Conserved and divergent features of kinetochores and spindle microtubule ends from five species

Journal of Cell Biology

Volumn 200, Issue 4, 2013, Pages 459-474

  Richard McIntosh, J ^a   O'Toole, Eileen ^a   Zhudenkov, Kirill ^b   Morphew, Mary ^a   Schwartz, Cindi ^a   Ataullakhanov, Fazly I ^b,c,d   Grishchuk, Ekaterina L ^e  

^a UNIVERSITY OF COLORADO   (United States)

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

^c Federal Research and Clinical Center of Pediatric Hematology   (Russian Federation)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE; ARTICLE; CELL STRUCTURE; CENTROMERE; FIBER; IN VITRO STUDY; METAPHASE; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; SPINDLE CELL; YEAST;

ANAPHASE; ANIMALS; CAENORHABDITIS ELEGANS; CATTLE; CELL LINE; CHLAMYDOMONAS REINHARDTII; CHROMOSOMES; ELECTRON MICROSCOPE TOMOGRAPHY; KINETOCHORES; MICROTUBULES; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES; SPECIES SPECIFICITY;

EID: 84874366606     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201209154     Document Type: Article

References (62)

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. 2010. Tension directly stabilizes reconstituted kinetochoremicrotubule attachments. Nature. 468:576-579. http://dx.doi.org/10.1038/nature09594
2. Albertson, D.G., and J.N. Thomson. 1982. The kinetochores of Caenorhabditis elegans. Chromosoma. 86:409-428. http://dx.doi.org/10.1007/BF00292267
3. Alushin, G.M., V.H. Ramey, S. Pasqualato, D.A. Ball, N. Grigorieff, A. Musacchio, and E. Nogales. 2010. The Ndc80 kinetochore complex forms oligomeric arrays along microtubules. Nature. 467:805-810. http://dx.doi.org/10.1038/nature09423
4. Austin, J.R. II, J.M. Seguí-Simarro, and L.A. Staehelin. 2005. Quantitative analysis of changes in spatial distribution and plus-end geometry of microtubules involved in plant-cell cytokinesis. J. Cell Sci. 118:3895-3903. http://dx.doi.org/10.1242/jcs.02512
5. Bajer, A.S., and J. Mole-Bajer. 1972. Spindle dynamics and chromosome movements. International Review of Cytology, Supplement 3. Academic Press, New York. 271 pp.
6. Cheeseman, I.M., S. Niessen, S. Anderson, F. Hyndman, J.R. Yates III, K. Oegema, and A. Desai. 2004. A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev. 18:2255-2268. http://dx.doi.org/10.1101/gad.1234104
7. Cheng, L., J. Zhang, S. Ahmad, L. Rozier, H. Yu, H. Deng, and Y. Mao. 2011. Aurora B regulates formin mDia3 in achieving metaphase chromosome alignment. Dev. Cell. 20:342-352. http://dx.doi.org/10.1016/j.devcel.2011.01.008
8. Chrétien, D., S.D. Fuller, and E. Karsenti. 1995. Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates. J. Cell Biol. 129:1311-1328. http://dx.doi.org/10.1083/jcb.129.5.1311
9. DeLuca, J.G., and A. Musacchio. 2012. Structural organization of the kinetochore- microtubule interface. Curr. Opin. Cell Biol. 24:48-56. http://dx.doi.org/10.1016/j.ceb.2011.11.003
10. Ding, R., K.L. McDonald, and J.R. McIntosh. 1993. Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J. Cell Biol. 120:141-151. http://dx.doi.org/10.1083/jcb.120.1.141
11. Ding, R., R.R. West, D.M. Morphew, B.R. Oakley, and J.R. McIntosh. 1997. The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds. Mol. Biol. Cell. 8: 1461-1479.
12. Dong, Y., K.J. Vanden Beldt, X. Meng, A. Khodjakov, and B.F. McEwen. 2007. The outer plate in vertebrate kinetochores is a flexible network with multiple microtubule interactions. Nat. Cell Biol. 9:516-522. http://dx.doi.org/10.1038/ncb1576
13. Dumont, S., E.D. Salmon, and T.J. Mitchison. 2012. Deformations within moving kinetochores reveal different sites of active and passive force generation. Science. 337:355-358. http://dx.doi.org/10.1126/science.1221886
