Step-Wise Assembly, Maturation and Dynamic Behavior of the Human CENP-P/O/R/Q/U Kinetochore Sub-Complex

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Eskat, Anja ^a,c   Deng, Wen ^b   Hofmeister, Antje ^a   Rudolphi, Sven ^a   Emmerth, Stephan ^c,f   Hellwig, Daniela ^a,g   Ulbricht, Tobias ^a   Döring, Volker ^a   Bancroft, James M ^e   McAinsh, Andrew D ^e   Cardoso, M Cristina ^d   Meraldi, Patrick ^c   Hoischen, Christian ^a   Leonhardt, Heinrich ^b   Diekmann, Stephan ^a  

^a Molecular Biology   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c ETH ZURICH   (Switzerland)

^d DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^e UNIVERSITY OF WARWICK   (United Kingdom)

^f FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^g HKI   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN N; CENTROMERE PROTEIN O; CENTROMERE PROTEIN P; CENTROMERE PROTEIN Q; CENTROMERE PROTEIN R; CENTROMERE PROTEIN T; CENTROMERE PROTEIN U; CENTROMERE PROTEIN W; CONSTITUITIVE CENTROMERE ASSOCIATED NETWORK COMPLEX; HETERODIMER; NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE S PHASE; CENTROMERE; COMPLEX FORMATION; CONFORMATION; CONTROLLED STUDY; CYTOPLASM; FLUORESCENCE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MICROTUBULE; MOLECULAR DYNAMICS; NUCLEOSOME; OLIGOMERIZATION; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY;

BLOTTING, WESTERN; CELL LINE, TUMOR; CHROMOSOMAL PROTEINS, NON-HISTONE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELLS; HUMANS; KINETOCHORES; NUCLEAR PROTEINS;

MAMMALIA;

EID: 84866484902     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044717     Document Type: Article

References (70)

