A CENP-S/X complex assembles at the centromere in S and G2 phases of the human cell cycle

Open Biology

Volumn 4, Issue FEB, 2014, Pages

  Dornblut, Carsten ^a   Quinn, Nadine ^b   Monajambashi, Shamci ^a   Prendergast, Lisa ^b,e   Van Vuuren, Chelly ^b   Münch, Sandra ^a   Deng, Wen ^c   Leonhardt, Heinrich ^c   Cardoso, M Cristina ^d   Hoischen, Christian ^a   Diekmann, Stephan ^a   Sullivan, Kevin F ^b  

^a FLI   (Germany)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^c UNIVERSITY OF MUNICH   (Germany)

^d DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^e INSTITUT CURIE   (France)

Author keywords

Centromere; Constitutive centromere associated network; Kinetochore; Mitosis

Indexed keywords

APITD1 PROTEIN, HUMAN; APOPTOSIS REGULATORY PROTEIN; DNA; DNA BINDING PROTEIN; HISTONE; NONHISTONE PROTEIN; NUCLEAR PROTEIN; STRA13 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; BINDING SITE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CENTROMERE; CHEMICAL STRUCTURE; CONSTITUTIVE CENTROMERE-ASSOCIATED NETWORK; DNA DAMAGE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MITOSIS; TUMOR CELL LINE;

CENTROMERE; CONSTITUTIVE CENTROMERE-ASSOCIATED NETWORK; KINETOCHORE; MITOSIS;

APOPTOSIS REGULATORY PROTEINS; BINDING SITES; CELL LINE, TUMOR; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA; DNA DAMAGE; DNA-BINDING PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; G2 PHASE; HELA CELLS; HISTONES; HUMANS; MODELS, MOLECULAR; NUCLEAR PROTEINS; S PHASE; TUMOR SUPPRESSOR PROTEINS;

EID: 84901049522     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.130229     Document Type: Article

References (65)