14. Gonen, S., B. Akiyoshi, M.G. Iadanza, D. Shi, N. Duggan, S. Biggins, and T. Gonen. 2012. The structure of purified kinetochores reveals multiple microtubule-attachment sites. Nat. Struct. Mol. Biol. 19:925-929. http://dx.doi.org/10.1038/nsmb.2358
15. Grishchuk, E.L., and J.R. McIntosh. 2006. Microtubule depolymerization can drive poleward chromosome motion in fission yeast. EMBO J. 25:4888- 4896. http://dx.doi.org/10.1038/sj.emboj.7601353
16. Grishchuk, E.L., I.S. Spiridonov, and J.R. McIntosh. 2007. Mitotic chromosome biorientation in fission yeast is enhanced by dynein and a minus-enddirected, kinesin-like protein. Mol. Biol. Cell. 18:2216-2225. http://dx.doi.org/10.1091/mbc.E06-11-0987
17. Grishchuk, E.L., A.K. Efremov, V.A. Volkov, I.S. Spiridonov, N. Gudimchuk, S. Westermann, D. Drubin, G. Barnes, J.R. McIntosh, and F.I. Ataullakhanov. 2008. The Dam1 ring binds microtubules strongly enough to be a processive as well as energy-efficient coupler for chromosome motion. Proc. Natl. Acad. Sci. USA. 195:15423-15428. http://dx.doi.org/10.1073/pnas.0807859105
18. Heumann, J.M., A. Hoenger, and D.N. Mastronarde. 2011. Clustering and variance maps for cryo-electron tomography using wedge-masked differences. J. Struct. Biol. 175:288-299. http://dx.doi.org/10.1016/j.jsb.2011.05.011
19. Höög, J.L., S.M. Huisman, Z. Sebö-Lemke, L. Sandblad, J.R. McIntosh, C. Antony, and D. Brunner. 2011. Electron tomography reveals a flared morphology on growing microtubule ends. J. Cell Sci. 124:693-698. http://dx.doi.org/10.1242/jcs.072967
20. Howell, B.J., B.F. McEwen, J.C. Canman, D.B. Hoffman, E.M. Farrar, C.L. Rieder, and E.D. Salmon. 2001. Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J. Cell Biol. 155:1159-1172. http://dx.doi.org/10.1083/jcb.200105093
21. Jackson, W.T., and B.G. Doyle. 1982. Membrane distribution in dividing endosperm cells of Haemanthus. J. Cell Biol. 94:637-643. http://dx.doi.org/10.1083/jcb.94.3.637
22. Jiang, K., and A. Akhmanova. 2011. Microtubule tip-interacting proteins: a view from both ends. Curr. Opin. Cell Biol. 23:94-101. http://dx.doi.org/10.1016/j.ceb.2010.08.008
23. Joglekar, A.P., D. Bouck, K. Finley, X. Liu, Y. Wan, J. Berman, X. He, E.D. Salmon, and K.S. Bloom. 2008. Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J. Cell Biol. 181:587-594. http://dx.doi.org/10.1083/jcb.200803027
24. Kremer, J.R., D.N. Mastronarde, and J.R. McIntosh. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116:71-76. http://dx.doi.org/10.1006/jsbi.1996.0013
25. Kubai, D.F. 1973. Unorthodox mitosis in Trichonympha agilis: kinetochore differentiation and chromosome movement. J. Cell Sci. 13:511-552.
26. Kubai, D.F. 1975. The evolution of the mitotic spindle. Int. Rev. Cytol. 43:167-227. http://dx.doi.org/10.1016/S0074-7696(08)60069-8
27. Laan, L., N. Pavin, J. Husson, G. Romet-Lemonne, M. van Duijn, M.P. López, R.D. Vale, F. Jülicher, S.L. Reck-Peterson, and M. Dogterom. 2012. Cortical dynein controls microtubule dynamics to generate pulling forces that position microtubule asters. Cell. 148:502-514. http://dx.doi.org/10.1016/j.cell.2012.01.007
28. Liu, X., I. McLeod, S. Anderson, J.R. Yates III, and X. He. 2005. Molecular analysis of kinetochore architecture in fission yeast. EMBO J. 24:2919-2930. http://dx.doi.org/10.1038/sj.emboj.7600762
29. Maddox, P.S., K.S. Bloom, and E.D. Salmon. 2000. The polarity and dynamics of microtubule assembly in the budding yeast Saccharomyces cerevisiae. Nat. Cell Biol. 2:36-41. http://dx.doi.org/10.1038/71357
