Abstract
The chromatin structure of the central core region of Schizosaccharomyces pombe centromeric DNA is unusual. This distinctive chromatin structure is associated only with central core sequences in a functional context and is modulated by a novel cis-acting DNA element (centromere enhancer) within the functionally critical K centromeric repeat, which is found in multiple copies in all three S. pombe centromeres. The centromere enhancer alters central core chromatin structure from a distance and in an orientation-independent manner without altering the nucleosomal packaging of sequences between the enhancer and the central core. These findings suggest a functionally relevant structural interaction between the enhancer and the centromeric central core brought about by DNA looping.
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- Baum M., Ngan V. K., Clarke L. The centromeric K-type repeat and the central core are together sufficient to establish a functional Schizosaccharomyces pombe centromere. Mol Biol Cell. 1994 Jul;5(7):747–761. doi: 10.1091/mbc.5.7.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bloom K. S., Carbon J. Yeast centromere DNA is in a unique and highly ordered structure in chromosomes and small circular minichromosomes. Cell. 1982 Jun;29(2):305–317. doi: 10.1016/0092-8674(82)90147-7. [DOI] [PubMed] [Google Scholar]
- Chikashige Y., Kinoshita N., Nakaseko Y., Matsumoto T., Murakami S., Niwa O., Yanagida M. Composite motifs and repeat symmetry in S. pombe centromeres: direct analysis by integration of NotI restriction sites. Cell. 1989 Jun 2;57(5):739–751. doi: 10.1016/0092-8674(89)90789-7. [DOI] [PubMed] [Google Scholar]
- Clarke L., Amstutz H., Fishel B., Carbon J. Analysis of centromeric DNA in the fission yeast Schizosaccharomyces pombe. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8253–8257. doi: 10.1073/pnas.83.21.8253. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clarke L., Baum M. P. Functional analysis of a centromere from fission yeast: a role for centromere-specific repeated DNA sequences. Mol Cell Biol. 1990 May;10(5):1863–1872. doi: 10.1128/mcb.10.5.1863. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clarke L., Baum M., Marschall L. G., Ngan V. K., Steiner N. C. Structure and function of Schizosaccharomyces pombe centromeres. Cold Spring Harb Symp Quant Biol. 1993;58:687–695. doi: 10.1101/sqb.1993.058.01.076. [DOI] [PubMed] [Google Scholar]
- Clarke L., Carbon J. Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature. 1980 Oct 9;287(5782):504–509. doi: 10.1038/287504a0. [DOI] [PubMed] [Google Scholar]
- Cottarel G., Shero J. H., Hieter P., Hegemann J. H. A 125-base-pair CEN6 DNA fragment is sufficient for complete meiotic and mitotic centromere functions in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Aug;9(8):3342–3349. doi: 10.1128/mcb.9.8.3342. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ding R., McDonald K. L., McIntosh J. R. Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J Cell Biol. 1993 Jan;120(1):141–151. doi: 10.1083/jcb.120.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Earnshaw W. C., Ratrie H., 3rd, Stetten G. Visualization of centromere proteins CENP-B and CENP-C on a stable dicentric chromosome in cytological spreads. Chromosoma. 1989 Jun;98(1):1–12. doi: 10.1007/BF00293329. [DOI] [PubMed] [Google Scholar]
- Fishel B., Amstutz H., Baum M., Carbon J., Clarke L. Structural organization and functional analysis of centromeric DNA in the fission yeast Schizosaccharomyces pombe. Mol Cell Biol. 1988 Feb;8(2):754–763. doi: 10.1128/mcb.8.2.754. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Forrester W. C., Takegawa S., Papayannopoulou T., Stamatoyannopoulos G., Groudine M. Evidence for a locus activation region: the formation of developmentally stable hypersensitive sites in globin-expressing hybrids. Nucleic Acids Res. 1987 Dec 23;15(24):10159–10177. doi: 10.1093/nar/15.24.10159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grosveld F., van Assendelft G. B., Greaves D. R., Kollias G. Position-independent, high-level expression of the human beta-globin gene in transgenic mice. Cell. 1987 Dec 24;51(6):975–985. doi: 10.1016/0092-8674(87)90584-8. [DOI] [PubMed] [Google Scholar]
