Chromosome Research

, Volume 26, Issue 3, pp 115–138 | Cite as

Alpha satellite DNA biology: finding function in the recesses of the genome

  • Shannon M. McNulty
  • Beth A. SullivanEmail author
Waldeyer-Flemming Special Collection


Repetitive DNA, formerly referred to by the misnomer “junk DNA,” comprises a majority of the human genome. One class of this DNA, alpha satellite, comprises up to 10% of the genome. Alpha satellite is enriched at all human centromere regions and is competent for de novo centromere assembly. Because of the highly repetitive nature of alpha satellite, it has been difficult to achieve genome assemblies at centromeres using traditional next-generation sequencing approaches, and thus, centromeres represent gaps in the current human genome assembly. Moreover, alpha satellite DNA is transcribed into repetitive noncoding RNA and contributes to a large portion of the transcriptome. Recent efforts to characterize these transcripts and their function have uncovered pivotal roles for satellite RNA in genome stability, including silencing “selfish” DNA elements and recruiting centromere and kinetochore proteins. This review will describe the genomic and epigenetic features of alpha satellite DNA, discuss recent findings of noncoding transcripts produced from distinct alpha satellite arrays, and address current progress in the functional understanding of this oft-neglected repetitive sequence. We will discuss unique challenges of studying human satellite DNAs and RNAs and point toward new technologies that will continue to advance our understanding of this largely untapped portion of the genome.


satellite centromere kinetochore variation transcription noncoding RNA repetitive DNA epiallele 



Antisense oligonucleotide


Base pair


CRISPR-associated protein 9


Centromere protein


Chromatin immunoprecipitation


Nuclease-deficient Cas9


Deoxyribonucleic acid


Double-stranded RNA


Green fluorescent protein


Human artificial chromosome


Holliday Junction Recognition Protein


Higher-order repeat


Heterochromatin protein 1


Homo sapiens






Krüppel-associated box




Ribonucleic acid


RNA polymerase


Short hairpin RNA


Transfer RNA


Virus protein 16



We thank Megan Aldrup-Macdonald for data contributing to Fig. 3 and Karen Miga (University of California, Santa Cruz) for helpful discussions and sharing data prior to publication.

Author contribution

SMM and BAS conceived and jointly wrote the manuscript.

