The past, present, and future of human centromere genomics

Genes

Volumn 5, Issue 1, 2014, Pages 33-50

  Aldrup MacDonald, Megan E ^a,b   Sullivan, Beth A ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alpha satellite; CENP; Chromosome truncation; Dicentric; Heterochromatin; Higher order repeat; Human artificial chromosome; Tet operon; Transcription

Indexed keywords

CENTROMERE PROTEIN A; CENTROMERE PROTEIN B;

BINDING SITE; CELL GENOMICS; CENTROMERE; CHROMOSOME SATELLITE; DNA MICROARRAY; DNA POLYMORPHISM; DNA SEQUENCE; EPIGENETICS; GENE DELETION; GENE LINKAGE DISEQUILIBRIUM; GENE MAPPING; GENOMIC INSTABILITY; GENOMICS; HETEROCHROMATIN; HUMAN; HUMAN ARTIFICIAL CHROMOSOME; MINICHROMOSOME; OPERON; PROTEIN ASSEMBLY; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 84893040699     PISSN: None     EISSN: 20734425     Source Type: Journal    
DOI: 10.3390/genes5010033     Document Type: Review

References (81)

1. Panchenko, T.; Black, B.E. The epigenetic basis for centromere identity. Prog. Mol. Subcell. Biol. 2009, 48, 1-32.
2. Valente, L.P.; Silva, M.C.; Jansen, L.E. Temporal control of epigenetic centromere specification. Chromosome Res. 2012, 20, 481-492.
3. Choo, K.H. Domain organization at the centromere and neocentromere. Dev. Cell 2001, 1, 165-177.
4. Warburton, P.E. Chromosomal dynamics of human neocentromere formation. Chromosome Res. 2004, 12, 617-626.
5. Manuelidis, L.; Wu, J.C. Homology between human and simian repeated DNA. Nature 1978, 276, 92-94.
6. Waye, J.S.; Willard, H.F. Nucleotide sequence heterogeneity of alpha satellite repetitive DNA: A survey of alphoid sequences from different human chromosomes. Nucleic Acids Res. 1987, 15, 7549-7569.
7. Willard, H.F. Chromosome-specific organization of human alpha satellite DNA. Am. J. Hum. Genet. 1985, 37, 524-532.
8. Muro, Y.; Masumoto, H.; Yoda, K.; Nozaki, N.; Ohashi, M.; Okazaki, T. Centromere protein B assembles human centromeric alpha-satellite DNA at the 17-bp sequence, CENP-B box. J. Cell Biol. 1992, 116, 585-596.
9. Schueler, M.G.; Sullivan, B.A. Structural and functional dynamics of human centromeric chromatin. Annu. Rev. Genomics Hum. Genet. 2006, 7, 301-313.
10. Choo, K.H.; Vissel, B.; Nagy, A.; Earle, E.; Kalitsis, P. A survey of the genomic distribution of alpha satellite DNA on all the human chromosomes, and derivation of a new consensus sequence. Nucleic Acids Res. 1991, 19, 1179-1182.
11. Vissel, B.; Choo, K.H. Human alpha satellite DNA-Consensus sequence and conserved regions. Nucleic Acids Res. 1987, 15, 6751-6752.
12. Alexandrov, I.A.; Mitkevich, S.P.; Yurov, Y.B. The phylogeny of human chromosome specific alpha satellites. Chromosoma 1988, 96, 443-453.
13. Alexandrov, I.; Kazakov, A.; Tumeneva, I.; Shepelev, V.; Yurov, Y. Alpha-satellite DNA of primates: Old and new families. Chromosoma 2001, 110, 253-266.
14. Devilee, P.; Kievits, T.; Waye, J.S.; Pearson, P.L.; Willard, H.F. Chromosome-specific alpha satellite DNA: Isolation and mapping of a polymorphic alphoid repeat from human chromosome 10. Genomics 1988, 3, 1-7.
15. Mahtani, M.M.; Willard, H.F. Pulsed-field gel analysis of alpha-satellite DNA at the human X chromosome centromere: High-frequency polymorphisms and array size estimate. Genomics 1990, 7, 607-613.
