Dynamics of inner kinetochore assembly and maintenance in living cells

Journal of Cell Biology

Volumn 180, Issue 6, 2008, Pages 1101-1114

  Hemmerich, Peter ^a   Weidtkamp Peters, Stefanie ^a,b   Hoischen, Christian ^a   Schmiedeberg, Lars ^a,c   Erliandri, Indri ^a   Diekmann, Stephan ^a  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; CENTROMERE PROTEIN B; CENTROMERE PROTEIN C; CENTROMERE PROTEIN H; CENTROMERE PROTEIN I; GREEN FLUORESCENT PROTEIN; NUCLEAR PROTEIN; PROTEIN HMIS12; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CENTROMERE; CHROMATIN; CONTROLLED STUDY; GENE REPLICATION; HUMAN; HUMAN CELL; MICROSCOPY; MITOSIS; PLASTICITY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN IMMOBILIZATION; PROTEIN STABILITY; QUANTITATIVE ANALYSIS;

AUTOANTIGENS; BINDING SITES; CELL CYCLE; CELL DIVISION; CELL LINE; CENTROMERE; CENTROMERE PROTEIN B; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; DNA REPLICATION; DNA-BINDING PROTEINS; G1 PHASE; HUMANS; KINETOCHORES; MICROTUBULE-ASSOCIATED PROTEINS; MITOTIC SPINDLE APPARATUS; PROTEIN BINDING; S PHASE;

EID: 41549127153     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200710052     Document Type: Article

References (87)

1. Alonso, A., B. Fritz, D. Hasson, G. Abrusan, F. Cheung, K. Yoda, B. Radlwimmer, A.G. Ladurner, and P.E. Warburton. 2007. Co-localization of CENP-C and CENP-H to discontinuous domains of CENP-A chromatin at human neocentromeres. Genome Biol. 8:R148.
2. Amor, D.J., P. Kalitsis, H. Sumer, and K.H.A. Choo. 2004. Building the centromere: from foundation proteins to 3D organisation. Trends Cell Biol. 14:359-368.
3. Ando, S., H. Yang, N. Nozaki, T. Okazaki, and K. Yoda. 2002. CENP-A, CENP-B and CENP-C chromatin complex that contains the I-type alpha-satellite array constitutes the prekinetochore in HeLa cells. Mol. Cell. Biol. 22:2229-2241.
4. Banks, D.S., and C. Fradin. 2005. Anomalous diffusion of proteins due to molecular crowding. Biophys. J. 89:2960-2971.
5. Beaudouin, J., F. Mora-Bermudez, T. Klee, N. Daigle, and J. Ellenberg. 2006. Dissecting the contribution of diffusion and interactions to the mobility of nuclear proteins. Biophys. J. 90:1878-1894.
6. Belmont, A. 2003. Dynamics of chromatin, proteins, and bodies within the cell nucleus. Curr. Opin. Cell Biol. 15:304-310.
7. Bloom, K. 2007. Centromere dynamics. Curr. Opin. Genet. Dev. 17:151-156.
8. Bulinski, J.C., D.J. Odde, B.J. Howell, T.D. Salmon, and C.M. Waterman-Storer. 2001. Rapid dynamics of the microtubule binding of ensconsin in vivo. J. Cell Sci. 114:3885-3897.
9. Carroll, C.W., and A.F. Straight. 2006. Centromere formation: from epigenetics to self-assembly. Trends Cell Biol. 16:70-78.
10. Chan, G.K., S.T. Liu, and T.J. Yen. 2005. Kinetochore structure and function. Trends Cell Biol. 15:589-598.
11. 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.
12. Chen, D., M. Dundr, C. Wang, A. Leung, A. Lamond, T. Misteli, and S. Huang. 2005. Condensed mitotic chromatin is accessible to transcription factors and chromatin structural proteins. J. Cell Biol. 168:41-54.
13. Cimini, D., and F. Degrassi. 2005. Aneuploidy: a matter of bad connections. Trends Cell Biol. 15:442-451.
14. Cleveland, D.W., Y. Mao, and K.F. Sullivan. 2003. Centromeres and kinetochores: from epigentics to mitotic checkpoint signaling. Cell. 112:407-421.
