The Ndc80 kinetochore complex forms oligomeric arrays along microtubules

Nature

Volumn 467, Issue 7317, 2010, Pages 805-810

  Alushin, Gregory M ^a   Ramey, Vincent H ^a   Pasqualato, Sebastiano ^b   Ball, David A ^c   Grigorieff, Nikolaus ^d   Musacchio, Andrea ^b,e   Nogales, Eva ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d BRANDEIS UNIVERSITY   (United States)

^e ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; AURORA B KINASE; BETA TUBULIN; DIMER; MONOMER; NDC80 COMPLEX;

CYTOGENETICS; ELECTRON MICROSCOPY; POLYMER; PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CENTROMERE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; MICROTUBULE; MITOSIS; MOLECULAR DOCKING; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE;

BINDING SITES; CRYOELECTRON MICROSCOPY; HUMANS; KINETOCHORES; MICROTUBULES; MITOSIS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; NUCLEAR PROTEINS; PROTEIN CONFORMATION; TUBULIN;

EID: 77957968002     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature09423     Document Type: Article

References (57)

1. Cheeseman, I. M., Chappie, J. S., Wilson-Kubalek, E. M. & Desai, A. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127, 983-997 (2006).
2. Wei, R. R., Al-Bassam, J. & Harrison, S. C. The Ndc80/HEC1 complex is a contact point for kinetochore-microtubule attachment. Nature Struct. Mol. Biol. 14, 54-59 (2007).
3. DeLuca, J. G. et al. Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127, 969-982 (2006).
4. Martin-Lluesma, S., Stucke, V. M. & Nigg, E. A. Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2. Science 297, 2267-2270 (2002).
5. DeLuca, J. G. et al. Nuf2 and Hec1 are required for retention of the checkpoint proteins Mad1 and Mad2 to kinetochores. Curr. Biol. 13, 2103-2109 (2003).
6. Kemmler, S. et al. Mimicking Ndc80 phosphorylation triggers spindle assembly checkpoint signalling. EMBO J. 28, 1099-1110 (2009).
7. Chen, Y., Riley, D. J., Chen, P. L. & Lee, W. H. HEC, A novel nuclear protein rich in leucine heptad repeats specifically involved in mitosis. Mol. Cell. Biol. 17, 6049-6056 (1997).
8. Wigge, P. A. et al. Analysis of the Saccharomyces spindle pole by matrix-assisted laser desorption/ionization (MALDI) mass spectrometry.J. Cell Biol. 141, 967-977 (1998).
9. Wei, R. R., Sorger, P. K. & Harrison, S. C. Molecular organization of the Ndc80 complex, An essential kinetochore component. Proc. Natl Acad. Sci. USA 102, 5363-5367 (2005).
10. Ciferri, C. et al. Architecture of the human ndc80-hec1 complex, A critical constituent of the outer kinetochore. J. Biol. Chem. 280, 29088-29095 (2005).
11. Wei, R. R. et al. Structure of a central component of the yeast kinetochore: the Spc24p/Spc25p globular domain. Structure 14, 1003-1009 (2006).
12. Ciferri, C. et al. Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex. Cell 133, 427-439 (2008).
13. Wang, H. W. et al. Architecture and flexibility of the yeast Ndc80 kinetochore complex. J. Mol. Biol. 383, 894-903 (2008).
14. Hayashi, I., Wilde, A., Mal, T. K. & Ikura, M. Structural basis for the activation of microtubuleassemblybytheEB1andp150Gluedcomplex.Mol. Cell19, 449-460 (2005).
15. Slep, K. C. & Vale, R. D. Structural basis of microtubule plus end tracking by XMAP215, CLIP-170, and EB1. Mol. Cell 27, 976-991 (2007).
16. Guimaraes, G. J., Dong, Y., McEwen, B. F. & Deluca, J. G. Kinetochore-microtubule attachment relies on the disordered N-terminal tail domain of Hec1. Curr. Biol. 18, 1778-1784 (2008).
17. Miller, S.A., Johnson, M.L. & Stukenberg, P.T. Kinetochore attachments require an interaction between unstructured tails on microtubules and Ndc80(Hec1). Curr. Biol. 18, 1785-1791 (2008).
18. Cheeseman, I. M. et al. Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111, 163-172 (2002).
19. Ramey, V. H., Wang, H. W. & Nogales, E. Ab initio reconstruction of helical samples with heterogeneity, Disorder and coexisting symmetries. J. Struct. Biol. 167, 97-105 (2009).
20. Egelman, E. H. The iterative helical real space reconstruction method: surmounting the problems posed by real polymers. J. Struct. Biol. 157, 83-94 (2007).
21. Wilson-Kubalek, E. M., Cheeseman, I. M., Yoshioka, C., Desai, A. & Milligan, R. A. Orientation and structure of the Ndc80 complex on the microtubule lattice. J. Cell Biol. 182, 1055-1061 (2008).
22. Mizuno, N., Narita, A., Kon, T., Sutoh, K. & Kikkawa, M. Three-dimensional structure of cytoplasmic dynein bound to microtubules. Proc. Natl Acad. Sci. USA 104, 20832-20837 (2007).
23. Hoenger, A. & Gross, H. Structural investigations into microtubule-MAP complexes. Methods Cell Biol. 84, 425-444 (2008).