16. Greig, G.M.; Parikh, S.; George, J.; Powers, V.E.; Willard, H.F. Molecular cytogenetics of alpha satellite DNA from chromosome 12: Fluorescence in situ hybridization and description of DNA and array length polymorphisms. Cytogenet. Cell Genet. 1991, 56, 144-148.
17. Wevrick, R.; Willard, H.F. 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. USA 1989, 86, 9394-9398.
18. Willard, H.F.; Waye, J.S.; Skolnick, M.H.; Schwartz, C.E.; Powers, V.E.; England, S.B. 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. USA 1986, 83, 5611-5615.
19. Abruzzo, M.A.; Griffin, D.K.; Millie, E.A.; Sheean, L.A.; Hassold, T.J. The effect of Y-chromosome alpha-satellite array length on the rate of sex chromosome disomy in human sperm. Hum. Genet. 1996, 97, 819-823.
20. Oakey, R.; Tyler-Smith, C. Y chromosome DNA haplotyping suggests that most European and Asian men are descended from one of two males. Genomics 1990, 7, 325-330.
21. Willard, H.F. Evolution of alpha satellite. Curr. Opin. Genet. Dev. 1991, 1, 509-514.
22. Waye, J.S.; Willard, H.F. 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. 1986, 14, 6915-6927.
23. Waye, J.S.; Willard, H.F. 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. 1986, 6, 3156-3165.
24. Willard, H.F.; Greig, G.M.; Powers, V.E.; Waye, J.S. Molecular organization and haplotype analysis of centromeric DNA from human chromosome 17: Implications for linkage in neurofibromatosis. Genomics 1987, 1, 368-373.
25. Warburton, P.E.; Willard, H.F. Interhomologue sequence variation of alpha satellite DNA from human chromosome 17: Evidence for concerted evolution along haplotypic lineages. J. Mol. Evol. 1995, 41, 1006-1015.
26. Maloney, K.A.; Sullivan, L.L.; Matheny, J.E.; Strome, E.D.; Merrett, S.L.; Ferris, A.; Sullivan, B.A. Functional epialleles at an endogenous human centromere. Proc. Natl. Acad. Sci. USA 2012, 109, 13704-13709.
27. Brown, K.E.; Barnett, M.A.; Burgtorf, C.; Shaw, P.; Buckle, V.J.; Brown, W.R. Dissecting the centromere of the human Y chromosome with cloned telomeric DNA. Hum. Mol. Genet. 1994, 3, 1227-1237.
28. Farr, C.J.; Bayne, R.A.; Kipling, D.; Mills, W.; Critcher, R.; Cooke, H.J. Generation of a human X-derived minichromosome using telomere-associated chromosome fragmentation. EMBO J. 1995, 14, 5444-5454.
29. Harrington, J.J.; van Bokkelen, G.; Mays, R.W.; Gustashaw, K.; Willard, H.F. Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat. Genet. 1997, 15, 345-355.
30. Ikeno, M.; Grimes, B.R.; Okazaki, T.; Nakano, M.; Saitoh, K.; Hoshino, H.; McGill, N.I.; Cooke, H.; Masumoto, H. Construction of YAC-based mammalian artificial chromosomes. Nat. Biotechnol. 1998, 16, 431-439.
31. Grimes, B.R.; Babcock, J.; Rudd, M.K.; Chadwick, B.; Willard, H.F. Assembly and characterization of heterochromatin and euchromatin on human artificial chromosomes. Genome Biol. 2004, 5, R89.
32. Grimes, B.R.; Rhoades, A.A.; Willard, H.F. Alpha-satellite DNA and vector composition influence rates of human artificial chromosome formation. Mol. Ther. 2002, 5, 798-805.
33. Ohzeki, J.; Nakano, M.; Okada, T.; Masumoto, H. CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J. Cell Biol. 2002, 159, 765-775.
34. Haaf, T.; Warburton, P.E.; Willard, H.F. Integration of human alpha-satellite DNA into simian chromosomes: Centromere protein binding and disruption of normal chromosome segregation. Cell 1992, 70, 681-696.
