Human Artificial Chromosomes with Alpha Satellite-Based De Novo Centromeres Show Increased Frequency of Nondisjunction and Anaphase Lag

Molecular and Cellular Biology

Volumn 23, Issue 21, 2003, Pages 7689-7697

  Rudd, M Katharine ^a,b   Mays, Robert W ^a,c   Schwartz, Stuart ^a   Willard, Huntington F ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY   (United States)

^c ATHERSYS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE;

ANAPHASE; ARTICLE; ARTIFICIAL CHROMOSOME; CELL DIVISION; CENTROMERE; CHROMATIN; CHROMOSOME 17; CHROMOSOME SEGREGATION; CHROMOSOME SIZE; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA CONTENT; DNA MODIFICATION; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL; X CHROMOSOME;

ANAPHASE; CELL LINE, TUMOR; CENTROMERE; CHROMOSOME SEGREGATION; CHROMOSOMES, ARTIFICIAL, HUMAN; CHROMOSOMES, HUMAN, PAIR 17; DNA, SATELLITE; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; NONDISJUNCTION, GENETIC; RING CHROMOSOMES;

EID: 0142027869     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.21.7689-7697.2003     Document Type: Article

References (73)

1. Alexandrov, I., A. Kazakov, I. Tumeneva, V. Shepelev, and Y. Yurov. 2001. Alpha-satellite DNA of primates: old and new families. Chromosoma 110: 253-266.
2. Beach, D., M. Piper, and S. Shall. 1980. Isolation of chromosomal origins of replication in yeast. Nature 284:185-187.
3. Bernard, P., J. F. Maure, J. F. Partridge, S. Genier, J. P. Javerzat, and R. C. Allshire. 2001. Requirement of heterochromatin for cohesion at centromeres. Science 294:2539-2542.
4. Bloom, K. S., and J. Carbon. 1982. Yeast centromere DNA is in a unique and highly ordered structure in chromosomes and small circular minichromosomes. Cell 29:305-317.
5. Choo, K. H. 2001. Domain organization at the centromere and neocentromere. Dev. Cell 1:165-177.
6. Cimini, D., D. Fioravanti, E. D. Salmon, and F. Degrassi. 2002. Merotelic kinetochore orientation versus chromosome mono-orientation in the origin of lagging chromosomes in human primary cells. J. Cell Sci. 115:507-515.
7. Clarke, L., H. Amstutz, B. Fishel, and J. Carbon. 1986. Analysis of centromeric DNA in the fission yeast Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 83:8253-8257.
8. Cleveland, D. W., Y. Mao, and K. F. Sullivan. 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112:407-421.
9. Copenhaver, G. P., K. Nickel, T. Kuromori, M. I. Benito, S. Kaul, X. Lin, M. Bevan, G. Murphy, B. Harris, L. D. Parnell, W. R. McCombie, R. A. Martienssen, M. Marra, and D. Preuss. 1999. Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286:2468-2474.
10. de Lange, T. 2002. Protection of mammalian telomeres. Oncogene 21:532-540.
11. Ebersole, T. A., A. Ross, E. Clark, N. McGill, D. Schindelhauer, H. Cooke, and B. Grimes. 2000. Mammalian artificial chromosome formation from circular alphoid input DNA does not require telomere repeats. Hum. Mol. Genet. 9:1623-1631.
12. Frengen, E., B. Zhao, S. Howe, D. Weichenhan, K. Osoegawa, E. Gjernes, J. Jessee, H. Prydz, C. Huxley, and P. J. de Jong. 2000. Modular bacterial artificial chromosome vectors for transfer of large inserts into mammalian cells. Genomics 68:118-126.
13. Gilbert, D. M. 2001. Making sense of eukaryotic DNA replication origins. Science 294:96-100.
14. Grimes, B. R., A. A. Rhoades, and H. F. Willard. 2002. Alpha-satellite DNA and vector composition influence rates of human artificial chromosome formation. Mol. Ther. 5:798-805.
