The unconventional structure of centromeric nucleosomes

详细信息    查看全文

• 作者：Steven Henikoff (1) steveh@fhcrc.org
  Takehito Furuyama (1)
• 刊名：Chromosoma
• 出版年：2012
• 出版时间：August 2012
• 年：2012
• 卷：121
• 期：4
• 页码：341-352
• 全文大小：524.7 KB
• 参考文献：1. Ahmad K, Henikoff S (2002) Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci USA 99(Suppl 4):16477–16484
  2. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD (1989) Molecular biology of the cell. Garland, New York
  3. 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
  4. Amor DJ, Bentley K, Ryan J, Perry J, Wong L, Slater H, Choo KH (2004) Human centromere repositioning “in progress”. Proc Natl Acad Sci USA 101:6542–6547
  5. Black BE, Cleveland DW (2011) Epigenetic centromere propagation and the nature of CENP-A nucleosomes. Cell 144:471–479
  6. Bloom KS, Amaya E, Carbon J, Clarke L, Hill A, Yeh E (1984) Chromatin conformation of yeast centromeres. J Cell Biol 99:1559–1568
  7. Blower MD, Sullivan BA, Karpen GH (2002) Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2:319–330
  8. Buchwitz BJ, Ahmad K, Moore LL, Roth MB, Henikoff S (1999) A histone-H3-like protein in C. elegans. Nature 401:547–548
  9. Camahort R, Shivaraju M, Mattingly M, Li B, Nakanishi S, Zhu D, Shilatifard A, Workman JL, Gerton JL (2009) Cse4 is part of an octameric nucleosome in budding yeast. Mol Cell 35:794–805
  10. Chen W, Tabor S, Struhl K (1987) Distinguishing between mechanisms of eukaryotic transcriptional activation with bacteriophage T7 RNA polymerase. Cell 50:1047–1055
  11. Cho US, Harrison SC (2011) Recognition of the centromere-specific histone Cse4 by the chaperone Scm3. Proc Natl Acad Sci USA 108:9367–9371
  12. Clarke L, Carbon J (1980) Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287:504–509
  13. Coffman VC, Wu P, Parthun MR, Wu JQ (2011) CENP-A exceeds microtubule attachment sites in centromere clusters of both budding and fission yeast. J Cell Biol 195:563–572
  14. Cole HA, Howard BH, Clark DJ (2011) The centromeric nucleosome of budding yeast is perfectly positioned and covers the entire centromere. Proc Natl Acad Sci USA 108:12687–12692
  15. Collins KA, Furuyama S, Biggins S (2004) Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr Biol 14:1968–1972
  16. Conde e Silva N, Black BE, Sivolob A, Filipski J, Cleveland DW, Prunell A (2007) CENP-A-containing nucleosomes: easier disassembly versus exclusive centromeric localization. J Mol Biol 370:555–573
  17. da Rosa JL, Holik J, Green EM, Rando OJ, Kaufman PD (2010) Overlapping regulation of CenH3 localization and histone H3 turnover by CAF-1 and HIR proteins in Saccharomyces cerevisiae. Genetics 187:9–19
  18. Dalal Y, Bui M (2010) Down the rabbit hole of centromere assembly and dynamics. Curr Opin Cell Biol 22:392–402
  19. Dalal Y, Wang H, Lindsay S, Henikoff S (2007) Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol 5:e218
  20. Deal RB, Henikoff JG, Henikoff S (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328:1161–1164
  21. Dechassa ML, Wyns K, Li M, Hall MA, Wang MD, Luger K (2011) Structure and Scm3-mediated assembly of budding yeast centromeric nucleosomes. Nat Commun 2:313
  22. Densmore L, Payne WE, Fitzgerald-Hayes M (1991) In vivo genomic footprint of a yeast centromere. Mol Cell Biol 11:154–165
  23. Dimitriadis EK, Weber C, Gill RK, Diekmann S, Dalal Y (2010) Tetrameric organization of vertebrate centromeric nucleosomes. Proc Natl Acad Sci USA 107:20317–20322
  24. Dion M, Kaplan T, Friedman N, Rando OJ (2007) Dynamics of replication-independent histone turnover in budding yeast. Science 315:1405–1408
  25. Dunleavy EM, Roche D, Tagami H, Lacoste N, Ray-Gallet D, Nakamura Y, Daigo Y, Nakatani Y, Almouzni-Pettinotti G (2009) HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137:485–497