Funding information

Our research is supported by the National Science Foundation Graduate Research Fellowship DGE-1644868 (S.M.M.) and the National Institutes of Health grant R01 GM124041 (B.A.S.).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Aagaard L, Laible G, Selenko P, Schmid M, Dorn R, Schotta G, Kuhfittig S, Wolf A, Lebersorger A, Singh PB, Reuter G, Jenuwein T (1999) Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J 18:1923–1938PubMedPubMedCentralCrossRefGoogle Scholar
  2. Aagaard L, Schmid M, Warburton P, Jenuwein T (2000) Mitotic phosphorylation of SUV39H1, a novel component of active centromeres, coincides with transient accumulation at mammalian centromeres. J Cell Sci 113(Pt 5):817–829PubMedGoogle Scholar
  3. Aldrup-MacDonald ME, Kuo ME, Sullivan LL, Chew K, Sullivan BA (2016) Genomic variation within alpha satellite DNA influences centromere location on human chromosomes with metastable epiallelesGoogle Scholar
  4. Alexandrov I, Kazakov A, Tumeneva I, Shepelev V, Yurov Y (2001) Alpha-satellite DNA of primates: old and new families. Chromosoma 110:253–266PubMedCrossRefGoogle Scholar
  5. Alexandrov IA, Mashkova TD, Akopian TA, Medvedev LI, Kisselev LL, Mitkevich SP, Yurov YB (1991) Chromosome-specific alpha satellites: two distinct families on human chromosome 18. Genomics 11:15–23PubMedCrossRefGoogle Scholar
  6. Alexandrov IA, Mashkova TD, Romanova LY, Yurov YB, Kisselev LL (1993a) Segment substitutions in alpha satellite DNA. Unusual structure of human chromosome 3-specific alpha satellite repeat unit. J Mol Biol 231:516–520PubMedCrossRefGoogle Scholar
  7. Alexandrov IA, Medvedev LI, Mashkova TD, Kisselev LL, Romanova LY, Yurov YB (1993b) Definition of a new alpha satellite suprachromosomal family characterized by monomeric organization. Nucleic Acids Res 21:2209–2215PubMedPubMedCentralCrossRefGoogle Scholar
  8. Alexandrov IA, Mitkevich SP, Yurov YB (1988) The phylogeny of human chromosome specific alpha satellites. Chromosoma 96:443–453PubMedCrossRefGoogle Scholar
  9. Ando S, Yang H, Nozaki N, Okazaki T, Yoda K (2002) CENP-A, -B, and -C chromatin complex that contains the I-type alpha-satellite array constitutes the prekinetochore in HeLa cells. Mol Cell Biol 22:2229–2241PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bailey AO, Panchenko T, Shabanowitz J, Lehman SM, Bai DL, Hunt DF, Black BE, Foltz DR (2016) Identification of the post-translational modifications present in centromeric chromatin. Mol Cell Proteomics 15:918–931PubMedCrossRefGoogle Scholar
  11. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120–124PubMedCrossRefGoogle Scholar
  12. Bergmann JH, Martins NM, Larionov V, Masumoto H, Earnshaw WC (2012) HACking the centromere chromatin code: insights from human artificial chromosomes. Chromosom Res 20:505–519CrossRefGoogle Scholar
  13. Bergmann JH, Rodriguez MG, Martins NM, Kimura H, Kelly DA, Masumoto H, Larionov V, Jansen LE, Earnshaw WC (2011) Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 30:328–340PubMedCrossRefGoogle Scholar
  14. Blower MD, Sullivan BA, Karpen GH (2002) Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2:319–330PubMedPubMedCentralCrossRefGoogle Scholar
  15. 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 24:923–932PubMedPubMedCentralCrossRefGoogle Scholar
  16. Britten RJ, Kohne DE (1968) Repeated sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science (New York, NY) 161:529–540CrossRefGoogle Scholar
  17. Brown KE, Barnett MA, Burgtorf C, Shaw P, Buckle VJ, Brown WR (1994) Dissecting the centromere of the human Y chromosome with cloned telomeric DNA. Hum Mol Genet 3:1227–1237PubMedCrossRefGoogle Scholar
  18. Canzio D, Chang EY, Shankar S, Kuchenbecker KM, Simon MD, Madhani HD, Narlikar GJ, Al-Sady B (2011) Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly. Mol Cell 41:67–81PubMedPubMedCentralCrossRefGoogle Scholar
  19. Cao S, Zhou K, Zhang Z, Luger K, Straight AF (2018) Constitutive centromere-associated network contacts confer differential stability on CENP-A nucleosomes in vitro and in the cell. Mol Biol Cell 29:751–762PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cardinale S, Bergmann JH, Kelly D, Nakano M, Valdivia MM, Kimura H, Masumoto H, Larionov V, Earnshaw WC (2009) Hierarchical inactivation of a synthetic human kinetochore by a chromatin modifier. Mol Biol Cell 20:4194–4204PubMedPubMedCentralCrossRefGoogle Scholar
  21. 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 11:896–902PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chan DYL, Moralli D, Khoja S, Monaco ZL (2017) Noncoding centromeric RNA expression impairs chromosome stability in human and murine stem cells. Dis Markers 2017:7506976PubMedPubMedCentralCrossRefGoogle Scholar
  23. Chan FL, Marshall OJ, Saffery R, Kim BW, Earle E, Choo KH, Wong LH (2012) Active transcription and essential role of RNA polymerase II at the centromere during mitosis. Proc Natl Acad Sci U S A 109:1979–1984PubMedPubMedCentralCrossRefGoogle Scholar
  24. Charlieu JP, Murgue B, Laurent AM, Marcais B, Bellis M, Roizes G (1992) Discrimination between alpha-satellite DNA sequences from chromosomes 21 and 13 by using polymerase chain reaction. Genomics 14:515–516PubMedCrossRefGoogle Scholar