15. Dalal, Y., T. Furuyama, D. Vermaak, and S. Henikoff. 2007. Structure, dynamics, and evolution of centromeric nucleosomes. Proc. Natl. Acad. Sci. USA. 104:15974-15981.
16. Dawe, R.K., and S. Henikoff. 2006. Centromeres put epigenetics in the driver' s seat. Trends Biochem. Sci. 31:662-669.
17. Dunleavy, E., A. Pidoux, and R. Allshire. 2005. Centromeric chromatin makes its mark. Trends Biochem. Sci. 30:172-175.
18. Faragher, A.J., X.M. Sun, M. Butterworth, N. Harper, M. Mulheran, S. Ruchaud, W.C. Earnshaw, and G.M. Cohen. 2007. Death receptor-induced apoptosis reveals a novel interplay between the chromosomal passenger complex and CENP-C during interphase. Mol. Biol. Cell. 18:1337-1347.
19. Foltz, D.R., L.E.T. Jansen, B.E. Black, A.O. Bailey, J.R.I.I.I. Yates, and D.W. Cleveland. 2006. The human CENP-A centromeric complex. Nat. Cell Biol. 8:458-469.
20. Fujita, Y., T. Hayashi, T. Kiyomitsu, Y. Toyoda, A. Kokubu, C. Obuse, and M. Yanagida. 2007. Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev. Cell. 12:17-30.
21. Fukagawa, T. 2004. Assembly of kinetochores in vertebrate cells. Exp. Cell Res. 296:21-27.
22. Fukagawa, T., Y. Mikami, A. Nishihashi, V. Regnier, T. Haraguchi, Y. Hiraoka, N. Sugata, K. Todokoro, W. Brown, and T. Ikemura. 2001. CENP-H, a constitutive centromere component, is required for centromere targeting of CENP-C in vertebrate cells. EMBO J. 20:4603-4617.
23. Gerlich, D., B. Koch, F. Dupeux, J.M. Peters, and J. Ellenberg. 2006. Live-cell imaging reveals a stable cohesin-chromatin interaction after but not before DNA replication. Curr. Biol. 16:1571-1578.
24. Goldberg, A.D., C.D. Allis, and E. Bernstein. 2007. Epigenetics: A landscape takes shape. Cell. 128:635-638.
25. Goshima, G., T. Kiyomitsu, K. Yoda, and M. Yanagida. 2003. Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J. Cell Biol. 160:25-39.
26. Hager, G.L., C. Elbi, and M. Becker. 2002. Protein dynamics in the nuclear compartment. Curr. Opin. Genet. Dev. 12:137-141.
27. Hancock, R. 2004. A role for macromolecular crowding effects in the assembly and function of compartments in the nucleus. J. Struct. Biol. 146:281-290.
28. Hori, T., T. Haraguchi, Y. Hiraoka, H. Kimura, and T. Fukagawa. 2003. Dynamic behavior of Nuf2-Hec1 complex that localizes to the centrosome and centromere and is essential for mitotic progression in vertebrate cells. J. Cell Sci. 116:3347-3362.
29. Houtsmuller, A.B., S. Rademakers, A.L. Nigg, D. Hoogstraten, J.H. Hoeijmakers, and W. Vermeulen. 1999. Action of DNA repair endonuclease ERCC1/ XPF in living cells. Science. 284:958-961.
30. Howell, B.J., B. Moree, E.M. Farrar, S. Stewart, G. Fang, and E.D. Salmon. 2004. Spindle checkpoint protein dynamics at kinetochores in living cells. Curr. Biol. 14:953-964.
31. Howman, E.V., K.J. Fowler, A.J. Newson, S. Redward, A.C. MacDonald, P. Kalitsis, and K.H.A. Choo. 2000. Early disruption of centromeric chromatin organisation in centromere protein A (CENP-A) null mice. Proc. Natl. Acad. Sci. USA. 97:1148-1153.