15. Hall, S. E., G. Kettler, and D. Preuss. 2003. Centromere satellites from Arabidopsis populations: maintenance of conserved and variable domains. Genome Res. 13:195-205.
16. Harrington, J. J., G. Van Bokkelen, R. W. Mays, K. Gustashaw, and H. F. Willard. 1997. Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat. Genet. 15:345-355.
17. Henikoff, S., K. Ahmad, and H. S. Malik. 2001. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098-1102.
18. Henning, K. A., E. A. Novotny, S. T. Compton, X. Y. Guan, P. P. Liu, and M. A. Ashlock. 1999. Human artificial chromosomes generated by modification of a yeast artificial chromosome containing both human alpha satellite and single-copy DNA sequences. Proc. Natl. Acad. Sci. USA 96:592-597.
19. Hieter, P., D. Pridmore, J. H. Hegemann, M. Thomas, R. W. Davis, and P. Philippsen. 1985. Functional selection and analysis of yeast centromeric DNA. Cell 42:913-921.
20. Higgins, A. W., M. G. Schueler, and H. F. Willard. 1999. Chromosome engineering: generation of mono- and dicentric isochromosomes in a somatic cell hybrid system. Chromosoma 108:256-265.
21. Hyman, A. A., and P. K. Sorger. 1995. Structure and function of kinetochores in budding yeast. Annu. Rev. Cell Dev. Biol. 11:471-495.
22. Ikeno, M., B. Grimes, T. Okazaki, M. Nakano, K. Saitoh, H. Hoshino, N. I. McGill, H. Cooke, and H. Masumoto. 1998. Construction of YAC-based mammalian artificial chromosomes. Nat. Biotechnol. 16:431-439.
23. Koshland, D., L. Rutledge, M. Fitzgerald-Hayes, and L. H. Hartwell. 1987. A genetic analysis of dicentric minichromosomes in Saccharomyces cerevisiae. Cell 48:801-812.
24. Kouprina, N., T. Ebersole, M. Koriabine, E. Pak, I. B. Rogozin, M. Katoh, M. Oshimura, K. Ogi, M. Peredelchuk, G. Solomon, W. Brown, J. C. Barrett, and V. Larionov. 2003. Cloning of human centromeres by transformation-associated recombination in yeast and generation of functional human artificial chromosomes. Nucleic Acids Res. 31:922-934.
25. Lansdorp, P. M., N. P. Verwoerd, F. M. van de Rijke, V. Dragowska, M. T. Little, R. W. Dirks, A. K. Raap, and H. J. Tanke. 1996. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 5:685-691.
26. Larin, Z., and J. E. Mejia. 2002. Advances in human artificial chromosome technology. Trends Genet. 18:313-319.
27. Lee, J. Y., and T. L. Orr-Weaver. 2001. The molecular basis of sister-chromatid cohesion. Annu. Rev. Cell Dev. Biol. 17:753-777.
28. Lopez, J. M., G. H. Karpen, and T. L. Orr-Weaver. 2000. Sister-chromatid cohesion via MEI-S332 and kinetochore assembly are separable functions of the Drosophila centromere. Curr. Biol. 10:997-1000.
29. Mahtani, M. M., and H. F. Willard. 1990. Pulsed-field gel analysis of alpha satellite DNA at the human X chromosome centromere: high frequency polymorphisms and array size estimate. Genomics 7:607-613.
30. Malik, H. S., and S. Henikoff. 2002. Conflict begets complexity: the evolution of centromeres. Curr. Opin. Genet. Dev. 12:711-718.
31. Manuelidis, L. 1978. Chromosomal localization of complex and simple repeated human DNAs. Chromosoma 66:23-32.
32. Marahrens, Y., and B. Stillman. 1992. A yeast chromosomal origin of DNA replication defined by multiple functional elements. Science 255:817-823.
33. Masumoto, H., M. Ikeno, M. Nakano, T. Okazaki, B. Grimes, H. Cooke, and N. Suzuki. 1998. Assay of centromere function using a human artificial chromosome. Chromosoma 107:406-416.
34. Mejia, J. E., A. Alazami, A. Willmott, P. Marschall, E. Levy, W. C. Earnshaw, and Z. Larin. 2002. Efficiency of de novo centromere formation in human artificial chromosomes. Genomics 79:297-304.