  25. Choo KH, Earle E, Vissel B, Filby RG (1990) Identification of two distinct subfamilies of alpha satellite DNA that are highly specific for human chromosome 15. Genomics 7:143–151PubMedCrossRefGoogle Scholar
  26. Denegri M, Moralli D, Rocchi M, Biggiogera M, Raimondi E, Cobianchi F, De Carli L, Riva S, Biamonti G (2002) Human chromosomes 9, 12, and 15 contain the nucleation sites of stress-induced nuclear bodies. Mol Biol Cell 13:2069–2079PubMedPubMedCentralCrossRefGoogle Scholar
  27. Devilee P, Cremer T, Slagboom P, Bakker E, Scholl HP, Hager HD, Stevenson AF, Cornelisse CJ, Pearson PL (1986) Two subsets of human alphoid repetitive DNA show distinct preferential localization in the pericentric regions of chromosomes 13, 18, and 21. Cytogenet Cell Genet 41:193–201PubMedCrossRefGoogle Scholar
  28. Du Y, Topp CN, Dawe RK (2010) DNA binding of centromere protein C (CENPC) is stabilized by single-stranded RNA. PLoS Genet 6:e1000835PubMedPubMedCentralCrossRefGoogle Scholar
  29. 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 137:485–497PubMedCrossRefGoogle Scholar
  30. Durfy SJ, Willard HF (1987) Molecular analysis of a polymorphic domain of alpha satellite from the human X chromosome. Am J Hum Genet 41:391–401PubMedPubMedCentralGoogle Scholar
  31. Earnshaw WC, Ratrie H 3rd, Stetten G (1989) Visualization of centromere proteins CENP-B and CENP-C on a stable dicentric chromosome in cytological spreads. Chromosoma 98:1–12PubMedCrossRefGoogle Scholar
  32. Earnshaw WC, Rothfield N (1985) Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91:313–321PubMedCrossRefGoogle Scholar
  33. Eymery A, Horard B, El Atifi-Borel M, Fourel G, Berger F, Vitte AL, Van den Broeck A, Brambilla E, Fournier A, Callanan M, Gazzeri S, Khochbin S, Rousseaux S, Gilson E, Vourc'h C (2009) A transcriptomic analysis of human centromeric and pericentric sequences in normal and tumor cells. Nucleic Acids Res 37:6340–6354PubMedPubMedCentralCrossRefGoogle Scholar
  34. Fachinetti D, Folco HD, Nechemia-Arbely Y, Valente LP, Nguyen K, Wong AJ, Zhu Q, Holland AJ, Desai A, Jansen LE, Cleveland DW (2013) A two-step mechanism for epigenetic specification of centromere identity and function. Nat Cell Biol 15:1056–1066PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fachinetti D, Han JS, McMahon MA, Ly P, Abdullah A, Wong AJ, Cleveland DW (2015) DNA sequence-specific binding of CENP-B enhances the fidelity of human centromere function. Dev Cell 33:314–327PubMedPubMedCentralCrossRefGoogle Scholar
  36. Farr CJ, Bayne RA, Kipling D, Mills W, Critcher R, Cooke HJ (1995) Generation of a human X-derived minichromosome using telomere-associated chromosome fragmentation. EMBO J 14:5444–5454PubMedPubMedCentralCrossRefGoogle Scholar
  37. Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T (2003) The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 278:4035–4040PubMedCrossRefGoogle Scholar
  38. Ge Y, Wagner MJ, Siciliano M, Wells DE (1992) Sequence, higher order repeat structure, and long-range organization of alpha satellite DNA specific to human chromosome 8. Genomics 13:585–593PubMedCrossRefGoogle Scholar
  39. Greig GM, Warburton PE, Willard HF (1993) Organization and evolution of an alpha satellite DNA subset shared by human chromosomes 13 and 21. J Mol Evol 37:464–475PubMedCrossRefGoogle Scholar
  40. Guo LY, Allu PK, Zandarashvili L, McKinley KL, Sekulic N, Dawicki-McKenna JM, Fachinetti D, Logsdon GA, Jamiolkowski RM, Cleveland DW, Cheeseman IM, Black BE (2017) Centromeres are maintained by fastening CENP-A to DNA and directing an arginine anchor-dependent nucleosome transition. Nat Commun 8:15775PubMedPubMedCentralCrossRefGoogle Scholar
  41. Haaf T, Warburton PE, Willard HF (1992) Integration of human alpha-satellite DNA into simian chromosomes: centromere protein binding and disruption of normal chromosome segregation. Cell 70:681–696PubMedCrossRefGoogle Scholar
  42. Haaf T, Ward DC (1994) Structural analysis of alpha-satellite DNA and centromere proteins using extended chromatin and chromosomes. Hum Mol Genet 3:697–709PubMedCrossRefGoogle Scholar
  43. Hall LL, Byron M, Carone DM, Whitfield TW, Pouliot GP, Fischer A, Jones P, Lawrence JB (2017) Demethylated HSATII DNA and HSATII RNA foci sequester PRC1 and MeCP2 into cancer-specific nuclear bodies. Cell Rep 18:2943–2956PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hall LL, Carone DM, Gomez AV, Kolpa HJ, Byron M, Mehta N, Fackelmayer FO, Lawrence JB (2014) Stable C0T-1 repeat RNA is abundant and is associated with euchromatic interphase chromosomes. Cell 156:907–919PubMedPubMedCentralCrossRefGoogle Scholar
  45. 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 15:345–355PubMedCrossRefGoogle Scholar
  46. Hasson D, Panchenko T, Salimian KJ, Salman MU, Sekulic N, Alonso A, Warburton PE, Black BE (2013) The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat Struct Mol Biol 20:687–695PubMedPubMedCentralCrossRefGoogle Scholar
  47. Hayden KE, Strome ED, Merrett SL, Lee HR, Rudd MK, Willard HF (2013) Sequences associated with centromere competency in the human genome. Mol Cell Biol 33:763–772PubMedPubMedCentralCrossRefGoogle Scholar
  48. Ideue T, Cho Y, Nishimura K, Tani T (2014) Involvement of satellite I noncoding RNA in regulation of chromosome segregation. Genes Cells 19:528–538PubMedCrossRefGoogle Scholar