35. Nakashima, H.; Nakano, M.; Ohnishi, R.; Hiraoka, Y.; Kaneda, Y.; Sugino, A.; Masumoto, H. Assembly of additional heterochromatin distinct from centromere-kinetochore chromatin is required for de novo formation of human artificial chromosome. J. Cell Sci. 2005, 118, 5885-5898.
36. Nakano, M.; Cardinale, S.; Noskov, V.N.; Gassmann, R.; Vagnarelli, P.; Kandels-Lewis, S.; Larionov, V.; Earnshaw, W.C.; Masumoto, H. Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev. Cell 2008, 14, 507-522.
37. Bergmann, J.H.; Rodriguez, M.G.; Martins, N.M.; Kimura, H.; Kelly, D.A.; Masumoto, H.; Larionov, V.; Jansen, L.E.; Earnshaw, W.C. Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J. 2011, 30, 328-340.
38. Cardinale, S.; Bergmann, J.H.; Kelly, D.; Nakano, M.; Valdivia, M.M.; Kimura, H.; Masumoto, H.; Larionov, V.; Earnshaw, W.C. Hierarchical inactivation of a synthetic human kinetochore by a chromatin modifier. Mol. Biol. Cell 2009, 20, 4194-4204.
39. Kononenko, A.V.; Lee, N.C.; Earnshaw, W.C.; Kouprina, N.; Larionov, V. Re-engineering an alphoid(tetO)-HAC-based vector to enable high-throughput analyses of gene function. Nucleic Acids Res. 2013, 41, e107.
40. Murphy, T.D.; Karpen, G.H. Centromeres take flight: Alpha satellite and the quest for the human centromere. Cell 1998, 93, 317-320.
41. Henikoff, S. Near the edge of a chromosome's "black hole". Trends Genet. 2002, 18, 165-167.
42. Collins, F.S.; Patrinos, A.; Jordan, E.; Chakravarti, A.; Gesteland, R.; Walters, L. New goals for the U.S. Human Genome Project: 1998-2003. Science 1998, 282, 682-689.
43. Eichler, E.E. Repetitive conundrums of centromere structure and function. Hum. Mol. Genet. 1999, 8, 151-155.
44. Horvath, J.E.; Bailey, J.A.; Locke, D.P.; Eichler, E.E. Lessons from the human genome: Transitions between euchromatin and heterochromatin. Hum. Mol. Genet. 2001, 10, 2215-2223.
45. Horvath, J.E.; Viggiano, L.; Loftus, B.J.; Adams, M.D.; Archidiacono, N.; Rocchi, M.; Eichler, E.E. Molecular structure and evolution of an alpha satellite/non-alpha satellite junction at 16p11. Hum. Mol. Genet. 2000, 9, 113-123.
46. She, X.; Horvath, J.E.; Jiang, Z.; Liu, G.; Furey, T.S.; Christ, L.; Clark, R.; Graves, T.; Gulden, C.L.; Alkan, C., et al. The structure and evolution of centromeric transition regions within the human genome. Nature 2004, 430, 857-864.
47. Hoskins, R.A.; Carlson, J.W.; Kennedy, C.; Acevedo, D.; Evans-Holm, M.; Frise, E.; Wan, K.H.; Park, S.; Mendez-Lago, M.; Rossi, F., et al. Sequence finishing and mapping of Drosophila melanogaster heterochromatin. Science 2007, 316, 1625-1628.
48. Smith, C.D.; Shu, S.; Mungall, C.J.; Karpen, G.H. The Release 5.1 annotation of Drosophila melanogaster heterochromatin. Science 2007, 316, 1586-1591.
49. Kalitsis, P.; Griffiths, B.; Choo, K.H. Mouse telocentric sequences reveal a high rate of homogenization and possible role in Robertsonian translocation. Proc. Natl. Acad. Sci. USA 2006, 103, 8786-8791.
50. Mouse Genome Sequencing Consortium; Waterston, R.H.; Lindblad-Toh, K.; Birney, E.; Rogers, J.; Abril, J.F.; Agarwal, P.; Agarwala, R.; Ainscough, R.; Alexandersson, M.; et al. Initial sequencing and comparative analysis of the mouse genome. Nature 2002, 420, 520-562.