  26. Flemming W (1882) Zellsubstanz. Kern und Zelltheilung. F. C. W, Vogel, Leipzig
  27. Floridia G, Gimelli G, Zuffardi O, Earnshaw WC, Warburton PE, Tyler-Smith C (2000) A neocentromere in the DAZ region of the human Y chromosome. Chromosoma 109:318–327
  28. Foltz DR, Jansen LE, Black BE, Bailey AO, Yates JR 3rd, Cleveland DW (2006) The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 8:458–469
  29. Furuyama S, Biggins S (2007) Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc Natl Acad Sci USA 104:14706–14711
  30. Furuyama T, Henikoff S (2009) Centromeric nucleosomes induce positive DNA supercoils. Cell 138:104–113
  31. Furuyama T, Dalal Y, Henikoff S (2006) Chaperone-mediated assembly of centromeric chromatin in vitro. Proc Natl Acad Sci USA 103:6172–6177
  32. Gkikopoulos T, Singh V, Tsui K, Awad S, Renshaw MJ, Scholfield P, Barton GJ, Nislow C, Tanaka TU, Owen-Hughes T (2011) The SWI/SNF complex acts to constrain distribution of the centromeric histone variant Cse4. EMBO J 30:1919–1927
  33. Hamiche A, Richard-Foy H (1998) The switch in the helical handedness of the histone (H3-H4)2 tetramer within a nucleoprotein particle requires a reorientation of the H3–H3 interface. J Biol Chem 273:9261–9269
  34. Harrington JJ, Van Bokkelen G, Mays RW, Gustashaw K, Willard HF (1997) Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat Genet 15:345–355
  35. Henikoff S, Furuyama T (2010) Epigenetic inheritance of centromeres. Cold Spring Harb Symp Quant Biol 75:51–60
  36. Henikoff S, Henikoff JG (2012) ‘Point’ Centromeres of Saccharomyces harbor single CenH3 nucleosomes. Genetics 190:1575–1577
  37. Heun P, Erhardt S, Blower MD, Weiss S, Skora AD, Karpen GH (2006) Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell 10:303–315
  38. Hewawasam G, Shivaraju M, Mattingly M, Venkatesh S, Martin-Brown S, Florens L, Workman JL, Gerton JL (2010) Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol Cell 40:444–454
  39. Huang CC, Chang KM, Cui H, Jayaram M (2011) Histone H3-variant Cse4-induced positive DNA supercoiling in the yeast plasmid has implications for a plasmid origin of a chromosome centromere. Proc Natl Acad Sci USA 108:13671–13676
  40. Kent NA, Adams S, Moorhouse A, Paszkiewicz K (2011) Chromatin particle spectrum analysis: a method for comparative chromatin structure analysis using paired-end mode next-generation DNA sequencing. Nucleic Acids Res 39:e26
  41. Ketel C, Wang HS, McClellan M, Bouchonville K, Selmecki A, Lahav T, Gerami-Nejad M, Berman J (2009) Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5:e1000400
  42. Kingston IJ, Yung JS, Singleton MR (2011) Biophysical characterization of the centromere-specific nucleosome from budding yeast. J Biol Chem 286:4021–4026
  43. Krassovsky K, Henikoff JG, Henikoff S (2012) Tripartite organization of centromeric chromatin in budding yeast. Proc Natl Acad Sci USA 109:243–248
  44. Lander ES, Linton LM, Birren B, Nusbaum C et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
  45. Lantermann AB, Straub T, Stralfors A, Yuan GC, Ekwall K, Korber P (2010) Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae. Nat Struct Mol Biol 17:251–257
  46. Lavelle C, Recouvreux P, Wong H, Bancaud A, Viovy JL, Prunell A, Victor JM (2009) Right-handed nucleosome: myth or reality? Cell 139:1216–1217, Author reply 1217–1218
  47. 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
  48. Lefrancois P, Euskirchen GM, Auerbach RK, Rozowsky J, Gibson T, Yellman CM, Gerstein M, Snyder M (2009) Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing. BMC Genomics 10:37
  49. Lomiento M, Jiang Z, D'Addabbo P, Eichler EE, Rocchi M (2008) Evolutionary-new centromeres preferentially emerge within gene deserts. Genome Biol 9:R173