  49. Ikeno M, Grimes B, Okazaki T, Nakano M, Saitoh K, Hoshino H, McGill NI, Cooke H, Masumoto H (1998) Construction of YAC-based mammalian artificial chromosomes. Nat Biotechnol 16:431–439PubMedCrossRefGoogle Scholar
  50. Ikeno M, Masumoto H, Okazaki T (1994) Distribution of CENP-B boxes reflected in CREST centromere antigenic sites on long-range alpha-satellite DNA arrays of human chromosome 21. Hum Mol Genet 3:1245–1257PubMedCrossRefGoogle Scholar
  51. Jain M, Olsen HE, Turner DJ, Stoddart D, Bulazel KV, Paten B, Haussler D, Willard HF, Akeson M, Miga KH (2018) Linear assembly of a human centromere on the Y chromosome. Nat Biotechnol 36:321–323PubMedCrossRefPubMedCentralGoogle Scholar
  52. Jansen LE, Black BE, Foltz DR, Cleveland DW (2007) Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176:795–805PubMedPubMedCentralCrossRefGoogle Scholar
  53. Johnson WL, Yewdell WT, Bell JC, McNulty SM, Duda Z, O’Neill RJ, Sullivan BA, Straight AF (2017) RNA-dependent stabilization of SUV39H1 at constitutive heterochromatin. eLife 6Google Scholar
  54. Jolly C, Metz A, Govin J, Vigneron M, Turner BM, Khochbin S, Vourc'h C (2004) Stress-induced transcription of satellite III repeats. J Cell Biol 164:25–33PubMedPubMedCentralCrossRefGoogle Scholar
  55. Jorgensen AL, Kolvraa S, Jones C, Bak AL (1988) A subfamily of alphoid repetitive DNA shared by the NOR-bearing human chromosomes 14 and 22. Genomics 3:100–109PubMedCrossRefGoogle Scholar
  56. Kim JH, Ebersole T, Kouprina N, Noskov VN, Ohzeki J, Masumoto H, Mravinac B, Sullivan BA, Pavlicek A, Dovat S, Pack SD, Kwon YW, Flanagan PT, Loukinov D, Lobanenkov V, Larionov V (2009) Human gamma-satellite DNA maintains open chromatin structure and protects a transgene from epigenetic silencing. Genome Res 19:533–544PubMedPubMedCentralCrossRefGoogle Scholar
  57. Klein SJ, O’Neill RJ (2018) Transposable elements: genome innovation, chromosome diversity, and centromere conflict. Chromosom Res 26:5–23CrossRefGoogle Scholar
  58. Kononenko AV, Lee NC, Earnshaw WC, Kouprina N, Larionov V (2013) Re-engineering an alphoid(tetO)-HAC-based vector to enable high-throughput analyses of gene function. Nucleic Acids Res 41:e107PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kornberg RD (1974) Chromatin structure: a repeating unit of histones and DNA. Science (New York, NY) 184:868–871CrossRefGoogle Scholar
  60. Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116–120PubMedCrossRefGoogle Scholar
  61. Lam AL, Boivin CD, Bonney CF, Rudd MK, Sullivan BA (2006) Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA. Proc Natl Acad Sci U S A 103:4186–4191PubMedPubMedCentralCrossRefGoogle Scholar
  62. Lee HS, Lee NC, Grimes BR, Samoshkin A, Kononenko AV, Bansal R, Masumoto H, Earnshaw WC, Kouprina N, Larionov V (2013a) A new assay for measuring chromosome instability (CIN) and identification of drugs that elevate CIN in cancer cells. BMC Cancer 13:252PubMedPubMedCentralCrossRefGoogle Scholar
  63. Lee NC, Kononenko AV, Lee HS, Tolkunova EN, Liskovykh MA, Masumoto H, Earnshaw WC, Tomilin AN, Larionov V, Kouprina N (2013b) Protecting a transgene expression from the HAC-based vector by different chromatin insulators. Cell Mol Life Sci 70:3723–3737PubMedPubMedCentralCrossRefGoogle Scholar
  64. Liu H, Qu Q, Warrington R, Rice A, Cheng N, Yu H (2015) Mitotic transcription installs Sgo1 at centromeres to coordinate chromosome segregation. Mol Cell 59:426–436PubMedCrossRefGoogle Scholar
  65. Looijenga LH, Oosterhuis JW, Smit VT, Wessels JW, Mollevanger P, Devilee P (1992) Alpha satellite DNAs on chromosomes 10 and 12 are both members of the dimeric suprachromosomal subfamily, but display little identity at the nucleotide sequence level. Genomics 13:1125–1132PubMedCrossRefGoogle Scholar
  66. Mahtani MM, Willard HF (1990) Pulsed-field gel analysis of alpha-satellite DNA at the human X chromosome centromere: high-frequency polymorphisms and array size estimate. Genomics 7:607–613PubMedCrossRefGoogle Scholar
  67. Mahtani MM, Willard HF (1998) Physical and genetic mapping of the human X chromosome centromere: repression of recombination. Genome Res 8:100–110PubMedCrossRefGoogle Scholar
  68. Maison C, Bailly D, Peters AH, Quivy JP, Roche D, Taddei A, Lachner M, Jenuwein T, Almouzni G (2002) Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet 30:329–334PubMedCrossRefGoogle Scholar
  69. Maison C, Bailly D, Roche D, Montes de Oca R, Probst AV, Vassias I, Dingli F, Lombard B, Loew D, Quivy JP, Almouzni G (2011) SUMOylation promotes de novo targeting of HP1alpha to pericentric heterochromatin. Nat Genet 43:220–227PubMedCrossRefGoogle Scholar
  70. Maloney KA, Sullivan LL, Matheny JE, Strome ED, Merrett SL, Ferris A, Sullivan BA (2012) Functional epialleles at an endogenous human centromere. Proc Natl Acad Sci U S A 109:13704–13709PubMedPubMedCentralCrossRefGoogle Scholar
  71. Manuelidis L (1978) Chromosomal localization of complex and simple repeated human DNAs. Chromosoma 66:23–32PubMedCrossRefGoogle Scholar
  72. Marcais B, Bellis M, Gerard A, Pages M, Boublik Y, Roizes G (1991) Structural organization and polymorphism of the alpha satellite DNA sequences of chromosomes 13 and 21 as revealed by pulse field gel electrophoresis. Hum Genet 86:311–316PubMedGoogle Scholar