32. Hudson, D.F., K.J. Fowler, E. Earle, R. Saffery, P. Kalitsis, H. Trowell, J. Hill, N.G. Wreford, D.M. de Kretser, M.R. Cancilla, et al. 1998. Centromere protein B null mice are mitotically and meiotically normal but have lower body and testis weights. J. Cell Biol. 141:309-319.
33. Izuta, H., M. Ikeno, N. Suzuki, T. Tomonaga, N. Nozaki, C. Obuse, Y. Kisu, N. Goshima, F. Nomura, N. Nomura, and K. Yoda. 2006. Comprehensive analysis of the ICEN (interphase centromere complex) components enriched in the CENP-A chromatin of human cells. Genes Cells. 11: 673-684.
34. Jansen, L.E., B.E. Black, D.R. Foltz, and D.W. Cleveland. 2007. Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176: 795-805.
35. Joglekar, A.P., D.C. Bouck, J.N. Molk, K.S. Bloom, and E.D. Salmon. 2006. Molecular architecture of a kinetochore-microtubule attachment site. Nat. Cell Biol. 8:581-585.
36. Kallio, M.J., V.A. Beardmore, J. Weinstein, and G.J. Gorbsky. 2002. Rapid microtubule-independent dynamics of Cdc20 at kinetochores and centrosomes in mammalian cells. J. Cell Biol. 158:841-847.
37. Kimura, H., and P.R. Cook. 2001. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J. Cell Biol. 153:1341-1353.
38. Kline, S.L., I.M. Cheeseman, T. Hori, T. Fukagawa, and A. Desai. 2006. The human Mis12 complex is required for kinetochore assembly and proper chromosome segregation. J. Cell Biol. 173:9-17.
39. Kops, G.J., B.A. Weaver, and D.W. Cleveland. 2005. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer. 5:773-785.
40. Kwon, M.S., T. Hori, M. Okada, and T. Fukagawa. 2007. CENP-C is involved in chromosome segregation, mitotic checkpoint function, and kinetochore assembly. Mol. Biol. Cell. 18:2155-2168.
41. Lermontova, I., V. Schubert, J. Fuchs, S. Klatte, J. Macas, and I. Schubert. 2006. Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell. 18:2443-2451.
42. Liu, S.T., J.C. Hittle, S.A. Jablonski, M.S. Campbell, K. Yoda, and T.J. Yen. 2003. Human CENP-I specifies localisation of CENP-F, Mad1 and Mad2 to kinetochores and is essential for mitosis. Nat. Cell Biol. 5:341-345.
43. Liu, S.T., J.B. Rattner, S.A. Jablonski, and T.J. Yen. 2006. Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J. Cell Biol. 175:41-53.
44. Loyola, A., and G. Almouzni. 2007. Marking histone H3 variants: How, when and why? Trends Biochem. Sci. 32:425-433.
45. Maddox, P.S., F. Hyndman, J. Monen, K. Oegema, and A. Desai. 2007. Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. J. Cell Biol. 176:757-763.
46. Masumoto, H., H. Masukata, Y. Muro, N. Nozaki, and T. Okazaki. 1989. A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite. J. Cell Biol. 109: 1963-1973.
47. Misteli, T. 2001a. Protein dynamics: implications for nuclear architecture and gene expression. Science. 291:843-847.
48. Misteli, T. 2001b. The concept of self-organization in cellular architecture. J. Cell Biol. 155:181-185.
49. Morency, E., M. Sabra, F. Catez, P. Texier, and P. Lomonte. 2007. A novel cell response triggered by interphase centromere structural instability. J. Cell Biol. 177:757-768.
50. Morris, C.A., and D. Moazed. 2007. Centromere assembly and propagation. Cell. 128:647-650.
51. Nishihashi, A., T. Haraguchi, Y. Hiraoka, T. Ikemura, V. Regnier, H. Dodson, W.C. Earnshaw, and T. Fukagawa. 2002. CENP-I is essential for centromere function in vertebrate cells. Dev. Cell. 2:463-476.