24. Des Georges, A. et al. Mal3, The Schizosaccharomyces pombe homolog of EB1, Changes the microtubule lattice. Nature Struct. Mol. Biol. 15, 1102-1108 (2008).
25. Löwe, J., Li, H., Downing, K. H. & Nogales, E. Refined structure of alpha beta-tubulin at 3.5 A resolution. J. Mol. Biol. 313, 1045-1057 (2001).
26. Wang, H. W. & Nogales, E. Nucleotide-dependent bending flexibility of tubulin regulates microtubule assembly. Nature 435, 911-915 (2005).
27. Wilson, L., Jordan, M. A., Morse, A. & Margolis, R. L. Interaction of vinblastine with steady-state microtubules in vitro. J. Mol. Biol. 159, 125-149 (1982).
28. Joglekar, A. P., Bouck, D. C., Molk, J. N., Bloom, K. S. & Salmon, E. D. Molecular architecture of a kinetochore-microtubule attachment site. Nature Cell Biol. 8, 581-585 (2006).
29. Joglekar, A. P. et al. Molecular architecture of the kinetochore- microtubule attachment site is conserved between point and regional centromeres. J. Cell Biol. 181, 587-594 (2008).
30. Liu, D., Vader, G., Vromans, M. J., Lampson, M. A. & Lens, S. M. Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323, 1350-1353 (2009).
31. 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).
32. Andrews, P.D.et al. AuroraBregulates MCAKatthe mitotic centromere. Dev. Cell6, 253-268 (2004).
33. Santaguida, S. & Musacchio, A. The life and miraclesofkinetochores. EMBO J. 28, 2511-2531 (2009).
34. Maresca, T. J. & Salmon, E. D. Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity. J. Cell Biol. 184, 373-381 (2009).
35. Wan, X. et al. Protein architecture of the human kinetochore microtubule attachment site. Cell 137, 672-684 (2009).
36. Liu, D. et al. Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J. Cell Biol. 188, 809-820 (2010).
37. Hill, T. L. Theoretical problems related to the attachment of microtubules to kinetochores. Proc. Natl Acad. Sci. USA 82, 4404-4408 (1985).
38. Powers, A. F. et al. The Ndc80 kinetochore complex forms load-bearing attachments to dynamic microtubule tips via biased diffusion. Cell 136, 865-875 (2009).
39. Dong, Y., Vanden Beldt, K.J., Meng, X., Khodjakov, A.&McEwen, B.F.The outer plate in vertebrate kinetochores is a flexible network with multiple microtubule interactions. Nature Cell Biol. 9, 516-522 (2007).
40. Lombillo, V. A., Stewart, R. J. & McIntosh, J. R. Minus-end-directed motion of kinesin-coated microspheres driven by microtubule depolymerization. Nature 373, 161-164 (1995).
41. McIntosh, J. R. et al. Fibrils connect microtubule tips with kinetochores: a mechanism to couple tubulin dynamics to chromosome motion. Cell 135, 322-333 (2008).
42. Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199 (1996)
43. Mindell, J.A.&Grigorieff, N. Accurate determinationoflocal defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
44. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
45. Wade, R. H., Chretien, D. & Job, D. Characterization of microtubule protofilament numbers. How does the surface lattice accommodate? J. Mol. Biol. 212, 775-786 (1990)
46. Arnal, I.&Wade, R. H.How does taxol stabilize microtubules? Curr. Biol. 5, 900-908 (1995).
47. Grigorieff, N. FREALIGN: high-resolution refinement of single particle structures. J. Struct. Biol. 157, 117-125 (2007). (Pubitemid 44880784)
48. Sachse, C. et al. High-resolution electron microscopy of helical specimens: a fresh look at tobacco mosaic virus. J. Mol. Biol. 371, 812-835 (2007).
49. Stewart, A. & Grigorieff, N. Noise bias in the refinement of structures derived from single particles. Ultramicroscopy 102, 67-84 (2004).
50. Chen, J. Z. et al. Molecular interactions in rotavirus assembly and uncoating seen by high-resolution cryo-EM. Proc. Natl Acad. Sci. USA 106, 10644-10648 (2009).
51. Goddard, T.D., Huang, C.C.&Ferrin, T.E. Software extensionstoUCSF chimera for interactive visualization of large molecular assemblies. Structure 13, 473-482 (2005).
52. Abramoff, M. D., Magelhaes, P. J. & Ram, S. J. Image Processing with ImageJ. Biophotonics International 11, 36-42 (2004).
53. Amat, F.et al. Markov random field based automatic image alignment for electron tomography. J. Struct. Biol. 161, 260-275 (2008).
54. Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76 (1996).
55. Welch, B. L. The generalisation of student's problems when several different population variances are involved. Biometrika 34, 28-35 (1947).
56. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).
57. Landau, M. et al. Consurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33, W299-302 (2005).