  73. Marcais B, Laurent AM, Charlieu JP, Roizes G (1993) Organization of the variant domains of alpha satellite DNA on human chromosome 21. J Mol Evol 37:171–178PubMedCrossRefGoogle Scholar
  74. Masumoto H, Ikeno M, Nakano M, Okazaki T, Grimes B, Cooke H, Suzuki N (1998) Assay of centromere function using a human artificial chromosome. Chromosoma 107:406–416PubMedCrossRefGoogle Scholar
  75. Masumoto H, Masukata H, Muro Y, Nozaki N, Okazaki T (1989) A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite. J Cell Biol 109:1963–1973PubMedCrossRefGoogle Scholar
  76. McNulty SM, Sullivan LL, Sullivan BA (2017) Human centromeres produce chromosome-specific and array-specific alpha satellite transcripts that are complexed with CENP-A and CENP-C. Dev Cell 42:226–240.e226PubMedPubMedCentralCrossRefGoogle Scholar
  77. Metz A, Soret J, Vourc'h C, Tazi J, Jolly C (2004) A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules. J Cell Sci 117:4551–4558PubMedCrossRefGoogle Scholar
  78. Miga KH (2015) Completing the human genome: the progress and challenge of satellite DNA assembly. Chromosom Res 23:421–426CrossRefGoogle Scholar
  79. Miga KH, Newton Y, Jain M, Altemose N, Willard HF, Kent WJ (2014) Centromere reference models for human chromosomes X and Y satellite arrays. Genome Res 24:697–707PubMedPubMedCentralCrossRefGoogle Scholar
  80. Mills W, Critcher R, Lee C, Farr CJ (1999) Generation of an approximately 2.4 Mb human X centromere-based minichromosome by targeted telomere-associated chromosome fragmentation in DT40. Hum Mol Genet 8:751–761PubMedCrossRefGoogle Scholar
  81. Molina O, Vargiu G, Abad MA, Zhiteneva A, Jeyaprakash AA, Masumoto H, Kouprina N, Larionov V, Earnshaw WC (2016) Epigenetic engineering reveals a balance between histone modifications and transcription in kinetochore maintenance. Nat Commun 7:13334PubMedPubMedCentralCrossRefGoogle Scholar
  82. Moralli D, Jefferson A, Valeria Volpi E, Larin Monaco Z (2013) Comparative study of artificial chromosome centromeres in human and murine cells. Eur J Hum Genet 21:948–956PubMedPubMedCentralCrossRefGoogle Scholar
  83. Mravinac B, Sullivan LL, Reeves JW, Yan CM, Kopf KS, Farr CJ, Schueler MG, Sullivan BA (2009) Histone modifications within the human X centromere region. PLoS One 4:e6602PubMedPubMedCentralCrossRefGoogle Scholar
  84. Muchardt C, Guilleme M, Seeler JS, Trouche D, Dejean A, Yaniv M (2002) Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep 3:975–981PubMedPubMedCentralCrossRefGoogle Scholar
  85. Muro Y, Masumoto H, Yoda K, Nozaki N, Ohashi M, Okazaki T (1992) Centromere protein B assembles human centromeric alpha-satellite DNA at the 17-bp sequence, CENP-B box. J Cell Biol 116:585–596PubMedCrossRefGoogle Scholar
  86. Musacchio A, Desai A (2017) A molecular view of kinetochore assembly and function. Biology (Basel) 6Google Scholar
  87. Nakano M, Cardinale S, Noskov VN, Gassmann R, Vagnarelli P, Kandels-Lewis S, Larionov V, Earnshaw WC, Masumoto H (2008) Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev Cell 14:507–522PubMedPubMedCentralCrossRefGoogle Scholar
  88. Nan X, Campoy FJ, Bird A (1997) MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88:471–481PubMedCrossRefGoogle Scholar
  89. Ohzeki J, Bergmann JH, Kouprina N, Noskov VN, Nakano M, Kimura H, Earnshaw WC, Larionov V, Masumoto H (2012) Breaking the HAC barrier: histone H3K9 acetyl/methyl balance regulates CENP-A assembly. EMBO J 31:2391–2402PubMedPubMedCentralCrossRefGoogle Scholar
  90. Ohzeki J, Nakano M, Okada T, Masumoto H (2002) CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J Cell Biol 159:765–775PubMedPubMedCentralCrossRefGoogle Scholar
  91. Ohzeki J, Shono N, Otake K, Martins NM, Kugou K, Kimura H, Nagase T, Larionov V, Earnshaw WC, Masumoto H (2016) KAT7/HBO1/MYST2 regulates CENP-A chromatin assembly by antagonizing Suv39h1-mediated centromere inactivation. Dev Cell 37:413–427PubMedPubMedCentralCrossRefGoogle Scholar
  92. Okada T, Ohzeki J, Nakano M, Yoda K, Brinkley WR, Larionov V, Masumoto H (2007) CENP-B controls centromere formation depending on the chromatin context. Cell 131:1287–1300PubMedCrossRefGoogle Scholar
  93. 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 U S A 88:3734–3738PubMedPubMedCentralCrossRefGoogle Scholar
  94. Palmer DK, O'Day K, Wener MH, Andrews BS, Margolis RL (1987) A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J Cell Biol 104:805–815PubMedCrossRefGoogle Scholar
  95. Pesenti E, Kouprina N, Liskovykh M, Aurich-Costa J, Larionov V, Masumoto H, Earnshaw WC, Molina O (2018) Generation of a synthetic human chromosome with two centromeric domains for advanced epigenetic engineering studies. ACS Synth Biol 7:1116–1130PubMedPubMedCentralCrossRefGoogle Scholar
  96. Peters AH, Kubicek S, Mechtler K, O'Sullivan RJ, Derijck AA, Perez-Burgos L, Kohlmaier A, Opravil S, Tachibana M, Shinkai Y, Martens JH, Jenuwein T (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 12:1577–1589PubMedCrossRefGoogle Scholar
  97. Peters AH, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323–337PubMedCrossRefGoogle Scholar
  98. Peterson CL, Laniel M-A (2004) Histones and histone modifications. Curr Biol 14:R546–R551PubMedCrossRefGoogle Scholar
  99. Pironon N, Puechberty J, Roizes G (2010) Molecular and evolutionary characteristics of the fraction of human alpha satellite DNA associated with CENP-A at the centromeres of chromosomes 1, 5, 19, and 21. BMC Genomics 11:195PubMedPubMedCentralCrossRefGoogle Scholar