30. Maiato, H., P.J. Hergert, S. Moutinho-Pereira, Y. Dong, K.J. Vandenbeldt, C.L. Rieder, and B.F. McEwen. 2006. The ultrastructure of the kinetochore and kinetochore fiber in Drosophila somatic cells. Chromosoma. 115:469-480. http://dx.doi.org/10.1007/s00412-006-0076-2
31. Mandelkow, E.M., E. Mandelkow, and R.A. Milligan. 1991. Microtubule dynamics and microtubule caps: a time-resolved cryo-electron microscopy study. J. Cell Biol. 114:977-991. http://dx.doi.org/10.1083/jcb.114.5.977
32. Mastronarde, D.N. 2005. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152:36-51. http://dx.doi.org/10.1016/j.jsb.2005.07.007
33. McEwen, B.F., Y. Ding, and A.B. Heagle. 1998a. Relevance of kinetochore size and microtubule-binding capacity for stable chromosome attachment during mitosis in PtK1 cells. Chromosome Res. 6:123-132. http://dx.doi.org/10.1023/A:1009239013215
34. McEwen, B.F., C.E. Hsieh, A.L. Mattheyses, and C.L. Rieder. 1998b. A new look at kinetochore structure in vertebrate somatic cells using high-pressure freezing and freeze substitution. Chromosoma. 197:366-375. http://dx.doi.org/10.1007/s004120050320
35. McIntosh, J.R. 2007. Cellular Electron Microscopy. In Methods in Cell Biology. Vol. 79. L. Wilson and P. Matsudaira, editors. Academic Press, San Diego. xxi-xxv.
36. L. Wilson and P. Matsudaira, editors. Academic Press, San Diego. xxi-xxv.
37. 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. 2008. Fibrils connect microtubule tips with kinetochores: a mechanism to couple tubulin dynamics to chromosome motion. Cell. 135:322-333. http://dx.doi.org/10.1016/j.cell.2008.08.038
38. McIntosh, J.R., V. Volkov, F.I. Ataullakhanov, and E.L. Grishchuk. 2010. Tubulin depolymerization may be an ancient biological motor. J. Cell Sci. 123:3425-3434. http://dx.doi.org/10.1242/jcs.067611
39. Miranda, J.J., P. De Wulf, P.K. Sorger, and S.C. Harrison. 2005. The yeast DASH complex forms closed rings on microtubules. Nat. Struct. Mol. Biol. 12:138-143. http://dx.doi.org/10.1038/nsmb896
40. Mitchison, T.J. 1989. Polewards microtubule flux in the mitotic spindle: evidence from photoactivation of fluorescence. J. Cell Biol. 199:637-652. http://dx.doi.org/10.1083/jcb.109.2.637
41. Morphew, M., W. He, P.J. Bjorkman, and J.R. McIntosh. 2008. Silver enhancement of Nanogold particles during freeze substitution for electron microscopy. J. Microsc. 230:263-267. http://dx.doi.org/10.1111/j.1365-2818.2008.01983.x
42. Müller-Reichert, T., J. Mäntler, M. Srayko, and E. O'Toole. 2008. Electron microscopy of the early Caenorhabditis elegans embryo. J. Microsc. 230:297-307. http://dx.doi.org/10.1111/j.1365-2818.2008.01985.x
43. Nishino, T., K. Takeuchi, K.E. Gascoigne, A. Suzuki, T. Hori, T. Oyama, K. Morikawa, I.M. Cheeseman, and T. Fukagawa. 2012. CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold. Cell. 148:487-501. http://dx.doi.org/10.1016/j.cell.2011.11.061
44. O'Toole, E.T., M. Winey, J.R. McIntosh, and D.N. Mastronarde. 2002. Electron tomography of yeast cells. Methods Enzymol. 351:81-95. http://dx.doi.org/10.1016/S0076-6879(02)51842-5
45. O'Toole, E.T., T.H. Giddings, J.R. McIntosh, and S.K. Dutcher. 2003. Threedimensional organization of basal bodies from wild-type and deltatubulin deletion strains of Chlamydomonas reinhardtii. Mol. Biol. Cell. 14:2999-3012. http://dx.doi.org/10.1091/mbc.E02-11-0755
46. Pidoux, A.L., and R.C. Allshire. 2000. Centromeres: getting a grip of chromosomes. Curr. Opin. Cell Biol. 12:308-319. http://dx.doi.org/10.1016/S0955-0674(00)00094-6
47. Preble, A.M., T.H. Giddings Jr., and S.K. Dutcher. 2001. Extragenic bypass suppressors of mutations in the essential gene BLD2 promote assembly of basal bodies with abnormal microtubules in Chlamydomonas reinhardtii. Genetics. 157:163-181.