52. Ochs, R.L., and R.I. Press. 1992. Centromere autoantigens are associated with the nucleolus. Exp. Cell Res. 200:339-350.
53. Ohzeki, J., M. Nakano, T. Okada, and H. Masumoto. 2002. CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J. Cell Biol. 159:765-775.
54. Okada, M., I.M. Cheeseman, T. Hori, K. Okawa, I.X. McLeod Jr., I.I.I. Yates, A. Desai, and T. Fukagawa. 2006. The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat. Cell Biol. 8:446-457.
55. Orthaus, A., C. Biskup, B. Hoffmann, C. Hoischen, S. Ohndorf, K. Benndorf, and S. Diekmann. 2007. Assembly of the inner kinetochore proteins CENP-A and CENP-B in living human cells. Chembiochem. 9:77-92.
56. Palmer, D.K., K. O' Day, H.L. Trong, H. Charbonneau, and R.L. Margolis. 1991. Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone. Proc. Natl. Acad. Sci. USA. 88: 3734-3738.
57. Phair, R.D., P. Scaffidi, C. Elbi, J. Vecerova, A. Dey, K. Ozato, D.T. Brown, G. Hager, M. Bustin, and T. Misteli. 2004. Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol. Cell. Biol. 24:6393-6402.
58. Pluta, A.F., and W.C. Earnshaw. 1996. Specific interaction between human kinetochore protein CENP-C and a nucleolar transcriptional regulator. J. Biol. Chem. 271:18767-18774.
59. Politi, V., G. Perini, S. Trazzi, A. Pliss, I. Raska, W.C. Earnshaw, and G. Della Valle. 2002. CENP-C binds the alpha-satellite DNA in vivo at specific centromere domains. J. Cell Sci. 115:2317-2327.
60. Rabut, G., V. Doye, and J. Ellenberg. 2004. Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat. Cell Biol. 6:1114-1121.
61. Régnier, V., P. Vagnarelli, T. Fukagawa, T. Zerjal, E. Burns, D. Trouche, W. Earnshaw, and W. Brown. 2005. CENP-A is required for accurate chromosome segregation and sustained kinetochore association of BubR1. Mol. Cell. Biol. 25:3967-3981.
62. Saffery, R., D.V. Irvine, B. Griffiths, P. Kalitsis, L. Wordeman, and K.H. Choo. 2000. Human centromeres and neocentromeres show identical distribution patterns of >20 functionally important kinetochore-associated proteins. Hum. Mol. Genet. 9:175-185.
63. Saxton, M.J. 2001. Anomalous subdiffusion in fluorescence photobleaching recovery: a Monte Carlo study. Biophys. J. 81:2226-2240.
64. Schmiedeberg, L., K. Weisshart, S. Diekmann, G.M. Hoerste, and P. Hemmerich. 2004. High- and low-mobility populations of HP1 in heterochromatin and mammalian cells. Mol. Biol. Cell. 15:2819-2833.
65. Schueler, M.G., and B.A. Sullivan. 2006. Structural and functional dynamics of human centromeric chromatin. Annu. Rev. Genomics Hum. Genet. 7:301-313.
66. Schuh, M., C.F. Lehner, and S. Heidmann. 2007. Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr. Biol. 17:237-243.
67. Schwille, P., J. Korlach, and W.W. Webb. 1999. Fluorescence correlation spectroscopy with single molecule sensitivity on cell and model membranes. Cytometry. 36:176-182.
68. Shah, J.V., E. Botvinick, Z. Bonday, F. Furnari, M. Berns, and D.W. Cleveland. 2004. Dynamics of centromere and kinetochore proteins: implications for checkpoint signaling and silencing. Curr. Biol. 14:942-952.
69. Shelby, R.D., K. Monier, and K.F. Sullivan. 2000. Chromatin assembly at kinetochores is uncoupled from DNA replication. J. Cell Biol. 151:1113-1118.
70. Somanathan, S., T.M. Suchyna, A.J. Siegel, and R. Berezney. 2001. Targeting of PCNA to sites of DNA replication in the mammalian cell nucleus. J. Cell. Biochem. 81:56-67.
