Skip to main content
Log in

Analysing the Contribution of Nucleic Acids to the Structure and Properties of Centric Heterochromatin

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

A class of repetitive DNA sequences frequently found at centromeric regions are R/Y-satellites showing an asymmetric distribution of residues resulting in one strand being rich in purines (R-strand) while the complementary strand is pyrimidine-rich (Y-strand). The dodeca-satellite of Drosophila belongs to this class of centromeric satellites. In vitro, the dodeca-satellite forms altered DNA structures in which the R-strand forms very stable intramolecular fold-backs that are stabilised by the formation of tandem G · A mismatches. A single-stranded nucleic acids binding protein, DDP1, binds the unstructured dodeca-satellite Y-strand with high affinity. In polytene chromosomes, DDP1 associates with the heterochromatic chromocenter and, at the euchromatic chromosome arms, co-localises with HP1. DDP1 is a vigilin. Vigilins are highly conserved multi-KH-domain proteins. Scp160p, the vigilin from S. cerevisiae, is involved in the control of ploidy. DDP1 complements a Δscp160 deletion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abad, J.P., M. Carmena, S. Baars, R.D.C. Saunders, D.M. Glover, P. Ludeña, C. Sentis, C. Tyler-Smith & A. Villasante, 1992. Dodeca-satellite: a conserved G+C-rich satellite from centromeric heterochromatin of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 89: 4663-4667.

    Google Scholar 

  • Alfenito, M.R. & J.A. Birchler, 1993. Molecular characterization of a maize B chromosome centric sequence. Genetics 135: 589–597.

    Google Scholar 

  • Baum, M., V.K. Ngan & L. Clarke, 1994. The centromeric K-type repeat and the central core are together sufficient to establish the functional Schizosaccharomyces pombe centromere. Mol. Cell. Biol. 5: 747–761.

    Google Scholar 

  • Buchwitz, B.J., K. Ahmad, L.L. Moore, M.B. Roth & S. Henikoff, 1999. A histone H3-like protein in C. elegans. Nature 401: 547–548.

    Google Scholar 

  • Carmena, M., J.P. Abad, A. Villasante & C. González, 1993. The Drosophila melanogaster dodecasatellite sequence is closely linked to the centromere and can form connections between sister chromatids during mitosis. J. Cell Sci. 105: 41–50.

    Google Scholar 

  • Catasti, P., G. Gupta, A.E. Garcia, R. Ratliff, L. Hong, P. Yau, R.K. Moyzis & E.M. Bradbury, 1994. Unusual structures of the tandem repetitive DNA sequences located at human centromeres. Biochemistry 33: 3819-3830.

    Google Scholar 

  • Choo, K.H.A., 2001. Domain organization at the centromere and neocentromere. Dev. Cell 1: 165–177.

    Google Scholar 

  • Chou, S.-H., L. Zhu & B.R. Reid, 1994. The unusual structure of the human centromere (GGA)2 motif. J. Mol. Biol. 244: 259–268.

    Google Scholar 

  • Cortés, A. & F. Azorín, 2000. DDP1, a heterochromatin-associated multi-KH-domain protein of Drosophila melanogaster, interacts specifically with centromeric satellite DNA sequences. Mol. Cell. Biol. 20: 3860-3869.

    Google Scholar 

  • Cortés, A., D. Huertas, L. Fanti, S. Pimpinelli, F.X. Marsellach, B. Piña & F. Azorín, 1999. DDP1, a single-stranded nucleic acid-binding protein of Drosophila, associates with pericentric heterochromatin and is functionally homologous to the yeast Scp160p, which is involved in the control of cell ploidy. EMBO J. 18: 3820-3833.

    Google Scholar 

  • Dodson, R.E. & D.J. Shapiro, 1997. Vigilin, a ubiquitous protein with 14K homology domains, is the estrogen-inducible vitellogenin mRNA 3′-untranslated region-binding protein. J. Biol. hem. 272: 12249–12252.

    Google Scholar 

  • Dorer, D.R. & S. Henikoff, 1994. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77: 993–1002.

    Google Scholar 

  • Ferrer, N., F. Azorín, A. Villasante, C. Gutiérrez & J.P. Abad, 1995. Centromeric dodeca-satellite DNA sequences form fold-back structures. J. Mol. Biol. 245: 8–21.