35. Mills, W., R. Critcher, C. Lee, and C. J. Farr. 1999. Generation of an approximately 2.4 Mb human X centromere-based minichromosome by targeted telomere-associated chromosome fragmentation in DT40. Hum. Mol. Genet. 8:751-761.
36. Murray, A. W., N. P. Schultes, and J. W. Szostak. 1986. Chromosome length controls mitotic chromosome segregation in yeast. Cell 45:529-536.
37. Murray, A. W., and J. W. Szostak. 1983. Construction of artificial chromosomes in yeast. Nature 305:189-193.
38. Musacchio, A., and K. G. Hardwick. 2002. The spindle checkpoint: structural insights into dynamic signalling. Nat. Rev. Mol. Cell Biol. 3:731-741.
39. Nakaseko, Y., N. Kinoshita, and M. Yanagida. 1987. A novel sequence common to the centromere regions of Schizosaccharomyces pombe chromosomes. Nucleic Acids Res. 15:4705-4715.
40. Ohzeki, J., M. Nakano, T. Okada, and H. Masumoto. 2002. CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J. Cell Biol. 159:765-775.
41. Palmer, D. K., K. O'Day, M. H. Wener, B. S. Andrews, and R. L. Margolis. 1987. A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J. Cell Biol. 104:805-815.
42. Round, E. K., S. K. Flowers, and E. J. Richards. 1997. Arabidopsis thaliana centromere regions: genetic map positions and repetitive DNA structure. Genome Res. 7:1045-1053.
43. Saffery, R., L. H. Wong, D. V. Irvine, M. A. Bateman, B. Griffiths, S. M. Cutts, M. R. Cancilla, A. C. Cendron, A. J. Stafford, and K. H. Choo. 2001. Construction of neocentromere-based human minichromosomes by telomere-associated chromosomal truncation. Proc. Natl. Acad. Sci. USA 98: 5705-5710.
44. Schindelhauer, D., and T. Schwarz. 2002. Evidence for a fast, intrachromosomal conversion mechanism from mapping of nucleotide variants within a homogeneous alpha-satellite DNA array. Genome Res. 12:1815-1826.
45. Schueler, M. G., A. W. Higgins, M. K. Rudd, K. Gustashaw, and H. F. Willard. 2001. Genomic and genetic definition of a functional human centromere. Science 294:109-115.
46. Shampay, J., J. W. Szostak, and E. H. Blackburn. 1984. DNA sequences of telomeres maintained in yeast. Nature 310:154-157.
47. Shen, M. H., J. W. Yang, J. Yang, C. Pendon, and W. R. Brown. 2001. The accuracy of segregation of human mini-chromosomes varies in different vertebrate cell lines, correlates with the extent of centromere formation and provides evidence for a trans-acting centromere maintenance activity. Chromosoma 109:524-535.
48. Stoler, S., K. C. Keith, K. E. Curnick, and M. Fitzgerald-Hayes. 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.
49. Sullivan, B. A., M. D. Blower, and G. H. Karpen. 2001. Determining centromere identity: cyclical stories and forking paths. Nat. Rev. Genet. 2:584-596.
50. Sullivan, B. A., and S. Schwartz. 1995. Identification of centromeric antigens in dicentric Robertsonian translocations: CENP-C and CENP-E are necessary components of functional centromeres. Hum. Mol. Genet. 5:2189-2198.
51. Sullivan, B. A., A. D. Skora, H. D. Le, and G. H. Karpen. 2002. CENP-A chromatin occupies "euchromatic" histone modifications. Am. J. Hum. Genet. 71:218.
52. Sullivan, B. A., and P. E. Warburton. 1999. Studying progression of vertebrate chromosomes through mitosis by immunofluorescence and FISH, p. 81-101. In W. A. Bickmore (ed.), Chromosome structural analysis: a practical approach. Oxford University Press, Oxford, United Kingdom.
53. Sullivan, B. A., and H. F. Willard. 1998. Stable dicentric X chromosomes with two functional centromeres. Nat. Genet. 20:227-228.