1. Perpelescu M, Fukagawa T, (2011) The ABCs of CENPs. Chromosoma 120: 425-446.
2. Takeuchi K, Fukagawa T, (2012) Molecular architecture of vertebrate kinetochores. Exp Cell Res 318: 1367-1374.
3. Cheeseman IM, Desai A, (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9: 33-46.
4. Przewloka M, Glover DM, (2009) The kinetochore and the centromere: a working long distance relationship. Annu Rev Genet 43: 439-465.
5. Foltz DR, Jansen LET, Black BE, Bailey AO, YatesIII JR, et al. (2006) The human CENP-A centromeric complex. Nat Cell Biol 8: 458-469.
6. Okada M, Cheeseman IM, Hori T, Okawa K, McLeod IX, et al. (2006) The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nature Cell Biol 8: 446-457.
7. Meraldi P, McAinsh AD, Rheinbay E, Sorger PK, (2006) Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7: R23.
8. McClelland SE, Borusu S, Amaro AC, Winter JR, Belwal M, et al. (2007) The CENP-A NAC/CAD kinetochore complex controls chromosome congression and spindle bipolarity. EMBO J 26: 5033-5047.
9. Hori T, Amano M, Suzuki A, Backer CB, Welburn JP, et al. (2008) CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135: 1039-1052.
10. Hori T, Okada M, Maenaka K, Fukagawa T, (2008) CENP-O class proteins form a stable complex and are required for proper kinetochore function. Mol Biol Cell 19: 843-854.
11. Amano M, Suzuki A, Hori T, Backer C, Okawa K, et al. (2009) The CENP-S complex is essential for the stable assembly of outer kinetochore structure. J Cell Biol 186: 173-182.
12. Nishino T, Takeuchi K, Gascoigne KE, Suzuki A, Hori T, et al. (2012) CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold. Cell 148: 487-501.
13. Santaguida S, Musacchio A, (2009) The life and miracles of kinetochores. EMBO J 28: 2511-2531.
14. Carroll CW, Silva MCC, Godek KM, Jansen LET, Straight AF, (2009) Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat Cell Biol 11: 896-902.
15. Carroll CW, Milks KJ, Straight AF, (2010) Dual recognition of CENP-A nucleosomes is required for centromere assembly. J Cell Biol 189: 1143-1155.
16. Guse A, Carroll CW, Moree B, Fuller CJ, Straight AF, (2011) In vitro centromere and kinetochore assembly on defined chromatin templates. Nature 477: 354-358.
17. Tachiwana H, Kagawa W, Shiga T, Osakabe A, Miya Y, et al. (2011) Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 476: 232-235.
18. Bui M, Dimitriadis EK, Hoischen C, An E, Quenet D, et al. (2012) Cell cycle-dependent structural transitions in the human CENP-A nucleosome in vivo. Cell 150: 317-326.
19. De Wulf P, McAinsh AD, Sorger PK, (2003) Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev 17: 2902-2921.
20. Cheeseman IM, Niessen S, Anderson S, Hyndman F, Yates JR 3rd, et al. (2004) A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev 18: 2255-2268.
21. Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A, (2006) The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127: 983-997.
22. Obuse C, Yang H, Nozaki N, Goto S, Okazaki T, et al. (2004) Proteomics analysis of the centromere complex from HeLa interphase cells: UV-damaged DNA binding protein 1 (DDB-1) is a component of the CEN-complex, while BMI-1 is transiently co-localised with the centromeric region in interphase. Genes to Cells 9: 105-120.
23. Liu X, McLeod I, Anderson S, Yates JR 3rd, He X, (2005) Molecular analysis of kinetochore architecture in fission yeast. EMBO J 24: 2919-2930.
24. Petrovic A, Pasqualato S, Dube P, Krenn V, Santaguida S, et al. (2010) The Mis12 complex is a protein interaction hub for outer kinetochore assembly. J Cell Biol 190: 835-852.
25. Kiyomitsu T, Iwasaki O, Obuse C, Yanagida M, (2010) Inner centromere formation requires hMis14, a trident kinetochore protein that specifically recruits HP1 to human chromosomes. J Cell Biol 188: 791-807.
