission yeast nuc2 mutant cells. J. Cell Biol. 110, 417-425 (1990).
25. Lee, G. M. Characterization of mitotic motors by their relative sensitivity to AMP-PNP. J. Cell Sci. 94, 425-441 (1989).
26. Broersma, S. Rotational diffusion constant of a cylindrical particle. J. Chem. Phys. 32, 1626-1631 (1960).
27. Hunt, A. J., Gittes, F. & Howard, J. The force exerted by a single kinesin molecule against a viscous load. Biophys. J. 67, 766-781 (1994).
28. Tirado, M. M. & de la Torre, J. G. Translational friction coef-cients of rigid, symmetric top macromolecules. Application to circular cylinders. J. Chem. Phys. 71, 2581-2587 (1979).
29. Drummond, D. R. & Cross, R. A. Dynamics of interphase microtubules in Schizosaccharomyces pombe. Curr. Biol. 10, 766-775 (2000).
30. Vogel, S. K., Raabe, I., Dereli, A., Maghelli, N. & Tolic-Norrelykke, I. Interphase microtubules determine the initial alignment of the mitotic spindle. Curr. Biol. 17, 438-444 (2007).
31. Gehlen, L. R. et al. Nuclear geometry and rapid mitosis ensure asymmetric episome segregation in yeast. Curr. Biol. 21, 25-33 (2011).
32. Shav-Tal, Y. et al. Dynamics of single mRNPs in nuclei of living cells. Science 304, 1797-1800 (2004).
33. Gopalakrishnan, M. & Govindan, B. S. A-rst-passage-time theory for search and capture of chromosomes by microtubules in mitosis. Bull. Math. Biol. 73, 2483-2506 (2011).
34. Ding, R., McDonald, K. L. & McIntosh, J. R. Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J. Cell Biol. 120, 141-151 (1993).
35. Neumann, F. R. & Nurse, P. Nuclear size control in fission yeast. J. Cell Biol. 179, 593-600 (2007).
36. Bahler, J. et al. Heterologous modules for ef-cient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951 (1998).
37. Penkett, C. J., Birtle, Z. E. & Bahler, J. Simplified primer design for PCR-based gene targeting and microarray primer database: two web tools for fission yeast. Yeast 23, 921-928 (2006).
38. Forsburg, S. L. & Rhind, N. Basic methods for fission yeast. Yeast 23, 173-183 (2006).
39. Russell, P. & Nurse, P. cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell 45, 145-153 (1986).