71. Sporbert, A., P. Domaing, H. Leonhardt, and M.C. Cardoso. 2005. PCNA acts as a stationary loading platform for transiently interacting Okazaki fragment maturation proteins. Nucleic Acids Res. 33:3521-3528.
72. Sprague, B.L., and J.G. McNally. 2005. FRAP analysis of binding: proper and fitting. Trends Cell Biol. 15:84-91.
73. Sugata, N., S. Li, W.C. Earnshaw, T.J. Yen, K. Yoda, H. Masumoto, E. Munekata, P.E. Warburton, and K. Todokoro. 2000. Human CENP-H multimers colocalize with CENP-A and CENP-C at active centromere-kinetochore complexes. Hum. Mol. Genet. 9:2919-2926.
74. Sugimoto, K., H. Yata, Y. Muro, and M. Himeno. 1994. Human centromere protein C (CENP-C) is a DNA-binding protein which possesses a novel DNA-binding motif. J. Biochem. (Tokyo). 116:877-881.
75. Sullivan, K.F., M. Hechenberger, and K. Masri. 1994. Human CENP-A contains a histone H3-related histone fold domain that is required for targeting to the centromere. J. Cell Biol. 127:581-592.
76. Suzuki, N., M. Nagano, N. Nozaki, S. Egashira, T. Okazaki, and H. Masumoto. 2004. CENP-B interacts with CENP-C domains containing Mif2 regions responsible for centromere localization. J. Biol. Chem. 279:5934-5946.
77. Takahashi, K., E.S. Chen, and M. Yanagida. 2000. Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science. 288:2215-2219.
78. Takahashi, K., Y. Takayama, F. Masuda, Y. Kobayashi, and S. Saitoh. 2005. Two distinct pathways responsible for the loading of CENP-A to centromeres in the fission yeast cell cycle. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360:595-607.
79. Ten Hagen, K.G., D.M. Gilbert, H.F. Willard, and S.N. Cohen. 1990. Replication timing of DNA sequences associated with human centromeres and telomeres. Mol. Cell. Biol. 10:6348-6355.
80. Tomkiel, J., C.A. Cooke, H. Saitoh, R.L. Bernat, and W.C. Earnshaw. 1994. CENP-C is required for maintaining proper kinetochore size and for a timely transition to anaphase. J. Cell Biol. 125:531-545.
81. Verreault, A. 2003. Histone deposition at the replication fork: a matter of urgency. Mol. Cell. 11:283-284.
82. Vos, L.J., J.K. Famulski, and G.K. Chan. 2006. How to build a centromere: from centromeric and pericentromeric chromatin to kinetochore assembly. Biochem. Cell Biol. 84:619-639.
83. Wachsmuth, M., W. Waldeck, and J. Langowski. 2000. Anomalous diffusion of fluorescent probes inside living cell nuclei investigated by spatially- resolved fluorescence correlation spectroscopy. J. Mol. Biol. 298:677-689.
84. Weidtkamp-Peters, S., H.P. Rahn, M.C. Cardoso, and P. Hemmerich. 2006. Replication of centromeric heterochromatin in mouse fibroblasts takes place in early, middle, and late S phase. Histochem. Cell Biol. 125: 91-102.
85. Weidtkamp-Peters, S., K. Weisshart, L. Schmiedeberg, and P. Hemmerich. 2008. Fluorescence correlation spectroscopy to assess the mobility of nuclear proteins. Methods Mol. Biol. In press.
86. Wieland, G., S. Orthaus, S. Ohndorf, S. Diekmann, and P. Hemmerich. 2004. Functional complementation of human centromere protein A (CENP-A) by Cse4 from S. cerevisiae. Mol. Cell. Biol. 24:6620-6630.
87. Yoda, K., S. Ando, A. Okuda, A. Kikuchi, and T. Okazaki. 1998. In vitro assembly of the CENP- B/alpha-satellite DNA/core histone complex: CENP-B causes nucleosome positioning. Genes Cells. 3:533-548.