48. Rieder, C.L. 1982. The formation, structure, and composition of the mammalian kinetochore and kinetochore fiber. Int. Rev. Cytol. 79:1-58. http://dx.doi.org/10.1016/S0074-7696(08)61672-1
49. Rogers, G.C., S.L. Rogers, T.A. Schwimmer, S.C. Ems-McClung, C.E. Walczak, R.D. Vale, J.M. Scholey, and D.J. Sharp. 2004. Two mitotic kinesins cooperate to drive sister chromatid separation during anaphase. Nature. 427:364-370. http://dx.doi.org/10.1038/nature02256
50. Sanchez-Perez, I., S.J. Renwick, K. Crawley, I. Karig, V. Buck, J.C. Meadows, A. Franco-Sanchez, U. Fleig, T. Toda, and J.B. Millar. 2005. The DASH complex and Klp5/Klp6 kinesin coordinate bipolar chromosome attachment in fission yeast. EMBO J. 24:2931-2943. http://dx.doi.org/10.1038/sj.emboj.7600761
51. Schittenhelm, R.B., S. Heeger, F. Althoff, A. Walter, S. Heidmann, K. Mechtler, and C.F. Lehner. 2007. Spatial organization of a ubiquitous eukaryotic kinetochore protein network in Drosophila chromosomes. Chromosoma. 116:385-402. http://dx.doi.org/10.1007/s00412-007-0103-y
52. 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, et al. 2012. The kinetochore-bound Ska1 complex tracks depolymerizing microtubules and binds to curved protofilaments. Dev. Cell. 23:968-980. http://dx.doi.org/10.1016/j.devcel.2012.09.012
53. Tanaka, K., E. Kitamura, Y. Kitamura, and T.U. Tanaka. 2007. Molecular mechanisms of microtubule-dependent kinetochore transport toward spindle poles. J. Cell Biol. 178:269-281. http://dx.doi.org/10.1083/jcb.200702141
54. Umen, J.G., and U.W. Goodenough. 2001. Control of cell division by a retinoblastoma protein homolog in Chlamydomonas. Genes Dev. 15:1652-1661. http://dx.doi.org/10.1101/gad.892101
55. VandenBeldt, K.J., R.M. Barnard, P.J. Hergert, X. Meng, H. Maiato, and B.F. McEwen. 2006. Kinetochores use a novel mechanism for coordinating the dynamics of individual microtubules. Curr. Biol. 16:1217-1223. http://dx.doi.org/10.1016/j.cub.2006.04.046
56. 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, et al. 2009. Protein architecture of the human kinetochore microtubule attachment site. Cell. 137:672-684. http://dx.doi.org/10.1016/j.cell.2009.03.035
57. Wang, H.-W., V.H. Ramey, S. Westermann, A.E. Leschziner, J.P.I. Welburn, Y. Nakajima, D.G. Drubin, G. Barnes, and E. Nogales. 2007. Architecture of the Dam1 kinetochore ring complex and implications for microtubuledriven assembly and force-coupling mechanisms. Nat. Struct. Mol. Biol. 14:721-726. http://dx.doi.org/10.1038/nsmb1274
58. Welburn, J.P., and I.M. Cheeseman. 2008. Toward a molecular structure of the eukaryotic kinetochore. Dev. Cell. 15:645-655. http://dx.doi.org/10.1016/j.devcel.2008.10.011
59. Westermann, S., A. Avila-Sakar, H.W. Wang, H. Niederstrasser, J. Wong, D.G. Drubin, E. Nogales, and G. Barnes. 2005. Formation of a dynamic kinetochore-microtubule interface through assembly of the Dam1 ring complex. Mol. Cell. 17:277-290. http://dx.doi.org/10.1016/j.molcel.2004.12.019
60. Westermann, S., D.G. Drubin, and G. Barnes. 2007. Structures and functions of yeast kinetochore complexes. Annu. Rev. Biochem. 76:563-591. http://dx.doi.org/10.1146/annurev.biochem.76.052705.160607
61. Winey, M., G.P. Morgan, P.D. Straight, T.H. Giddings Jr., and D.N. Mastronarde. 2005. Three-dimensional ultrastructure of Saccharomyces cerevisiae meiotic spindles. Mol. Biol. Cell. 16:1178-1188. http://dx.doi.org/10.1091/mbc.E04-09-0765
62. Yeh, E., C. Yang, E. Chin, P. Maddox, E.D. Salmon, D.J. Lew, and K. Bloom. 2000. Dynamic positioning of mitotic spindles in yeast: role of microtubule motors and cortical determinants. Mol. Biol. Cell. 11:3949-3961.