  50. Luconi L, Araki Y, Erlemann S, Schiebel E (2011) The CENP-A chaperone Scm3 becomes enriched at kinetochores in anaphase independently of CENP-A incorporation. Cell Cycle 10:3369–3378
  51. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260
  52. Luger K, Rechsteiner TJ, Richmond TJ (1999) Preparation of nucleosome core particle from recombinant histones. Methods Enzymol 304:3–19
  53. Luk E, Ranjan A, Fitzgerald PC, Mizuguchi G, Huang Y, Wei D, Wu C (2010) Stepwise histone replacement by SWR1 requires dual activation with histone H2A.Z and canonical nucleosome. Cell 143:725–736
  54. Malik HS, Henikoff S (2009) Major evolutionary transitions in centromere complexity. Cell 138:1067–1082
  55. Marshall OJ, Chueh AC, Wong LH, Choo KH (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82:261–282
  56. Meluh PB, Yang P, Glowczewski L, Koshland D, Smith MM (1998) Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94:607–613
  57. Mendiburo MJ, Padeken J, Fulop S, Schepers A, Heun P (2011) Drosophila CENH3 is sufficient for centromere formation. Science 334:686–690
  58. 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
  59. Moreno-Moreno O, Torras-Llort M, Azorin F (2006) Proteolysis restricts localization of CID, the centromere-specific histone H3 variant of Drosophila, to centromeres. Nucleic Acids Res 34:6247–6255
  60. Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36:138–145
  61. Niedenthal RK, Sen-Gupta M, Wilmen A, Hegemann JH (1993) Cpf1 protein induced bending of yeast centromere DNA element I. Nucleic Acids Res 21:4726–4733
  62. 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
  63. Pidoux AL, Choi ES, Abbott JK, Liu X, Kagansky A, Castillo AG, Hamilton GL, Richardson W, Rappsilber J, He X, Allshire RC (2009) Fission yeast Scm3: a CENP-A receptor required for integrity of subkinetochore chromatin. Mol Cell 33:299–311
  64. Pietrasanta LI, Thrower D, Hsieh W, Rao S, Stemmann O, Lechner J, Carbon J, Hansma H (1999) Probing the Saccharomyces cerevisiae centromeric DNA (CEN DNA)-binding factor 3 (CBF3) kinetochore complex by using atomic force microscopy. Proc Natl Acad Sci USA 96:3757–3762
  65. Platero JS, Ahmad K, Henikoff S (1999) A distal heterochromatic block displays centromeric activity when detached from a natural centromere. Mol Cell 4:995–1004
  66. Polizzi C, Clarke L (1991) The chromatin structure of centromeres from fission yeast: differentiation of the central core that correlates with function. J Cell Biol 112:191–201
  67. Qin JY, Zhang L, Clift KL, Hulur I, Xiang AP, Ren BZ, Lahn BT (2010) Systematic comparison of constitutive promoters and the doxycycline-inducible promoter. PLoS One 5:e10611
  68. Ranjitkar P, Press MO, Yi X, Baker R, MacCoss MJ, Biggins S (2010) An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol Cell 40:455–464
  69. Rose MD, Novick P, Thomas JH, Botstein D, Fink GR (1987) A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene 60:237–243
  70. Sandman K, Reeve JN (2006) Archaeal histones and the origin of the histone fold. Curr Opin Microbiol 9:520–525
  71. Segal E, Widom J (2009) Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr Opin Struct Biol 19:65–71
  72. Sekulic N, Bassett EA, Rogers DJ, Black BE (2010) The structure of (CENP-A-H4)(2) reveals physical features that mark centromeres. Nature 467:347–351
  73. Shivaraju M, Camahort R, Mattingly M, Gerton JL (2011) Scm3 is a centromeric nucleosome assembly factor. J Biol Chem 286:12016–12023
  74. 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
  75. Sun X, Wahlstrom J, Karpen G (1997) Molecular structure of a functional Drosophila centromere. Cell 91:1007–1019