54. Sun, X., H. D. Le, J. M. Wahlstrom, and G. H. Karpen. 2003. Sequence analysis of a functional Drosophila centromere. Genome Res. 13:182-194.
55. Sun, X., J. Wahlstrom, and G. Karpen. 1997. Molecular structure of a functional Drosophila centromere. Cell 91:1007-1019.
56. Surosky, R. T., C. S. Newlon, and B. K. Tye. 1986. The mitotic stability of deletion derivatives of chromosome III in yeast. Proc. Natl. Acad. Sci. USA 83:414-418.
57. Taddei, A., C. Maison, D. Roche, and G. Almouzni. 2001. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat. Cell Biol. 3:114-120.
58. Tanaka, T. U. 2002. Bi-orienting chromosomes on the mitotic spindle. Curr. Opin. Cell Biol. 14:365-371.
59. Tyler-Smith, C., R. J. Oakey, Z. Larin, R. B. Fisher, M. Crocker, N. A. Affara, M. A. Ferguson-Smith, M. Muenke, O. Zuffardi, and M. A. Jobling. 1993. Localization of DNA sequences required for human centromere function through an analysis of rearranged Y chromosomes. Nat. Genet. 5:368-375.
60. Uhlmann, F. 2003. Chromosome cohesion and separation: from men and molecules. Curr. Biol. 13:R104-R114.
61. Walmsley, R. W., C. S. Chan, B. K. Tye, and T. D. Petes. 1984. Unusual DNA sequences associated with the ends of yeast chromosomes. Nature 310:157-160.
62. Warburton, P., and H. Willard. 1996. Evolution of centromeric alpha satellite DNA: molecular organization within and between human and primate chromosomes, p. 121-145. In M. Jackson, T. Strachan, and G. Dover (ed.), Human genome evolution. BIOS Scientific Publishers, Oxford, United Kingdom.
63. Warburton, P. E., C. A. Cooke, S. Bourassa, O. Vafa, B. A. Sullivan, G. Stetten, G. Gimelli, D. Warburton, C. Tyler-Smith, K. F. Sullivan, G. G. Poirier, and W. C. Earnshaw. 1997. Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr. Biol. 7:901-904.
64. Waye, J. S., and H. F. Willard. 1986. 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. 6:3156-3165.
65. Weier, H. U., J. N. Lucas, M. Poggensee, R. Segraves, D. Pinkel, and J. W. Gray. 1991. Two-color hybridization with high complexity chromosome-specific probes and a degenerate alpha satellite probe DNA allows unambiguous discrimination between symmetrical and asymmetrical translocations. Chromosoma 100:371-376.
66. Wevrick, R., W. C. Earnshaw, P. N. Howard-Peebles, and H. F. Willard. 1990. Partial deletion of alpha satellite DNA associated with reduced amounts of the centromere protein CENP-B in a mitotically stable human chromosome rearrangement. Mol. Cell. Biol. 10:6374-6380.
67. Wevrick, R., and H. F. Willard. 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. USA 86:9394-9398.
68. Willard, H. F. 1998. Centromeres: the missing link in the development of human artificial chromosomes. Curr. Opin. Genet. Dev. 8:219-225.
69. Willard, H. F. 2001. Neocentromeres and human artificial chromosomes: an unnatural act. Proc. Natl. Acad. Sci. USA 98:5374-5376.
70. Willard, H. F., K. D. Smith, and J. Sutherland. 1983. Isolation and characterization of a major tandem repeat family from the human X chromosome. Nucleic Acids Res. 11:2017-2033.
71. Willard, H. F., and J. S. Waye. 1987. 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. 25:207-214.
72. Yen, T. J., D. A. Compton, D. Wise, R. P. Zinkowski, B. R. Brinkley, W. C. Earnshaw, and D. W. Cleveland. 1991. CENP-E, a novel human centromere-associated protein required for progression from metaphase to anaphase. EMBO J. 10:1245-1254.
73. Yen, T. J., G. Li, B. T. Schaar, I. Szilak, and D. W. Cleveland. 1992. CENP-E is a putative kinetochore motor that accumulates just before mitosis. Nature 359:536-539.