A unique chromatin complex occupies young a-satellite arrays of human centromeres

Science Advances

Volumn 1, Issue 1, 2015, Pages

  Henikoff, Jorja G ^a   Thakur, Jitendra ^a,b   Kasinathan, Sivakanthan ^a,c   Henikoff, Steven ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SATELLITES;

CHROMATIN IMMUNOPRECIPITATION; HIGH RESOLUTION; HIGHER-ORDER; NUCLEOSOMES; PRECISE POSITIONING; SEQUENCE DATA; TANDEM REPEATS;

CHROMOSOMES;

EID: 84929498966     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1400234     Document Type: Article

References (47)

1. I. Alexandrov, A. Kazakov, I Tumeneva, V. Shepelev, Y. Yurov, Alpha-satellite DNA of primates: Old and new families. Chromosoma 110, 253-266 (2001).
2. D. A. Benson, K. Clark, I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, E. W. Sayers, GenBank. Nucleic Acids Res. 42, D32-D37 (2014).
3. M. G. Schueler, A. W. Higgins, M. K. Rudd, K. Gustashaw, H. F. Willard, Genomic and genetic definition of a functional human centromere. Science 294, 109-115 (2001).
4. K. E. Hayden, E. D. Strome, S. L. Merrett, H.-R. Lee, M. K. Rudd, H. F. Willard, Sequences associated with centromere competency in the human genome. Mol. Cell. Biol. 33, 763-772 (2013).
5. D. P. Melters, K. R. Bradnam, H. A. Young, N. Telis, M. R. May, J. G. Ruby, R. Sebra, P. Peluso, J. Eid, D. Rank, J. F. Garcia, J. L. DeRisi, T. Smith, C. Tobias, J. Ross-Ibarra, I. Korf, S. W. L. Chan, Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol. 14, R10 (2013).
6. G. P. Smith, Evolution of repeated DNA sequences by unequal crossover. Science 191, 528-535 (1976).
7. S. Henikoff, K. Ahmad, H. S. Malik, The centromere paradox: Stable inheritance with rapidly evolving DNA. Science 293, 1098-1102 (2001).
8. K. Krassovsky, J. G. Henikoff, S. Henikoff, Tripartite organization of centromeric chromatin in budding yeast. Proc. Natl. Acad. Sci. U.S.A. 109, 243-248 (2012).
9. S. Levy, G. Sutton, P. C. Ng, L. Feuk, A. L. Halpern, B. P. Walenz, N. Axelrod, J. Huang, E. F. Kirkness, G. Denisov, Y. Lin, J. R. MacDonald, A. W. Pang, M. Shago, T. B. Stockwell, A. Tsiamouri, V. Bafna, V. Bansal, S. A. Kravitz, D. A. Busam, K. Y. Beeson, T. C. McIntosh, K. A. Remington, J. F. Abril, J. Gill, J. Borman, Y. H. Rogers, M. E. Frazier, S. W. Scherer, R. L. Strausberg, J. C. Venter, The diploid genome sequence of an individual human. PLOS Biol. 5, e254 (2007).
10. R. B. Slee, C. M. Steiner, B. S. Herbert, G. H. Vance, R. J. Hickey, T. Schwarz, S. Christan, M. Radovich, B. P. Schneider, D. Schindelhauer, B. R. Grimes, Cancer-associated alteration of pericentromeric heterochromatin may contribute to chromosome instability. Oncogene 31, 3244-3253 (2012).
11. D. Hasson, T. Panchenko, K. J. Salimian, M. U. Salman, N. Sekulic, A. Alonso, P. E. Warburton, B. E. Black, The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat. Struct. Mol. Biol. 20, 687-695 (2013).
12. N. Lacoste, A. Woolfe, H. Tachiwana, A. V. Garea, T. Barth, S. Cantaloube, H. Kurumizaka, A. Imhof, G. Almouzni, Mislocalization of the centromeric histone variant CenH3/CENP-A in human cells depends on the chaperone DAXX. Mol. Cell 53, 631-644 (2014).
13. S. F. Altschul, W. Gish, W. Miller, E. W. Myers, D. J. Lipman, Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).
14. A. Baldini, D. I. Smith, M. Rocchi, O. J. Miller, D. A. Miller, A human alphoid DNA clone from the EcoRI dimeric family: Genomic and internal organization and chromosomal assignment. Genomics 5, 822-828 (1989).
15. J. S. Waye, H. F. Willard, Human beta satellite DNA: Genomic organization and sequence definition of a class of highly repetitive tandem DNA. Chromosoma 97, 6250-6254 (1989).
16. H. Masumoto, H. Masukata, Y. Muro, N. Nozaki, T. Okazaki, 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 (1989).
17. M. J. P. Chaisson, J. Huddleston,M. Y.Dennis, P. H. Sudmant,M. Malig, F. Hormozdiari, F. Antonacci, U. Surti, R. Sandstrom, M. Boitano, J. M. Landolin, J. A. Stamatoyannopoulos, M. W. Hunkapiller, J. Korlach, E. E. Eichler, Resolving the complexity of the human genome using single-molecule sequencing. Nature (2014).
18. S. Koren, M. C. Schatz, B. P. Walenz, J. Martin, J. T. Howard, G. Ganapathy, Z. Wang, D. A. Rasko, W. R. McCombie, E. D. Jarvis, A. M Phillippy, Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat. Biotechnol. 30, 693-700 (2012).
19. D. L. Bodor, J. F. Mata, M. Sergeev, A. F. David, K. J. Salimian, T. Panchenko, T. W. Cleveland, B. E. Black, J. V. Shah, L. E. Jansen, The quantitative architecture of centromeric chromatin. eLife 3, e02137 (2014).