1. Santaguida S, Musacchio A. 2009 The life and miracles of kinetochores. EMBO J. 28, 2511-2531. (doi:10.1038/emboj.2009.173)
2. Wan X et al. 2009 Protein architecture of the human kinetochore microtubule attachment site. Cell 137, 672-684. (doi:10.1016/j.cell.2009.03.035)
3. Palmer DK, O'Day K, Trong HL, Charbonneau H, Margolis RL 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. (doi:10.1073/pnas.88.9.3734) (Pubitemid 21916698)
4. Stoler S, Keith KC, Curnick KE, Fitzgerald-Hayes M. 1995 A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev. 9, 573-586. (doi:10.1101/gad.9.5.573)
5. Earnshaw WC et al. 2013 Esperanto for histones: CENP-A, not CenH3, is the centromeric histone H3 variant. Chromosome Res. 21, 101-106. (doi:10.1007/s10577-013-9347-y)
6. Mendiburo MJ, Padeken J, Fulop S., Schepers A, Heun P. 2011 Drosophila CENH3 is sufficient for centromere formation. Science 334, 686-690. (doi:10.1126/science.1206880)
7. Barnhart MC, Kuich PH, Stellfox ME, Ward JA, Bassett EA, Black BE, Foltz DR 2011 HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J. Cell Biol. 194, 229-243. (doi:10.1083/jcb. 201012017)
8. Fachinetti D et al. 2013 A two-step mechanism for epigenetic specification of centromere identity and function. Nat. Cell Biol. 15, 1056-1066. (doi:10.1038/ncb2805)
9. Hori T et al. 2008 CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135, 1039-1052. (doi:10.1016/j.cell.2008.10.019)
10. Foltz DR, Jansen LE, Black BE, Bailey AO, Yates 3rd JR, Cleveland DW. 2006 The human CENP-A centromeric nucleosome-associated complex. Nat. Cell Biol. 8, 458-469. (doi:10.1038/ncb1397)
11. Perpelescu M, Fukagawa T. 2011 The ABCs of CENPs. Chromosoma 120, 425-446. (doi:10.1007/s00412-011-0330-0)
12. Hori T, Shang WH, Takeuchi K, Fukagawa T. 2013 The CCAN recruits CENP-A to the centromere and forms the structural core for kinetochore assembly. J. Cell Biol. 200, 45-60. (doi:10.1083/jcb.201210106)
13. Carroll CW, Silva MC, Godek KM, Jansen LE, Straight AF 2009 Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat. Cell Biol. 11, 896-902. (doi:10.1038/ncb1899)
14. Prendergast L, van Vuuren C, Kaczmarczyk A, Doering V., Hellwig D, Quinn N, Hoischen C., Diekmann S, Sullivan KF. 2011 Premitotic assembly of human CENPs-T and -W switches centromeric chromatin to a mitotic state. PLoS Biol. 9, e1001082. (doi:10.1371/journal.pbio.1001082)
15. Gascoigne KE, Takeuchi K, Suzuki A., Hori T, Fukagawa T, Cheeseman IM 2011 Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 145, 410-422. (doi:10.1016/j.cell.2011.03.031)
16. Screpanti E, De Antoni A, Alushin GM, Petrovic A, Melis T., Nogales E, Musacchio A. 2011 Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr. Biol. 21, 391-398. (doi:10.1016/j.cub.2010.12.039)
17. Przewloka MR, Venkei Z, Bolanos-Garcia VM, Debski J., Dadlez M, Glover DM 2011 CENP-C is a structural platform for kinetochore assembly. Curr. Biol. 21, 399-405. (doi:10.1016/j.cub.2011.02.005)
18. Dunleavy EM et al. 2009 HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137, 485-497. (doi:10.1016/j.cell.2009.02.040)
19. Foltz DR, Jansen LE, Bailey AO, Yates 3rd JR, Bassett EA, Wood S, Black BE, Cleveland DW. 2009 Centromere-specific assembly of CENP-A nucleosomes is mediated by HJURP. Cell 137, 472-484. (doi:10.1016/j.cell.2009.02.039)
20. Stoler S, Rogers K, Weitze S., Morey L, Fitzgerald-Hayes M, Baker RE 2007 Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc. Natl Acad. Sci. USA 104, 10571-10576. (doi:10.1073/pnas.0703178104) (Pubitemid 47185706)
21. Mizuguchi G, Xiao H, Wisniewski J., Smith MM, Wu C. 2007 Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129, 1153-1164. (doi:10.1016/j.cell.2007.04.026) (Pubitemid 46900852)
22. Pidoux AL et al. 2009 Fission yeast Scm3: a CENP-A receptor required for integrity of subkinetochore chromatin. Mol. Cell. 33, 299-311. (doi:10.1016/j.molcel.2009.01.019)
23. Fujita Y, Hayashi T, Kiyomitsu T., Toyoda Y, Kokubu A, Obuse C., Yanagida M. 2007 Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev. Cell 12, 17-30. (doi:10.1016/j.devcel.2006.11.002) (Pubitemid 46002597)