    Google Scholar 

  • Frey, S., M. Pool & M. Seedorf, 2001. Scp160p, an RNA-binding, polysome-associated protein, localizes to the endoplasmic reticulum of Saccharomyces cerevisiae in a microtubule-dependent manner. J. Biol. Chem. 276: 15905–15912.

    Google Scholar 

  • Fry, K. & W. Salser, 1977. Nucleotide sequence of HS-α satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell 12: 1069-1084.

    Google Scholar 

  • Grady, D.L., R.L. Ratliff, D.L. Robinson, E.C.McCanlies, J.Meyne & R.K. Moyzis, 1992. Highly conserved repetitive DNA sequences are present at human centromeres. Proc. Natl. Acad. Sci. SA 89: 1695-1699.

    Google Scholar 

  • Hahnenberg, K.M., J. Carbon & L.C. Clarke, 1991. Identification of DNA regions required for mitotic and meiotic functions within the centromere of Schizosaccharomyces pombe chromosome I. ol. Cell. Biol. 11: 2206-2215.

    Google Scholar 

  • Harrington, J.J., G. Van Bokkelen, R.W. Mays, K. Gustashaw & H.F. Willard, 1997. Formation of de novo centromeres and construction of first-generation human artificial chromosomes. Nat. enet. 15: 345–355.

    Google Scholar 

  • Howe, M., K.L. McDonald, D.G. Alberston & B.J. Meyer, 2001. IM-10 is required for kinetochore structure and function on Caenorhabditis elegans holocentric chromosomes. J. Cell Biol. 153: 1227-1238.

    Google Scholar 

  • Huertas, D. & F. Azorín, 1996. Structural polymorphism of homopurine DNA sequences. d(GGA)n and (GGGA)n repeats form intramolecular hairpins stabilized by different base-pairing interactions. Biochemistry (USA) 35: 13125–13135.

    Google Scholar 

  • Ikeno, M., B. Grimes, T. Okazaki, M. Nakano, K. Saitoh, H. oshino, N.I. McGill, H. Cooke & H. Masumoto, 1998. Construction of YAC-based mammalian artificial chromosomes. Nat. Biotechnol. 16: 431–439.

    Google Scholar 

  • Kalitsis, P. & K.H. Choo, 1997. Centromere DNA of higher eukaryotes, pp. 97–142 in The Centromere, edited by K.H. Choo. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Kanamori, H., R.E. Dodson & D.J. Shapiro, 1998. In vitro genetic analysis of the RNA binding site of vigilin, a multi-KH-domain protein. Mol. Cell. Biol. 18: 3991-4003.

    Google Scholar 

  • Karpen, G. & R. Allshire, 1997. The case for epigenetic effects on centromere identity and function. Trends Genet. 13: 489–496.

    Google Scholar 

  • Krüse, C., A. Grünweller, H. Notbohm, S. Kügler, W.G. Purschke & P.K. Müller, 1996. Evidence for a novel cytoplasmic tRNAcomplex containing the multi-KH-domain protein vigilin. Biochem. 329: 247–252.

    Google Scholar 

  • Krüse, C., A. Grünweller, D.K. Willkomm, T. Pfeiffer, R.K. Hartmann & P.K. Müller, 1998. tRNA is entrapped in similar, but distinct, nuclear and cytoplasmic ribonucleoprotein complexes, both of which contain vigilin and elongation factor 1a. Biochem. J. 329: 615–621.

    Google Scholar 

  • Kügler, S., A. Grünweller, C. Probst, M. Klinger, P.K. Müller & C. Krüse, 1996. Vigilin contains a functional nuclear localisation sequence and is present in both the cytoplasm and the nucleus. FEBS Lett. 382: 330–334.

    Google Scholar 

  • Lang, B.D. & J.L. Fridovich-Keil, 2000. Scp160p, a multiple KHdomain protein, is a component of mRNP complexes in yeast. Nucleic Acids Res. 28: 1576-1584.

    Google Scholar 

  • Lo, A.W., D.J. Magliano, M.C. Sibson, P. Kalitsis, J.M. Craig & K.H. Choo, 2001a. A novel chromatin immunoprecipitation and array (CIA) analysis identifies a 460-kb CENP-A-binding neocentromere DNA. Genome Res. 11: 448–457.