51. Hayden, K.E.; Strome, E.D.; Merrett, S.E.; Lee, H.R.; Rudd, M.K.; Willard, H.F. Sequences associated with centromere competency in the human genome. Mol. Cell. Biol. 2012, 33, 763-772.
52. Melters, D.P.; Bradnam, K.R.; Young, H.A.; Telis, N.; May, M.R.; Ruby, J.G.; Sebra, R.; Peluso, P.; Eid, J.; Rank, D., et al. Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol. 2013, 14, R10.
53. Mahtani, M.M.; Willard, H.F. Physical and genetic mapping of the human X chromosome centromere: Repression of recombination. Genome Res. 1998, 8, 100-110.
54. Puechberty, J.; Laurent, A.M.; Gimenez, S.; Billault, A.; Brun-Laurent, M.E.; Calenda, A.; Marçais, B.; Prades, C.; Ioannou, P.; Yurov, Y., et al. Genetic and physical analyses of the centromeric and pericentromeric regions of human chromosome 5: Recombination across 5cen. Genomics 1999, 56, 274-287.
55. Vermeesch, J.R.; Duhamel, H.; Raeymaekers, P.; van Zand, K.; Verhasselt, P.; Fryns, J.P.; Marynen, P. A physical map of the chromosome 12 centromere. Cytogenet. Genome Res. 2003, 103, 63-73.
56. Horvath, J.E.; Schwartz, S.; Eichler, E.E. The mosaic structure of human pericentromeric DNA: A strategy for characterizing complex regions of the human genome. Genome Res. 2000, 10, 839-852.
57. Bailey, J.A.; Yavor, A.M.; Massa, H.F.; Trask, B.J.; Eichler, E.E. Segmental duplications: Organization and impact within the current human genome project assembly. Genome Res. 2001, 11, 1005-1017.
58. Cheung, V.G.; Nowak, N.; Jang, W.; Kirsch, I.R.; Zhao, S.; Chen, X.N.; Furey, T.S.; Kim, U.J.; Kuo, W.L.; Olivier, M., et al. Integration of cytogenetic landmarks into the draft sequence of the human genome. Nature 2001, 409, 953-958.
59. Genovese, G.; Handsaker, R.E.; Li, H.; Kenny, E.E.; McCarroll, S.A. Mapping the human reference genome's missing sequence by three-way admixture in Latino genomes. Am. J. Hum. Genet. 2013, 93, 411-421.
60. Schueler, M.G.; Higgins, A.W.; Rudd, M.K.; Gustashaw, K.; Willard, H.F. Genomic and genetic definition of a functional human centromere. Science 2001, 294, 109-115.
61. Rudd, M.K.; Willard, H.F. Analysis of the centromeric regions of the human genome assembly. Trends Genet. 2004, 20, 529-533.
62. Nusbaum, C.; Mikkelsen, T.S.; Zody, M.C.; Asakawa, S.; Taudien, S.; Garber, M.; Kodira, C.D.; Schueler, M.G.; Shimizu, A.; Whittaker, C.A., et al. DNA sequence and analysis of human chromosome 8. Nature 2006, 439, 331-335.
63. Ross, M.T.; Grafham, D.V.; Coffey, A.J.; Scherer, S.; McLay, K.; Muzny, D.; Platzer, M.; Howell, G.R.; Burrows, C.; Bird, C.P., et al. The DNA sequence of the human X chromosome. Nature 2005, 434, 325-337.
64. Roizes, G. Human centromeric alphoid domains are periodically homogenized so that they vary substantially between homologues. Mechanism and implications for centromere functioning. Nucleic Acids Res. 2006, 34, 1912-1924.
65. Paar, V.; Pavin, N.; Rosandic, M.; Gluncic, M.; Basar, I.; Pezer, R.; Zinic, S.D. ColorHOR-Novel graphical algorithm for fast scan of alpha satellite higher-order repeats and HOR annotation for GenBank sequence of human genome. Bioinformatics 2005, 21, 846-852.