  100. Politi V, Perini G, Trazzi S, Pliss A, Raska I, Earnshaw WC, Della Valle G (2002) CENP-C binds the alpha-satellite DNA in vivo at specific centromere domains. J Cell Sci 115:2317–2327PubMedGoogle Scholar
  101. Quenet D, Dalal Y (2014) A long non-coding RNA is required for targeting centromeric protein A to the human centromere. eLife e03254Google Scholar
  102. Rea S, Eisenhaber F, O’Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593–599PubMedCrossRefGoogle Scholar
  103. Rizzi N, Denegri M, Chiodi I, Corioni M, Valgardsdottir R, Cobianchi F, Riva S, Biamonti G (2004) Transcriptional activation of a constitutive heterochromatic domain of the human genome in response to heat shock. Mol Biol Cell 15:543–551PubMedPubMedCentralCrossRefGoogle Scholar
  104. Rosandic M, Paar V, Basar I, Gluncic M, Pavin N, Pilas I (2006) CENP-B box and pJalpha sequence distribution in human alpha satellite higher-order repeats (HOR). Chromosom Res 14:735–753CrossRefGoogle Scholar
  105. Rosenbloom KR, Armstrong J, Barber GP, Casper J, Clawson H, Diekhans M, Dreszer TR, Fujita PA, Guruvadoo L, Haeussler M, Harte RA, Heitner S, Hickey G, Hinrichs AS, Hubley R, Karolchik D, Learned K, Lee BT, Li CH, Miga KH, Nguyen N, Paten B, Raney BJ, Smit AF, Speir ML, Zweig AS, Haussler D, Kuhn RM, Kent WJ (2015) The UCSC Genome Browser database: 2015 update. Nucleic Acids Res 43:D670–D681PubMedCrossRefGoogle Scholar
  106. Ross JE, Woodlief KS, Sullivan BA (2016) Inheritance of the CENP-A chromatin domain is spatially and temporally constrained at human centromeres. Epigenetics Chromatin 9:20PubMedPubMedCentralCrossRefGoogle Scholar
  107. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP, Frankish A, Lovell FL, Howe KL, Ashurst JL, Fulton RS, Sudbrak R, Wen G, Jones MC, Hurles ME, Andrews TD, Scott CE, Searle S, Ramser J, Whittaker A, Deadman R, Carter NP, Hunt SE, Chen R, Cree A, Gunaratne P, Havlak P, Hodgson A, Metzker ML, Richards S, Scott G, Steffen D, Sodergren E, Wheeler DA, Worley KC, Ainscough R, Ambrose KD, Ansari-Lari MA, Aradhya S, Ashwell RI, Babbage AK, Bagguley CL, Ballabio A, Banerjee R, Barker GE, Barlow KF, Barrett IP, Bates KN, Beare DM, Beasley H, Beasley O, Beck A, Bethel G, Blechschmidt K, Brady N, Bray-Allen S, Bridgeman AM, Brown AJ, Brown MJ, Bonnin D, Bruford EA, Buhay C, Burch P, Burford D, Burgess J, Burrill W, Burton J, Bye JM, Carder C, Carrel L, Chako J, Chapman JC, Chavez D, Chen E, Chen G, Chen Y, Chen Z, Chinault C, Ciccodicola A, Clark SY, Clarke G, Clee CM, Clegg S, Clerc-Blankenburg K, Clifford K, Cobley V, Cole CG, Conquer JS, Corby N, Connor RE, David R, Davies J, Davis C, Davis J, Delgado O, Deshazo D, Dhami P, Ding Y, Dinh H, Dodsworth S, Draper H, Dugan-Rocha S, Dunham A, Dunn M, Durbin KJ, Dutta I, Eades T, Ellwood M, Emery-Cohen A, Errington H, Evans KL, Faulkner L, Francis F, Frankland J, Fraser AE, Galgoczy P, Gilbert J, Gill R, Glockner G, Gregory SG, Gribble S, Griffiths C, Grocock R, Gu Y, Gwilliam R, Hamilton C, Hart EA, Hawes A, Heath PD, Heitmann K, Hennig S, Hernandez J, Hinzmann B, Ho S, Hoffs M, Howden PJ, Huckle EJ, Hume J, Hunt PJ, Hunt AR, Isherwood J, Jacob L, Johnson D, Jones S, de Jong PJ, Joseph SS, Keenan S, Kelly S, Kershaw JK, Khan Z, Kioschis P, Klages S, Knights AJ, Kosiura A, Kovar-Smith C, Laird GK, Langford C, Lawlor S, Leversha M, Lewis L, Liu W, Lloyd C, Lloyd DM, Loulseged H, Loveland JE, Lovell JD, Lozado R, Lu J, Lyne R, Ma J, Maheshwari M, Matthews LH, McDowall J, McLaren S, McMurray A, Meidl P, Meitinger T, Milne S, Miner G, Mistry SL, Morgan M, Morris S, Muller I, Mullikin JC, Nguyen N, Nordsiek G, Nyakatura G, O'Dell CN, Okwuonu G, Palmer S, Pandian R, Parker D, Parrish J, Pasternak S, Patel D, Pearce AV, Pearson DM, Pelan SE, Perez L, Porter KM, Ramsey Y, Reichwald K, Rhodes S, Ridler KA, Schlessinger D, Schueler MG, Sehra HK, Shaw-Smith C, Shen H, Sheridan EM, Shownkeen R, Skuce CD, Smith ML, Sotheran EC, Steingruber HE, Steward CA, Storey R, Swann RM, Swarbreck D, Tabor PE, Taudien S, Taylor T, Teague B, Thomas K, Thorpe A, Timms K, Tracey A, Trevanion S, Tromans AC, d’Urso M, Verduzco D, Villasana D, Waldron L, Wall M, Wang Q, Warren J, Warry GL, Wei X, West A, Whitehead SL, Whiteley MN, Wilkinson JE, Willey DL, Williams G, Williams L, Williamson A, Williamson H, Wilming L, Woodmansey RL, Wray PW, Yen J, Zhang J, Zhou J, Zoghbi H, Zorilla S, Buck D, Reinhardt R, Poustka A, Rosenthal A, Lehrach H, Meindl A, Minx PJ, Hillier LW, Willard HF, Wilson RK, Waterston RH, Rice CM, Vaudin M, Coulson A, Nelson DL, Weinstock G, Sulston JE, Durbin R, Hubbard T, Gibbs RA, Beck S, Rogers J, Bentley DR (2005) The DNA sequence of the human X chromosome. Nature 434:325–337PubMedPubMedCentralCrossRefGoogle Scholar
  108. Rudd MK, Mays RW, Schwartz S, Willard HF (2003a) Human artificial chromosomes with alpha satellite-based de novo centromeres show increased frequency of nondisjunction and anaphase lag. Mol Cell Biol 23:7689–7697PubMedPubMedCentralCrossRefGoogle Scholar
  109. Rudd MK, Schueler MG, Willard HF (2003b) Sequence organization and functional annotation of human centromeres. Cold Spring Harb Symp Quant Biol 68:141–149PubMedCrossRefGoogle Scholar