    Google Scholar 

  • Lo, A.W.I., J.M. Craig, R. Saffery, P. Kalitsis, D.V. Irvine, E. Earle, D.J. Magliano & K.H.A. Choo, 2001b. A 330 kb CENPA binding domain and altered replication timing at a human neocentromere. EMBO J. 20: 2087-2096.

    Google Scholar 

  • McKnight, G.L., J. Reasoner, T. Gilbert, K.O. Sundquist, B. Hokland, P.A. McKernan, J. Champagne, C.J. Johnson, M.C. Bailey, R. Holly, P.J. O'Hara & J.F. Oram, 1992. Cloning and expression of a cellular high density lipoprotein-binding protein that is up-regulated by cholesterol loading of cells. J. Biol. Chem. 267: 12131–12141.

    Google Scholar 

  • Meyne, J.E.A., 1990. Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequences in vertebrate chromosomes. Chromosoma 99: 3–10.

    Google Scholar 

  • Murphy, T.D. & G.H. Karpen, 1995. Localization of centromere function in a Drosophila minichromosome. Cell 82: 599–609.

    Google Scholar 

  • Nakaseko, Y., N. Kinoshita & M. Yanagida, 1986. Chromosome walking shows a highly repetitive sequence present in all the centromere regions of fission yeast. EMBO J. 5: 1011-1021.

    Google Scholar 

  • Nakaseko, Y., N. Kinoshita & M. Yanagida, 1987. A novel sequence common to the centromere regions of Schizosaccharomyces pombe chromosomes. Nucleic Acids Res. 15: 4705-4715.

    Google Scholar 

  • Novak, U., 1984. Structure and properties of highly repetitive DNA sequences in sheep. Nucleic Acids Res. 12: 2343-2350.

    Google Scholar 

  • Ortiz-Lombardía, M., A. Cortés, D. Huertas, R. Eritja & F. Azorín, 1998. Tandem 5′-GA:GA-3′ mismatches account for the high stability of the fold-back structures formed by the centromeric Drosophila dodecasatellite. J. Mol. Biol. 277: 757–762.

    Google Scholar 

  • Plenz, G., S. Kügler, S. Schnittger, H. Rieder, C. Fonatsch & P.K. Müller, 1994. The human vigilin gene: identification, chromosomal localization and expression pattern. Hum. Genet. 93: 575–582.

    Google Scholar 

  • Richards, E.J., H.M. Goodman & F.M. Ausubel, 1991. The centromere region of Arabidopsis thaliana chromosome I contains telomere-similar sequences. Nucleic Acids Res. 19: 3351-3357.

    Google Scholar 

  • Schmidt, C., B. Henkel, E. Pöschl, H. Zorbas, W.G. Purschke, T.R. Gloe & P.K. Müller, 1992. Complete cDNA sequence of chicken vigilin, a novel protein with amplified and evolutionary conserved domains. Eur. J. Biochem. 206: 625–634.

    Google Scholar 

  • Siomi, H., M.J. Matunis, W.M. Michael & G. Dreyfuss, 1993. The pre-mRNA binding protein K contains a novel evolutionarily conserved motif. Nucleic Acids Res. 21: 1193-1198.

    Google Scholar 

  • Stinchcomb, D.T., J.E. Shaw, S.H. Carr & D. Hirsh, 1985. Extrachromosomal DNA transformation of Caenorhabditis elegans. Mol. Cell. Biol. 5: 3484-3496.

    Google Scholar 

  • Sun, X., J. Wahlstrom & G. Karpen, 1997. Molecular structure of a functional Drosophila centromere. Cell 91: 1007-1019.

    Google Scholar 

  • Taparowsky, E.J. & S.A. Gerbi, 1982. Sequence analysis of bovine satellite I DNA (1.715 gm/cm3). Nucleic Acids Res. 10: 1271-1281.

    Google Scholar 

  • Wintersberger, U., C. Kühne & A. Karwan, 1995. Scp160p, a new yeast protein associated with the nuclear membrane and the endoplasmic reticulum, is necessary for maintenance of exact ploidy. Yeast 11: 929–944.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cortés, A., Huertas, D., Marsellach, F.X. et al. Analysing the Contribution of Nucleic Acids to the Structure and Properties of Centric Heterochromatin. Genetica 117, 117–125 (2003). https://doi.org/10.1023/A:1022947921402

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022947921402

Navigation