24. Jansen LE, Black BE, Foltz DR, Cleveland DW 2007 Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176, 795-805. (doi:10.1083/jcb.200701066) (Pubitemid 46425540)
25. Bodor DL, Valente LP, Mata JF, Black BE, Jansen LE 2013 Assembly in G1 phase and long-term stability are unique intrinsic features of CENP-A nucleosomes. Mol. Biol. Cell 24, 923-932. (doi:10.1091/mbc.E13-01-0034)
26. Dunleavy EM, Almouzni G, Karpen GH 2011 H3.3 is deposited at centromeres in S phase as a placeholder for newly assembled CENP-A in G phase. Nucleus 2, 146-157. (doi:10.4161/nucl.2.2.15211)
27. Perpelescu M, Nozaki N, Obuse C., Yang H, Yoda K. 2009 Active establishment of centromeric CENP-A chromatin by RSF complex. J. Cell Biol. 185, 397-407. (doi:10.1083/jcb.200903088)
28. Lagana A, Dorn JF, De Rop V, Ladouceur AM, Maddox AS, Maddox PS 2010 A small GTPase molecular switch regulates epigenetic centromere maintenance by stabilizing newly incorporated CENP-A. Nat. Cell Biol. 12, 1186-1193. (doi:10.1038/ncb2129)
29. Hemmerich P, Weidtkamp-Peters S, Hoischen C., Schmiedeberg L, Erliandri I, Diekmann S. 2008 Dynamics of inner kinetochore assembly and maintenance in living cells. J. Cell Biol. 180, 1101-1114. (doi:10.1083/jcb.200710052) (Pubitemid 351468468)
30. Nishino T, Takeuchi K, Gascoigne KE, Suzuki A., Hori T, Oyama T, Morikawa K., Cheeseman IM, Fukagawa T. 2012 CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold. Cell 148, 487-501. (doi:10.1016/j.cell.2011.11.061)
31. Schleiffer A, Maier M, Litos G., Lampert F, Hornung P, Mechtler K., Westermann S. 2012 CENP-T proteins are conserved centromere receptors of the Ndc80 complex. Nat. Cell Biol. 14, 604-613. (doi:10.1038/ncb2493)
32. Malvezzi F, Litos G, Schleiffer A., Heuck A, Mechtler K, Clausen T., Westermann S. 2013 A structural basis for kinetochore recruitment of the Ndc80 complex via two distinct centromere receptors. EMBO J. 32, 409-423. (doi:10.1038/emboj.2012.356)
33. Nishino T, Rago F, Hori T., Tomii K, Cheeseman IM, Fukagawa T. 2013 CENP-T provides a structural platform for outer kinetochore assembly. EMBO J. 32, 424-436. (doi:10.1038/emboj.2012.348)
34. Amano M, Suzuki A, Hori T., Backer C, Okawa K, Cheeseman IM, Fukagawa T. 2009 The CENP-S complex is essential for the stable assembly of outer kinetochore structure. J. Cell Biol. 186, 173-182. (doi:10.1083/jcb.200903100)
35. Singh TR et al. 2010 MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol. Cell 37, 879-886. (doi:10.1016/j.molcel.2010.01.036)
36. Yan Z et al. 2010 A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol. Cell 37, 865-878. (doi:10.1016/j.molcel.2010.01.039)
37. Huang M, Kim JM, Shiotani B, Yang K., Zou L, D'Andrea AD. 2010 The FANCM/FAAP24 complex is required for the DNA interstrand crosslink-induced checkpoint response. Mol. Cell39, 259-268. (doi:10.1016/j.molcel.2010.07.005)
38. Bacia K, Schwille P. 2007 Practical guidelines for dual-color fluorescence cross-correlation spectroscopy. Nat Protoc. 2, 2842-2856. (doi:10.1038/nprot.2007.410)
39. Kohl THE, Schwille P. 2005 Determining protease activity in vivo by fluorescence cross-correlation analysis. Biophys. J. 89, 2770-2782. (doi:10.1529/biophysj.105.061127) (Pubitemid 41401066)
40. 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. Nucleic Acids Res. 37, 3391-3406. (doi:10.1093/nar/gkp199)
41. Tramier M, Zahid M, Mevel JC, Masse MJ, Coppey-Moisan M. 2006 Sensitivity of CFP/YFP and GFP/mCherry pairs to donor photobleaching on FRET determination by fluorescence lifetime imaging microscopy in living cells. Microsc. Res. Tech. 69, 933-939. (doi:10.1002/jemt.20370) (Pubitemid 44706606)
42. Sittman DB, Graves RA, Marzluff WF 1983 Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. Proc. Natl Acad. Sci. USA 80, 1849-1853. (doi:10.1073/pnas.80.7.1849) (Pubitemid 13079193)
43. Pines J, Hunter T. 1990 Human cyclin A is adenovirus E1A-associated protein p60 and behaves differently from cyclin B. Nature 346, 760-763. (doi:10.1038/346760a0)