  110. Schueler MG, Dunn JM, Bird CP, Ross MT, Viggiano L, Program NCS, Rocchi M, Willard HF, Green ED (2005) Progressive proximal expansion of the primate X chromosome centromere. Proc Natl Acad Sci U S A 102:10563–10568PubMedPubMedCentralCrossRefGoogle Scholar
  111. Schueler MG, Higgins AW, Rudd MK, Gustashaw K, Willard HF (2001) Genomic and genetic definition of a functional human centromere. Science (New York, NY) 294:109–115CrossRefGoogle Scholar
  112. Shang WH, Hori T, Westhorpe FG, Godek KM, Toyoda A, Misu S, Monma N, Ikeo K, Carroll CW, Takami Y, Fujiyama A, Kimura H, Straight AF, Fukagawa T (2016) Acetylation of histone H4 lysine 5 and 12 is required for CENP-A deposition into centromeres. Nat Commun 7:13465PubMedPubMedCentralCrossRefGoogle Scholar
  113. Shelby RD, Monier K, Sullivan KF (2000) Chromatin assembly at kinetochores is uncoupled from DNA replication. J Cell Biol 151:1113–1118PubMedPubMedCentralCrossRefGoogle Scholar
  114. Shelby RD, Vafa O, Sullivan KF (1997) Assembly of CENP-A into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites. J Cell Biol 136:501–513PubMedPubMedCentralCrossRefGoogle Scholar
  115. Shepelev VA, Alexandrov AA, Yurov YB, Alexandrov IA (2009) The evolutionary origin of man can be traced in the layers of defunct ancestral alpha satellites flanking the active centromeres of human chromosomes. PLoS Genet 5:e1000641PubMedPubMedCentralCrossRefGoogle Scholar
  116. Shepelev VA, Uralsky LI, Alexandrov AA, Yurov YB, Rogaev EI, Alexandrov IA (2015) Annotation of suprachromosomal families reveals uncommon types of alpha satellite organization in pericentromeric regions of hg38 human genome assembly. Genom Data 5:139–146PubMedPubMedCentralCrossRefGoogle Scholar
  117. Shono N, Ohzeki J, Otake K, Martins NM, Nagase T, Kimura H, Larionov V, Earnshaw WC, Masumoto H (2015) CENP-C and CENP-I are key connecting factors for kinetochore and CENP-A assembly. J Cell Sci 128:4572–4587PubMedPubMedCentralCrossRefGoogle Scholar
  118. Slee RB, Steiner CM, Herbert B-S, Vance GH, Hickey RJ, Schwarz T, Christan S, Radovich M, Schneider BP, Schindelhauer D, Grimes BR (2011) Cancer-associated alteration of pericentromeric heterochromatin may contribute to chromosome instability. Oncogene 31:3244–3253PubMedCrossRefGoogle Scholar
  119. Sullivan BA, Karpen GH (2004) Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat Struct Mol Biol 11:1076–1083PubMedPubMedCentralCrossRefGoogle Scholar
  120. Sullivan BA, Schwartz S (1995) Identification of centromeric antigens in dicentric Robertsonian translocations: CENP-C and CENP-E are necessary components of functional centromeres. Hum Mol Genet 4:2189–2197PubMedCrossRefGoogle Scholar
  121. Sullivan LL, Boivin CD, Mravinac B, Song IY, Sullivan BA (2011) Genomic size of CENP-A domain is proportional to total alpha satellite array size at human centromeres and expands in cancer cells. Chromosom Res 19:457–470CrossRefGoogle Scholar
  122. Sullivan LL, Chew K, Sullivan BA (2017) alpha satellite DNA variation and function of the human centromere. Nucleus (Austin, Tex) 8:331–339Google Scholar
  123. Sullivan LL, Maloney KA, Towers AJ, Gregory SG, Sullivan BA (2016) Human centromere repositioning within euchromatin after partial chromosome deletion. Chromosom Res 24:451–466CrossRefGoogle Scholar
  124. Thakur J, Henikoff S (2018) Unexpected conformational variations of the human centromeric chromatin complex. Genes Dev 32:20–25PubMedPubMedCentralCrossRefGoogle Scholar
  125. Ting DT, Lipson D, Paul S, Brannigan BW, Akhavanfard S, Coffman EJ, Contino G, Deshpande V, Iafrate AJ, Letovsky S, Rivera MN, Bardeesy N, Maheswaran S, Haber DA (2011) Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science (New York, NY) 331:593–596CrossRefGoogle Scholar
  126. Trazzi S, Bernardoni R, Diolaiti D, Politi V, Earnshaw WC, Perini G, Della Valle G (2002) In vivo functional dissection of human inner kinetochore protein CENP-C. J Struct Biol 140:39–48PubMedCrossRefGoogle Scholar
  127. Trowell HE, Nagy A, Vissel B, Choo KH (1993) Long-range analyses of the centromeric regions of human chromosomes 13, 14 and 21: identification of a narrow domain containing two key centromeric DNA elements. Hum Mol Genet 2:1639–1649PubMedCrossRefGoogle Scholar
  128. Vafa O, Sullivan KF (1997) Chromatin containing CENP-A and alpha-satellite DNA is a major component of the inner kinetochore plate. Curr Biol 7:897–900PubMedCrossRefGoogle Scholar
  129. Valgardsdottir R, Chiodi I, Giordano M, Rossi A, Bazzini S, Ghigna C, Riva S, Biamonti G (2008) Transcription of satellite III non-coding RNAs is a general stress response in human cells. Nucleic Acids Res 36:423–434PubMedCrossRefGoogle Scholar
  130. Vissel B, Choo KH (1991) Four distinct alpha satellite subfamilies shared by human chromosomes 13, 14 and 21. Nucleic Acids Res 19:271–277PubMedPubMedCentralCrossRefGoogle Scholar
  131. Vissel B, Choo KH (1992) Evolutionary relationships of multiple alpha satellite subfamilies in the centromeres of human chromosomes 13, 14, and 21. J Mol Evol 35:137–146PubMedCrossRefGoogle Scholar
  132. Warburton PE, Cooke CA, Bourassa S, Vafa O, Sullivan BA, Stetten G, Gimelli G, Warburton D, Tyler-Smith C, Sullivan KF, Poirier GG, Earnshaw WC (1997) Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr Biol 7:901–904PubMedCrossRefGoogle Scholar