66. Rosandic, M.; Paar, V.; Gluncic, M.; Basar, I.; Pavin, N. Key-string algorithm-Novel approach to computational analysis of repetitive sequences in human centromeric DNA. Croat. Med. J. 2003, 44, 386-406.
67. Rudd, M.K.; Schueler, M.G.; Willard, H.F. Sequence organization and functional annotation of human centromeres. Cold Spring Harb. Symp. Quant. Biol. 2003, 68, 141-149.
68. Alkan, C.; Ventura, M.; Archidiacono, N.; Rocchi, M.; Sahinalp, S.C.; Eichler, E.E. Organization and evolution of primate centromeric DNA from whole-genome shotgun sequence data. PLoS Comput. Biol. 2007, 3, 1807-1818.
69. Alexandrov, I.A.; Mashkova, T.D.; Akopian, T.A.; Medvedev, L.I.; Kisselev, L.L.; Mitkevich, S.P.; Yurov, Y.B. Chromosome-specific alpha satellites: Two distinct families on human chromosome 18. Genomics 1991, 11, 15-23.
70. Choo, K.H.; Earle, E.; Vissel, B.; Filby, R.G. Identification of two distinct subfamilies of alpha satellite DNA that are highly specific for human chromosome 15. Genomics 1990, 7, 143-151.
71. Wevrick, R.; Willard, H.F. Physical map of the centromeric region of human chromosome 7: Relationship between two distinct alpha satellite arrays. Nucleic Acids Res. 1991, 19, 2295-2301.
72. Miga, K.H.; Newton, Y.; Jain, M.; Altemose, N.; Willard, H.F.; Kent, W.J. Centromere reference models for human chromosomes X and Y satellite arrays. arXiv 2013, arXiv:1307.0035v3 [q-bio.GN].
73. Schulze, S.; Sinclair, D.A.; Silva, E.; Fitzpatrick, K.A.; Singh, M.; Lloyd, V.K.; Morin, K.A.; Kim, J.; Holm, D.G.; Kennison, J.A.; et al. Essential genes in proximal 3L heterochromatin of Drosophila melanogaster. Mol. Gen. Genet. 2001, 264, 782-789.
74. Ryan, D.P.; da Silva, M.R.; Soong, T.W.; Fontaine, B.; Donaldson, M.R.; Kung, A.W.; Jongjaroenprasert, W.; Liang, M.C.; Khoo, D.H.; Cheah, J.S., et al. Mutations in potassium channel Kir2.6 cause susceptibility to thyrotoxic hypokalemic periodic paralysis. Cell 2010, 140, 88-98.
75. Masumoto, H.; Nakano, M.; Ohzeki, J. The role of CENP-B and alpha-satellite DNA: De novo assembly and epigenetic maintenance of human centromeres. Chromosome Res. 2004, 12, 543-556.
76. Blower, M.D.; Sullivan, B.A.; Karpen, G.H. Conserved organization of centromeric chromatin in flies and humans. Dev. Cell 2002, 2, 319-330.
77. Sullivan, B.A.; Karpen, G.H. Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat. Struct. Mol. Biol. 2004, 11, 1076-1083.
78. Hori, T.; Fukagawa, T. Establishment of the vertebrate kinetochores. Chromosome Res. 2012, 20, 547-561.
79. Spence, J.M.; Critcher, R.; Ebersole, T.A.; Valdivia, M.M.; Earnshaw, W.C.; Fukagawa, T.; Farr, C.J. Co-localization of centromere activity, proteins and topoisomerase II within a subdomain of the major human X alpha-satellite array. EMBO J. 2002, 21, 5269-5280.
80. Sullivan, L.L.; Boivin, C.D.; Mravinac, B.; Song, I.Y.; Sullivan, B.A. Genomic size of CENP-A domain is proportional to total alpha satellite array size at human centromeres and expands in cancer cells. Chromosome Res. 2011, 19, 457-470.
81. Hasson, D.; Panchenko, T.; Salimian, K.J.; Salman, M.U.; Sekulic, N.; Alonso, A.; Warburton, P.E.; Black, B.E. The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat. Struct. Mol. Biol. 2013, 20, 687-695.