Abstract
CENP-B, a highly conserved centromere-associated protein, binds to α-satellite DNA, the centromeric satellite of primate chromosomes, at a 17-bp sequence, the CENP-B box. By fluorescence in situ hybridization (FISH) with an oligomer specific for the CENP-B box sequence, we have demonstrated the abundance of CENP-B boxes on all chromosomes (except the Y) of humans, chimpanzee, pygmy chimpanzee, gorilla, and orangutan. This sequence motif was not detected in the genomes of other primates, including gibbons, Old and New World monkeys, and prosimians. Our results indicate that the CENP-B box containing subtype of α-satellite DNA may have emerged recently in the evolution of the large-bodied hominoids, after divergence of the phylogenetic lines leading to gibbons and apes; the box is thus on the order of 15–25 million years of age. The rapid process of dispersal and fixation of the CENP-B box sequence throughout the human and great ape genomes is thought to be a consequence of concerted evolution of α-satellite subsets on both homologous and nonhomologous chromosomes.
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References
Alves G, Seuánez HN, Fanning T (1994) Alpha satellite DNA in neotropical primates (Platyrrhini). Chromosoma 103:262–267
Baltimore D (1981) Gene conversion: some implications for immunoglobulin genes. Cell 24:592–594
Bernat RL, Borisy GG, Rothfield NF, Earnshaw WC (1990) Injection of anticentromere antibodies in interphase disrupts events required for chromosome movement at mitosis. J Cell Biol 111:1519–1533
Bernat RL, Delannoy MR, Rothfield NF, Earnshaw WC (1991) Disruption of centromere assembly during interphase inhibits kinetochore morphogenesis and function in mitosis. Cell 66:1229–1238
Calos MP, Miller JH (1980) Transposable elements. Cell 20:579–595
Cooke CA, Bernat RL, Eamshaw WC (1990) CENP-B: a major human centromere protein located beneath the kinetochore. J Cell Biol 110:1475–1488
Earnshaw WC, Rothfield N (1985) Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91:313–321
Earnshaw WC, Sullivan KF, Machlin PS, Cooke CA, Kaiser DA, Pollard TD, Rothfield NF, Cleveland DW (1987) Molecular cloning of a cDNA for CENP-B, the major human centromere autoantigen. J Cell Biol 104:817–829
Earnshaw WC, Ratrie III H, Stetten G (1989) Visualization of centromere proteins CENP-B and CENP-C on a stable dicentric chromosome in cytological spreads. Chromosoma 98:1–12
Haaf T, Ward DC (1994) Structural analysis of a-satellite DNA and centromere proteins using extended chromatin and chromosomes. Hum Mol Genet 3:679–709
Haaf T, Ward DC (1995) Rabl orientation of CENP-B box sequences in Tupaia belangeri fibroblasts. Cytogenet Cell Genet (in press)
Haaf T, Warburton PE, Willard HF (1992) Integration of human α-satellite DNA into simian chromosomes: centromere protein binding and disruption of normal chromosome segregation. Cell 70:681–696
Hourcade D, Dressler D, Wolfson J (1973) The amplification of ribosomal RNA genes involves a rolling circle intermediate. Proc Natl Acad Sci USA 70:2926–2930
Krystal M, D'Eustachio P, Ruddle FH, Arnheim N (1981) Human nucleolus organizers on non-homologous chromosomes can share the same ribosomal gene variants. Proc Natl Acad Sci USA 78: 5744–5748
Larin Z, Fricker MD, Tyler-Smith C (1994) De novo formation of several features of a centromere following introduction of a Y alphoid YAC into mammalian cells. Hum Mol Genet 3:689–695
Lohe AR, Brutlag DL (1987) Adjacent satellite DNA segments in Drosophila. Structure of junctions. J Mol Biol 194:171–179
Maio JJ (1971) Strand reassociation and polynucleotide binding in the African green monkey, Cercopithecus aethiops. J Mol Biol 56:579–595
Maio JJ, Brown FL, Musich PR (1981) Toward a molecular paleontology of primate genomes: the HindIII and EcoRl families of alphoid DNAs. Chromosoma 83:103–125
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 109:1963–1973
Matera AG, Ward DC (1992) Oligonucleotide probes for the analysis of specific repetitive DNA sequences by fluorescence in situ hybridization. Hum Mol Genet 1:535–539
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 116:585–596
Musich PR, Brown FL, Maio JJ (1980) Highly repetitive component alpha and related alphoid DNAs in man and monkeys. Chromosoma 80:331–348
Oakey R, Tyler-Smith C (1990) Y chromosome DNA haplotyping suggests that most European and Asian men are descended from one of two males. Genomics 7:325–330
Rosenberg H, Singer M, Rosenberg M (1978) Highly reiterated sequences of Simians. Science 200:394–402
Simerly C, Balczon R, Brinkley BR, Schatten G (1990) Microinjected kinetochore antibodies interfere with chromosome movement in meiotic and mitotic mouse oocytes. J Cell Biol 111:1491–1504
Smith GP (1976) Evolution of repeated DNA sequences by unequal crossing over. Science 191:528–535
Spradling AC (1981) The organization and amplification of two chromosomal domains containing Drosophila chorion genes. Cell 27: 193–201
Sullivan KF, Glass CA (1991) CENP-B is a highly conserved mammalian centromere protein with homology to the helix-loop-helix family of proteins. Chromosoma 100:360–370
Tyler-Smith C, Oakey RJ, Larin Z, Fisher RB, Crocker M, Affara NA, Ferguson-Smith MA, Muenke M, Zuffardi O, Jobling MA (1993) Localization of DNA sequences required for human centromere function through an analysis of rearranged Y chromosomes. Nature Genet 5:368–375
Waye JS, Willard HF (1989) Concerted evolution of alpha satellite DNA: evidence for species specificity and a general lack of sequence conservation among alphoid sequences of higher primates. Chromosoma 98:273–279
Wevrick R, Willard HF (1989) Long-range organization of tandem arrays of α satellite DNA at the centromeres of human chromosomes: high frequency array-length polymorphism and meiotic stability. Proc Natl Acad Sci USA 86:9394–9398
Willard HF (1991) Evolution of alpha satellite. Curr Opin Genet Dev 1:509–514
Willard HF, Waye JS (1987) Hierarchical order in chromosome-specific human alpha satellite DNA. Trends Genet 3:192–198
Wong AKC, Rattner JB (1988) Sequence organization and cytological localization of the minor satellite of mouse. Nucleic Acids Res 16:11645–11661
Yoda K, Kitagawa K, Masumoto H, Muro Y, Okazaki T (1993) A human centromere protein, CENP-B, has a DNA binding domain containing four potential a helices at the NH2 terminus, which is separable from dimerizing activity. J Cell Biol 119:1413–1427
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Correspondence to: T. Haaf
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Haaf, T., Mater, A.G., Wienberg, J. et al. Presence and abundance of CENP-B box sequences in great ape subsets of primate-specific α-satellite DNA. J Mol Evol 41, 487–491 (1995). https://doi.org/10.1007/BF00160320
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DOI: https://doi.org/10.1007/BF00160320