- Hahnenberger K. M., Baum M. P., Polizzi C. M., Carbon J., Clarke L. Construction of functional artificial minichromosomes in the fission yeast Schizosaccharomyces pombe. Proc Natl Acad Sci U S A. 1989 Jan;86(2):577–581. doi: 10.1073/pnas.86.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hahnenberger K. M., Carbon J., Clarke L. Identification of DNA regions required for mitotic and meiotic functions within the centromere of Schizosaccharomyces pombe chromosome I. Mol Cell Biol. 1991 Apr;11(4):2206–2215. doi: 10.1128/mcb.11.4.2206. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hayden J. H., Bowser S. S., Rieder C. L. Kinetochores capture astral microtubules during chromosome attachment to the mitotic spindle: direct visualization in live newt lung cells. J Cell Biol. 1990 Sep;111(3):1039–1045. doi: 10.1083/jcb.111.3.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kornberg R. D. Structure of chromatin. Annu Rev Biochem. 1977;46:931–954. doi: 10.1146/annurev.bi.46.070177.004435. [DOI] [PubMed] [Google Scholar]
- Kuhn R. M., Clarke L., Carbon J. Clustered tRNA genes in Schizosaccharomyces pombe centromeric DNA sequence repeats. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1306–1310. doi: 10.1073/pnas.88.4.1306. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maraschio P., Zuffardi O., Caiulo A., Dainotti E., Piantanida M., Rivera H., Tupler R. Deletion of specific sequences or modification of centromeric chromatin are responsible for Y chromosome centromere inactivation. Hum Genet. 1990 Oct;85(5):491–494. doi: 10.1007/BF00194222. [DOI] [PubMed] [Google Scholar]
- Murakami S., Matsumoto T., Niwa O., Yanagida M. Structure of the fission yeast centromere cen3: direct analysis of the reiterated inverted region. Chromosoma. 1991 Dec;101(4):214–221. doi: 10.1007/BF00365153. [DOI] [PubMed] [Google Scholar]
- Murray A. W., Szostak J. W. Construction of artificial chromosomes in yeast. Nature. 1983 Sep 15;305(5931):189–193. doi: 10.1038/305189a0. [DOI] [PubMed] [Google Scholar]
- Nakaseko Y., Adachi Y., Funahashi S., Niwa O., Yanagida M. Chromosome walking shows a highly homologous repetitive sequence present in all the centromere regions of fission yeast. EMBO J. 1986 May;5(5):1011–1021. doi: 10.1002/j.1460-2075.1986.tb04316.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakaseko Y., Kinoshita N., Yanagida M. A novel sequence common to the centromere regions of Schizosaccharomyces pombe chromosomes. Nucleic Acids Res. 1987 Jun 25;15(12):4705–4715. doi: 10.1093/nar/15.12.4705. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Polizzi C., Clarke L. The chromatin structure of centromeres from fission yeast: differentiation of the central core that correlates with function. J Cell Biol. 1991 Jan;112(2):191–201. doi: 10.1083/jcb.112.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ptashne M. How eukaryotic transcriptional activators work. Nature. 1988 Oct 20;335(6192):683–689. doi: 10.1038/335683a0. [DOI] [PubMed] [Google Scholar]
- Reitman M., Lee E., Westphal H., Felsenfeld G. An enhancer/locus control region is not sufficient to open chromatin. Mol Cell Biol. 1993 Jul;13(7):3990–3998. doi: 10.1128/mcb.13.7.3990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schulman I., Bloom K. S. Centromeres: an integrated protein/DNA complex required for chromosome movement. Annu Rev Cell Biol. 1991;7:311–336. doi: 10.1146/annurev.cb.07.110191.001523. [DOI] [PubMed] [Google Scholar]
- Singer M. F. Highly repeated sequences in mammalian genomes. Int Rev Cytol. 1982;76:67–112. doi: 10.1016/s0074-7696(08)61789-1. [DOI] [PubMed] [Google Scholar]
- Steiner N. C., Hahnenberger K. M., Clarke L. Centromeres of the fission yeast Schizosaccharomyces pombe are highly variable genetic loci. Mol Cell Biol. 1993 Aug;13(8):4578–4587. doi: 10.1128/mcb.13.8.4578. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takahashi K., Murakami S., Chikashige Y., Funabiki H., Niwa O., Yanagida M. A low copy number central sequence with strict symmetry and unusual chromatin structure in fission yeast centromere. Mol Biol Cell. 1992 Jul;3(7):819–835. doi: 10.1091/mbc.3.7.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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 U S A. 1989 Dec;86(23):9394–9398. doi: 10.1073/pnas.86.23.9394. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang X. Y., Fittler F., Hörz W. Eight different highly specific nucleosome phases on alpha-satellite DNA in the African green monkey. Nucleic Acids Res. 1983 Jul 11;11(13):4287–4306. doi: 10.1093/nar/11.13.4287. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zinkowski R. P., Meyne J., Brinkley B. R. The centromere-kinetochore complex: a repeat subunit model. J Cell Biol. 1991 Jun;113(5):1091–1110. doi: 10.1083/jcb.113.5.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]