26. Liu D, Vleugel M, Backer CB, Hori T, Fukagawa T, et al. (2010) Regulated targeting of protein phosphatise 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J Cell Biol 188: 809-820.
27. Przewloka MR, Venkei Z, Bolanos-Garcia VM, Debski J, et al. (2011) CENP-C is a structural platform for kinetochore assembly. Curr Biol 21: 399-405.
28. Tanaka TU, Desai A, (2008) Kinetochore-microtubule interactions: the means to the end. Curr Opin Cell Biol 20: 53-63.
29. Wan X, O'Quinn RP, Pierce HL, Joglekar AP, Gall WE, et al. (2009) Protein architecture of the human kinetochore microtubule attachment site. Cell 137: 672-684.
30. Moree B, Meyer CB, Fuller CJ, Straight AF, (2011) CENP-C recruits M18BP1 to centromeres to promote CENP-A chromatin assembly. J Cell Biol 194: 855-871.
31. Barnhart MC, Kuich HJL, Stellfox ME, Ward JA, Bassett EA, et al. (2011) HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J Cell Biol 194: 229-243.
32. Fukagawa T, Mikami Y, Nishihashi A, Regnier V, Haraguchi T, et al. (2001) CENP-H, a constitutive centromere component, is required for centromere targeting of CENP-C in vertebrate cells. EMBO J 20: 4603-4617.
33. McAinsh AD, Meraldi P, Draviam VM, Toso A, Sorger PK, (2006) The human kinetochore proteins Nnf1R and Mcm21R are required for accurate chromosome segregation. EMBO J 25: 4033-4049.
34. Toso A, Winter JR, Garrod AJ, Amaro AC, Meraldi P, et al. (2009) Kinetochore-generated pushing forces separate centrosomes during bipolar spindle assembly. J Cell Biol 184: 365-372.
35. Gascoigne KE, Takeuchi K, Suzuki A, Hori T, Fukagawa T, et al. (2011) Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 145: 410-422.
36. Amaro AC, Samora CP, Holtackers R, Wang E, Kingston IJ, et al. (2010) Molecular control of kinetochore-microtubule dynamics and chromosome oscillations. Nature Cell Biol 12: 319-329.
37. Izuta H, Ikeno M, Suzuki N, Tomonaga T, Nozaki N, et al. (2006) Comprehensive analysis of the ICEN (Interphase Centromere Complex) components enriched in the CENP-A chromatin of human cells. Genes Cells 11: 673-684.
38. Minoshima Y, Hori T, Okada M, Kimura H, Haraguchi T, et al. (2005) The constitutive centromere component CENP-50 is required for recovery from spindle damage. Mol Cell Biol 25: 10315-10328.
39. Hua S, Wang Z, Jiang K, Huang Y, Ward T, et al. (2011) CENP-U cooperates with Hec1 to orchestrate kinetochore-microtubule attachment. J Biol Chem 286: 1627-1638.
40. Kang YH, Park JE, Yu LR, Soung NK, Yun SM, et al. (2006) Self-regulated Plk1 recruitment to kinetochores by the Plk1-PBIP1 interaction is critical for proper chromosome segregation. Mol Cell 24: 409-422.
41. Kang YH, Park C-H, Kim T-S, Soung N-K, Bang JK, et al. (2011) Mammalian Polo-like kinase 1-dependent regulation of the PBIP1-CENP-Q complex at kinetochores. J Biol Chem 286: 19744-19757.
42. Schmitzberger F, Harrison SC, (2012) RWD domain: a recurring module in kinetochore architecture shown by Ctf19-Mcm21 complex structure. EMBO Rep 13: 216-222.
43. Hellwig D, Hoischen C, Ulbricht T, Diekmann S, (2009) Acceptor-photobleaching FRET analysis of core kinetochore and NAC proteins in living human cells. Eur Biophys J 38: 781-791.
44. Hellwig D, Emmerth S, Ulbricht T, Doering V, Hoischen C, et al. (2011) Dynamics of CENP-N kinetochore binding during the cell cycle. J Cell Sci 124: 3871-3883.
45. Tsukamoto T, Hashiguchi N, Janicki SM, Tumbar T, Belmont AS, et al. (2000) Visualization of gene activity in living cells. Nat Cell Biol 2: 871-878.
46. Rothbauer U, Zolghadr K, Tillib S, Nowak D, Schermelleh L, et al. (2006) Targeting and tracing antigens in live cells with fluorescent nanobodies. Nat Methods 3: 887-889.
47. Zolghadr K, Mortusewicz O, Rothbauer U, Kleinhans R, Goehler H, et al. (2008) A fluorescent two-hybrid assay for direct visualization of protein interactions in living cells. Mol Cell Proteomics 7: 2279-2287.