  76. Tachiwana H, Kagawa W, Shiga T, Osakabe A, Miya Y, Saito K, Hayashi-Takanaka Y, Oda T, Sato M, Park SY, Kimura H, Kurumizaka H (2011) Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 476:232–235
  77. Takahashi K, Murakami S, Chikashige Y, Funabiki H, Niwa O, Yanagida M (1992) A low copy number central sequence with strict symmetry and unusual chromatin structure in fission yeast centromere. Mol Biol Cell 3:819–835
  78. Talbert PB, Henikoff S (2010) Histone variants—ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11:264–275
  79. Tsankov AM, Thompson DA, Socha A, Regev A, Rando OJ (2010) The role of nucleosome positioning in the evolution of gene regulation. PLoS Biol 8:e1000414
  80. Van Hooser AA, Ouspenski II, Gregson HC, Starr DA, Yen TJ, Goldberg ML, Yokomori K, Earnshaw WC, Sullivan KF, Brinkley BR (2001) Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J Cell Sci 114:3529–3542
  81. Wang H, Dalal Y, Henikoff S, Lindsay S (2008) Single-epitope recognition imaging of native chromatin. Epigenetics Chromatin 1:10
  82. Warburton PE (2004) Chromosomal dynamics of human neocentromere formation. Chromosome Res 12:617–626
  83. Wieland G, Orthaus S, Ohndorf S, Diekmann S, Hemmerich P (2004) Functional complementation of human centromere protein A (CENP-A) by Cse4p from Saccharomyces cerevisiae. Mol Cell Biol 24:6620–6630
  84. Xiao H, Mizuguchi G, Wisniewski J, Huang Y, Wei D, Wu C (2011) Nonhistone Scm3 binds to AT-Rich DNA to organize atypical centromeric nucleosome of budding yeast. Mol Cell 43:369–380
  85. Yoda K, Ando S, Morishita S, Houmura K, Hashimoto K, Takeyasu K, Okazaki T (2000) Human centromere protein A (CENP-A) can replace histone 3 in nucleosome reconstitution in vitro. Proc Natl Acad Sci USA 97:7266–7271
  86. Yu HG, Hiatt EN, Chan A, Sweeney M, Dawe RK (1997) Neocentromere-mediated chromosome movement in maize. J Cell Biol 139:831–840
  87. Yuen KW, Nabeshima K, Oegema K, Desai A (2011) Rapid de novo centromere formation occurs independently of heterochromatin protein 1 in C. elegans embryos. Curr Biol 21:1800–1807
  88. Zhang W, Colmenares SU, Karpen GH (2012) Assembly of Drosophila centromeric nucleosomes requires CID dimerization. Mol Cell 45:263–269
• 作者单位：1. Howard Hughes Medical Institute and Basic Sciences Division, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, WA 98109-1024, USA
• ISSN：1432-0886

文摘

The centromere is a defining feature of the eukaryotic chromosome, required for attachment to spindle microtubules and segregation to the poles at both mitosis and meiosis. The fundamental unit of centromere identity is the centromere-specific nucleosome, in which the centromeric histone 3 (cenH3) variant takes the place of H3. The structure of the cenH3 nucleosome has been the subject of controversy, as mutually exclusive models have been proposed, including conventional and unconventional left-handed octamers (octasomes), hexamers with non-histone protein constituents, and right-handed heterotypic tetramers (hemisomes). Hemisomes have been isolated from native centromeric chromatin, but traditional nucleosome assembly protocols have generally yielded partially unwrapped left-handed octameric nucleosomes. In budding yeast, topology analysis and high-resolution mapping has revealed that a single right-handed cenH3 hemisome occupies the ~80-bp Centromere DNA Element II (CDEII) of each chromosome. Overproduction of cenH3 leads to promiscuous low-level incorporation of octasome-sized particles throughout the yeast genome. We propose that the right-handed cenH3 hemisome is the universal unit of centromeric chromatin, and that the inherent instability of partially unwrapped left-handed cenH3 octamers is an adaptation to prevent formation of neocentromeres on chromosome arms.