20. Y. Arimura, K. Shirayama, N. Horikoshi, R. Fujita, H. Taguchi, W. Kagawa, T. Fukagawa, G. Almouzni, H. Kurumizaka, Crystal structure and stable property of the cancer-associated heterotypic nucleosome containing CENP-A and H3.3. Sci. Rep. 4, 7115 (2014).
21. M. G. Schueler, W. Swanson, P. J. Thomas, E. D. Grxeen, Adaptive evolution of foundation kinetochore proteins in primates. Mol. Biol. Evol. 27, 1585-1597 (2010).
22. G. M. Greig, S. B. England, H. M. Bedford, H. F. Willard, Chromosome-specific alpha satellite DNA from the centromere of human chromosome 16. Am. J. Hum. Genet. 45, 862-872 (1989).
23. M. Plohl, N. Mestrovic, B. Mravinac, Centromere identity from the DNA point of view. Chromosoma 123, 313-325 (2014).
24. L. Mateo, J. Gonzalez, Pogo-like transposases have been repeatedly domesticated into CENP-B-related proteins. Genome Biol. Evol. 6, 2008-2016 (2014).
25. P. E. Warburton, J. S. Waye, H. F. Willard, 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, 6520-6529 (1993).
26. P. B. Talbert, S. Henikoff, Environmental responses mediated by histone variants. Trends Cell Biol. 24, 642-650 (2014).
27. J. D. Brown, R. J. O'Neill, Chromosomes, conflict, and epigenetics: Chromosomal speciation revisited. Annu. Rev. Genomics Hum. Genet. 11, 291-316 (2010).
28. H. S. Malik, S. Henikoff, Major evolutionary transitions in centromere complexity. Cell 138, 1067-1082 (2009).
29. L. Chmátal, S. I. Gabriel, G. P. Mitsainas, J. Martínez-Vargas, J. Ventura, J. B. Searle, R. M. Schultz, M. A. Lampson, Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Curr. Biol. 24, 2295-2300 (2014).
30. T. Zhang, P. B. Talbert, W. Zhang, Y. Wu, Z. Yang, J. G. Henikoff, S. Henikoff, J. Jiang, The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres. Proc. Natl. Acad. Sci. U.S.A. 110, E4875-E4883 (2013).
31. H. Tachiwana, W. Kagawa, T. Shiga, A. Osakabe, Y. Miya, K. Saito, Y. Hayashi-Takanaka, T. Oda, M. Sato, S. Y. Park, H. Kimura, H. Kurumizaka, Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 476, 7115 (2011).
32. F. A. Steiner, S. Henikoff, Holocentromeres are dispersed point centromeres localized at transcription factor hotspots. eLife 3, e02025 (2014).
33. S. Henikoff, S. Ramachandran, K. Krassovsky, T. D. Bryson, C. A. Codomo, K. Brogaard, J. Widom, J. P. Wang, J. G. Henikoff, The budding yeast Centromere DNA Element II wraps a stable Cse4 hemisome in either orientation in vivo. eLife 3, e01861 (2014).
34. L. Clarke, J. Carbon, Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287, 504-509 (1980).
35. K. A. Maloney, L. L. Sullivan, J. E. Matheny, E. D. Strome, S. L. Merrett, A. Ferris, B. A. Sullivan, Functional epialleles at an endogenous human centromere. Proc. Natl. Acad. Sci. U.S.A. 109, 13704-13709 (2012).
36. J. J. Harrington, G. Van Bokkelen, R. W. Mays, K. Gustashaw, H. F. Willard, Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat. Genet. 15, 345-355 (1997).
37. M. Kapoor, R. Montes de Oca Luna, G. Liu, G. Lozano, C. Cummings, M. Mancini, I. Ouspenski, B. R. Brinkley, G. S. May, The cenpB gene is not essential in mice. Chromosoma 107, 570-576 (1998).
38. T. Okada, J. Ohzeki, M. Nakano, K. Yoda, W. R. Brinkley, V. Larionov, H. Masumoto, CENP-B controls centromere formation depending on the chromatin context. Cell 131, 1287-1300 (2007).
39. J. Ohzeki, M. Nakano, T. Okada, H. Masumoto, CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J. Cell Biol. 159, 765-775 (2002).
40. J. G. Henikoff, J. A. Belsky, K. Krassovsky, D. M. Macalpine, S. Henikoff, Epigenome characterization at single base-pair resolution. Proc. Natl. Acad. Sci. U.S.A. 108, 18318-18323 (2011).
41. W. Li, A. Godzik, Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658-1659 (2006).
42. L. Fu, B. Niu, Z. Zhu, S. Wu, W. Li, Cd-hit: Accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150-3152 (2012).
43. H. Li, R. Durbin, Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
44. K. Katoh, D. M. Standley, MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772-780 (2013).
45. N. Saitou, M. Nei, The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425 (1987).
46. H. Thorvaldsdottir, J. T. Robinson, J. P. Mesirov, Integrative Genomics Viewer (IGV): Highperformance genomics data visualization and exploration. Brief Bioinform. 14, 178-192 (2013).
47. S. Henikoff, Near the edge of a chromosome's "black hole." Trends Genet. 18, 165-167 (2002).