44. Pines J, Hunter T. 1989 Isolation of a human cyclin cDNA: evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2. Cell 58, 833-846. (doi:10.1016/0092-8674(89)90936-7) (Pubitemid 19227894)
45. Gautier A, Juillerat A, Heinis C., Correa Jr IR, Kindermann M, Beaufils F, Johnsson K. 2008 An engineered protein tag for multiprotein labeling in living cells. Chem. Biol. 15, 128-136. (doi:10.1016/j.chembiol.2008.01.007) (Pubitemid 351253620)
46. Zolghadr K, Mortusewicz O, Rothbauer U., Kleinhans R, Goehler H, Wanker EE, Cardoso MC, Leonhardt H. 2008 A fluorescent two-hybrid assay for direct visualization of protein interactions in living cells. Mol. Cell Proteomics 7, 2279-2287. (doi:10.1074/mcp.M700548-MCP200)
47. Helfricht A, Wiegant WW, Thijssen PE, Vertegaal AC, Luijsterburg MS, van Attikum H. 2013 Remodeling and spacing factor 1 (RSF1) deposits centromere proteins at DNA double-strand breaks to promote non-homologous end-joining. Cell Cycle 12, 3070-3082. (doi:10.4161/cc.26033)
48. Bhattacharjee S, Osman F, Feeney L., Lorenz A, Bryer C, Whitby MC 2013 MHF1-2/CENP-S-X performs distinct roles in centromere metabolism and genetic recombination. Open Biol. 3, 130102. (doi:10.1098/rsob.130102)
49. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ 2002 Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319, 1097-1113. (doi:10.1016/s0022-2836(02) 00386-8) (Pubitemid 34729421)
50. Kimura H, Cook PR 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. (doi:10.1083/jcb.153.7.1341) (Pubitemid 34286121)
51. Silva MC, Bodor DL, Stellfox ME, Martins NM, Hochegger H, Foltz DR, Jansen LE 2012 Cdk activity couples epigenetic centromere inheritance to cell cycle progression. Dev. Cell 22, 52-63. (doi:10.1016/j.devcel.2011.10.014)
52. Venkei Z, Przewloka MR, Ladak Y, Albadri S., Sossick A, Juhasz G, Novak B., Glover DM 2012 Spatiotemporal dynamics of Spc105 regulates the assembly of the Drosophila kinetochore. Open Biol. 2, 110032. (doi:10.1098/rsob.110032)
53. Hellwig D et al. 2011 Dynamics of CENP-N kinetochore binding during the cell cycle. J. Cell Sci. 124, 3871-3883. (doi:10.1242/jcs.088625)
54. Eskat A et al. 2012 Step-wise assembly, maturation and dynamic behavior of the human CENP-P/O/R/Q/U kinetochore sub-complex. PLoS ONE 7, e44717. (doi:10.1371/journal.pone.0044717)
55. de Lichtenberg U., Jensen TS, Brunak S, Bork P., Jensen LJ 2007 Evolution of cell cycle control: same molecular machines, different regulation. Cell Cycle 6, 1819-1825. (doi:10.4161/cc.6.15.4537) (Pubitemid 47327898)
56. Dambacher S et al. 2012 CENP-C facilitates the recruitment of M18BP1 to centromeric chromatin. Nucleus 3, 1. (doi:10.4161/nucl.18955)
57. 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. (doi:10.1083/jcb.201106079)
58. Amaro AC, Samora CP, Holtackers R, Wang E., Kingston IJ, Alonso M, Lampson M, McAinsh AD, Meraldi P. 2010 Molecular control of kinetochore- microtubule dynamics and chromosome oscillations. Nat. Cell Biol. 12, 319-329. (doi:10.1038/ncb2033)
59. Monier K, Mouradian S, Sullivan KF 2007 DNA methylation promotes Aurora-B-driven phosphorylation of histone H3 in chromosomal subdomains. J. Cell Sci. 120, 101-114. (doi:10.1242/jcs.03326) (Pubitemid 46206653)
60. 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. (doi:10.1093/nar/gki665) (Pubitemid 41430575)
61. Pfaffl MW. 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45. (doi:10.1093/nar/29.9.e45)
62. Tsukamoto T, Hashiguchi N, Janicki SM, Tumbar T., Belmont AS, Spector DL 2000 Visualization of gene activity in living cells. Nat. Cell Biol. 2, 871-878. (doi:10.1038/35046510)
63. Alonso A, Fritz B, Hasson D., Abrusan G, Cheung F, Yoda K., Radlwimmer B, Ladurner AG, Warburton PE 2007 Co-localization of CENP-C and CENP-H to discontinuous domains of CENP - A chromatin at human neocentromeres. Genome Biol. 8, R148. (doi:10.1186/gb-2007-8-7-r148)
64. Chen D, Huang S. 2001 Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. J. Cell Biol. 153, 169-176. (doi:10.1083/jcb.153.1.169) (Pubitemid 34280203)
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. (doi:10.1091/mbc.E03-11-0827) (Pubitemid 38691870)