48. Orthaus S, Biskup C, Hoffmann B, Hoischen C, Ohndorf S, et al. (2008) Assembly of the inner kinetochore proteins CENP-A and CENP-B in living human cells. Chem Bio Chem 9: 77-92.
49. Bacia K, Schwille P, (2003) A dynamic view of cellular processes by in vivo fluorescence auto- and cross-correlation spectroscopy. Methods 29: 74-85.
50. Bacia K, Schwille P, (2007) Practical guidelines for dual-color fluorescence cross-correlation spectroscopy. Nature Protocols 2.28422856.
51. Orthaus S, Klement K, Happel N, Hoischen C, Diekmann S, (2009) Linker Histone H1 is present in centromeric chromatin of living human cells next to inner kinetochore proteins. Nucl Acids Res 37: 3391-3406.
52. Milks KJ, Moree B, Straight AF, (2009) Dissection of CENP-C directed centromere and kinetochore assembly. Mol Biol Cell 20: 4246-4255.
53. Qui SL, Wang JN, Yu C, He DC, (2009) CENP-K and CENP-H may form coiled-coils in the kinetochores. Sci China Ser C-Life Sci 52: 352-359.
54. Digman MA, Brown CM, Sengupta P, Wiseman PW, Horwitz AR, et al. (2005) Measuring fast dynamics in solutions and cells with a laser scanning microscope. Biophys J 89: 1317-1327.
55. Hemmerich P, Weidtkamp-Peters S, Hoischen C, Schmiedeberg L, Erliandri I, et al. (2008) Dynamics of inner kinetochore assembly and maintenance in living cells. J Cell Biol 180: 1101-1114.
56. Kohl T, Haustein E, Schwille P, (2005) Determining protease activity in vivo by fluorescence cross-correlation analysis. Biophys J 89: 2770-2782.
57. Hanissian SH, Akbar U, Teng B, Janjetovic Z, Hoffmann A, et al. (2004) cDNA cloning and characterization of a novel gene encoding the MLF1-interacting protein MLF1IP. Oncogene 23: 3700-3707.
58. Suzuki H, Arakawa Y, Ito M, Saito S, Takeda N, et al. (2007) MLF1-interacting protein is mainly localized in nucleolus through N-terminal bipartite nuclear localization signal. Anticancer Res 27: 1423-1430.
59. Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H, et al. (2003) A general method for the covalent labelling of fusion proteins with small molecules in vivo. Nat Biotechnol 21: 86-89.
60. Jansen LET, Black BE, Foltz DR, Cleveland DW, (2007) Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176: 795-805.
61. Prendergast L, van Vuuren C, Kaczmarczyk A, Döring V, Hellwig D, et al. (2011) Premitotic assembly of human CENPs-T and-W switches centromeric chromatin to a mitotic state. PloS Biol 9: e1001082.
62. Lee KS, Oh DY, Kang YH, Park JE, (2008) Self-regulated mechanism of Plk1 localisation to kinetochores: lessons from the Plk1-PBIP1 interaction. Cell Div 3: 4.
63. Leonhardt H, Rahn HP, Weinzierl P, Sporbert A, Cremer T, et al. (2000) Dynamics of DNA replication factories in living cells. J Cell Biol 149: 271-280.
64. Sporbert A, Domaing P, Leonhardt H, Cardoso MC, (2005) PCNA acts as a stationary loading platform for transiently interacting Okazaki fragment maturation proteins. Nucleic Acids Res 33: 3521-3528.
65. Schmiedeberg L, Weisshart K, Diekmann S, Meyer zu Hoerste G, Hemmerich P, (2004) High- and low-mobility populations of HP1 in heterochromatin of mammalian cells. Mol Biol Cell 15: 2819-2833.
66. Ribeiro SA, Vagnarelli P, Dong Y, Hori T, McEwen BF, et al. (2010) A super-resolution map of the vertebrate kinetochore. Proc Natl Acad Sci USA 107: 10484-10489.
67. Johnston K, Joglekar A, Hori T, Suzuki A, Fukagawa T, Salmon ED, (2010) Vertebrate kinetochore protein architecture: protein copy number. J Cell Biol 189: 937-943.
68. Lawrimore J, Bloom KS, Salmon ED, (2011) Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome. J Cell Biol 195: 573-582.
69. Hemmerich P, Schmiedeberg L, Diekmann S, (2011) Dynamic as well as stable protein interactions contribute to genome function and maintenance. Chromosome Res 19: 131-151.
70. Dong Y, VandenBeldt KJ, Meng X, Khodjakov A, McEwen BF, (2010) The outer plate in vertebrate kinetochores is a flexible network with multiple microtubule interactions. Nat Cell Biol 9: 516-522.