  133. Warburton PE, Waye JS, Willard HF (1993) Nonrandom localization of recombination events in human alpha satellite repeat unit variants: implications for higher-order structural characteristics within centromeric heterochromatin. Mol Cell Biol 13:6520–6529PubMedPubMedCentralCrossRefGoogle Scholar
  134. Warburton PE, Willard HF (1992) PCR amplification of tandemly repeated DNA: analysis of intra- and interchromosomal sequence variation and homologous unequal crossing-over in human alpha satellite DNA. Nucleic Acids Res 20:6033–6042PubMedPubMedCentralCrossRefGoogle Scholar
  135. Warburton PE, Willard HF (1995) Interhomologue sequence variation of alpha satellite DNA from human chromosome 17: evidence for concerted evolution along haplotypic lineages. J Mol Evol 41:1006–1015PubMedCrossRefGoogle Scholar
  136. Waye JS, Creeper LA, Willard HF (1987a) Organization and evolution of alpha satellite DNA from human chromosome 11. Chromosoma 95:182–188PubMedCrossRefGoogle Scholar
  137. Waye JS, England SB, Willard HF (1987b) Genomic organization of alpha satellite DNA on human chromosome 7: evidence for two distinct alphoid domains on a single chromosome. Mol Cell Biol 7:349–356PubMedPubMedCentralCrossRefGoogle Scholar
  138. Waye JS, Greig GM, Willard HF (1987c) Detection of novel centromeric polymorphisms associated with alpha satellite DNA from human chromosome 11. Hum Genet 77:151–156PubMedCrossRefGoogle Scholar
  139. Waye JS, Willard HF (1985) Chromosome-specific alpha satellite DNA: nucleotide sequence analysis of the 2.0 kilobasepair repeat from the human X chromosome. Nucleic Acids Res 13:2731–2743PubMedPubMedCentralCrossRefGoogle Scholar
  140. Waye JS, Willard HF (1986a) Molecular analysis of a deletion polymorphism in alpha satellite of human chromosome 17: evidence for homologous unequal crossing-over and subsequent fixation. Nucleic Acids Res 14:6915–6927PubMedPubMedCentralCrossRefGoogle Scholar
  141. Waye JS, Willard HF (1986b) Structure, organization, and sequence of alpha satellite DNA from human chromosome 17: evidence for evolution by unequal crossing-over and an ancestral pentamer repeat shared with the human X chromosome. Mol Cell Biol 6:3156–3165PubMedPubMedCentralCrossRefGoogle Scholar
  142. Waye JS, Willard HF (1987) Nucleotide sequence heterogeneity of alpha satellite repetitive DNA: a survey of alphoid sequences from different human chromosomes. Nucleic Acids Res 15:7549–7569PubMedPubMedCentralCrossRefGoogle Scholar
  143. Wevrick R, Willard HF (1989) Long-range organization of tandem arrays of alpha satellite DNA at the centromeres of human chromosomes: high-frequency array-length polymorphism and meiotic stability. Proc Natl Acad Sci U S A 86:9394–9398PubMedPubMedCentralCrossRefGoogle Scholar
  144. Wevrick R, Willard HF (1991) Physical map of the centromeric region of human chromosome 7: relationship between two distinct alpha satellite arrays. Nucleic Acids Res 19:2295–2301PubMedPubMedCentralCrossRefGoogle Scholar
  145. Willard HF (1985) Chromosome-specific organization of human alpha satellite DNA. Am J Hum Genet 37:524–532PubMedPubMedCentralGoogle Scholar
  146. Willard HF, Skolnick MH, Pearson PL, Mandel JL (1985) Report of the Committee on Human Gene Mapping by recombinant DNA techniques. Cytogenet Cell Genet 40:360–489PubMedCrossRefGoogle Scholar
  147. Willard HF, Waye JS (1987a) Chromosome-specific subsets of human alpha satellite DNA: analysis of sequence divergence within and between chromosomal subsets and evidence for an ancestral pentameric repeat. J Mol Evol 25:207–214PubMedCrossRefGoogle Scholar
  148. Willard HF, Waye JS (1987b) Hierarchical order in chromosome-specific alpha satellite DNA. Trends Genet 3:192–198CrossRefGoogle Scholar
  149. Willard HF, Waye JS, Skolnick MH, Schwartz CE, Powers VE, England SB (1986) Detection of restriction fragment length polymorphisms at the centromeres of human chromosomes by using chromosome-specific alpha satellite DNA probes: implications for development of centromere-based genetic linkage maps. Proc Natl Acad Sci U S A 83:5611–5615PubMedPubMedCentralCrossRefGoogle Scholar
  150. Wong LH, Brettingham-Moore KH, Chan L, Quach JM, Anderson MA, Northrop EL, Hannan R, Saffery R, Shaw ML, Williams E, Choo KH (2007) Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere. Genome Res 17:1146–1160PubMedPubMedCentralCrossRefGoogle Scholar
  151. Wu JC, Manuelidis L (1980) Sequence definition and organization of a human repeated DNA. J Mol Biol 142:363–386PubMedCrossRefGoogle Scholar
  152. Yasmineh WG, Yunis JJ (1974) Localization of repeated DNA sequences in CsC1 gradients by hybridization with complementary RNA. Exp Cell Res 88:340–344PubMedCrossRefGoogle Scholar
  153. Yoda K, Ando S, Okuda A, Kikuchi A, Okazaki T (1998) In vitro assembly of the CENP-B/alpha-satellite DNA/core histone complex: CENP-B causes nucleosome positioning. Genes Cells 3:533–548PubMedCrossRefGoogle Scholar
  154. Zhu Q, Pao GM, Huynh AM, Suh H, Tonnu N, Nederlof PM, Gage FH, Verma IM (2011) BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 477:179–184PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Molecular Genetics and MicrobiologyDuke University Medical CenterDurhamUSA
  2. 2.Division of Human GeneticsDuke University Medical CenterDurhamUSA

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