Advertisement
Journal Article
The genomic silencing of position-effect variegation in Drosophila melanogaster: interaction between the heterochromatin-associated proteins Su(var)3-7 and HP1
M. Delattre, A. Spierer, C.H. Tonka, P. Spierer
Journal of Cell Science 2000 113: 4253-4261;

Summary

Position-effect variegation results from mosaic silencing by chromosomal rearrangements juxtaposing euchromatin genes next to pericentric heterochromatin. An increase in the amounts of the heterochromatin-associated Su(var)3-7 and HP1 proteins augments silencing. Using the yeast two-hybrid protein interaction trap system, we have isolated HP1 using Su(var)3-7 as a bait. We have then delimited three binding sites on Su(var)3-7 for HP1. On HP1, the C-terminal moiety, including the chromo shadow domain, is required for interaction. In vivo, both proteins co-localise not only in heterochromatin, but also in a limited set of sites in euchromatin and at telomeres. When delocalised to the sites bound by the protein Polycomb in euchromatin, HP1 recruits Su(var)3-7. Finally, and in contrast with euchromatin genes, a decrease in the amounts of both proteins enhances variegation of the light gene, one of the few genetic loci mapped within pericentric heterochromatin. This body of data supports a direct link between Su(var)3-7 and HP1 in the genomic silencing of position-effect variegation.

REFERENCES

    1. Jenuwein, T.
    ( 1999). Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J 18, 1923– 1938
    OpenUrlAbstract
    1. Ainsztein, A. M.,
    2. Kandels-Lewis, S. E.,
    3. Mackay, A. M. and
    4. Earnshaw, W. C.
    ( 1998). INCENP centromere and spindle targeting: identification of essential conserved motifs and involvement of heterochromatin protein HP1. J. Cell Biol 143, 1763– 1774
    OpenUrlAbstract/FREE Full Text
    1. Belyaeva, E. S. and
    2. Zhimulev, I. F.
    ( 1991). Cytogenetic and molecular aspects of position effect variegation in Drosophila. III. Continuous and discontinuous compaction of chromosomal material as a result of position effect variegation. Chromosoma 100, 453– 466
    OpenUrlCrossRefPubMed
    1. Belyaeva, E. S.,
    2. Koryakov, D. E.,
    3. Pokholkova, G. V.,
    4. Demakova, O. V. and
    5. Zhimulev, I. F.
    ( 1997). Cytological study of the brown dominant position effect. Chromosoma 106, 124– 132
    OpenUrlCrossRefPubMed
    1. Brown, N. H. and
    2. Kafatos, F. C.
    ( 1988). Functional cDNA libraries from Drosophila embryos. J. Mol. Biol 203, 425– 437
    OpenUrlCrossRefPubMedWeb of Science
    1. Cleard, F.,
    2. Matsarskaia, M. and
    3. Spierer, P.
    ( 1995). The modifier of position-effect variegation Suvar(3)7 of Drosophila: there are two alternative transcripts and seven scattered zinc fingers, each preceded by a tryptophan box. Nucl. Acids Res 23, 796– 802
    OpenUrlAbstract/FREE Full Text
    1. Cleard, F.,
    2. Delattre, M. and
    3. Spierer, P.
    ( 1997). SU(VAR)3-7, a Drosophila heterochromatin-associated protein and companion of HP1 in the genomic silencing of position-effect variegation. EMBO J 16, 5280– 5288
    OpenUrlAbstract
    1. Csink, A. K. and
    2. Henikoff, S.
    ( 1996). Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381, 529– 531
    OpenUrlCrossRefPubMed
    1. Dernburg, A. F.,
    2. Broman, K. W.,
    3. Fung, J. C.,
    4. Marshall, W. F.,
    5. Philips, J.,
    6. Agard, D. A. and
    7. Sedat, J. W.
    ( 1996). Perturbation of nuclear architecture by long-distance chromosome interactions. Cell 85, 745– 759
    OpenUrlCrossRefPubMedWeb of Science
    1. Dorer, D. R. and
    2. Henikoff, S.
    ( 1994). Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77, 993– 1002
    OpenUrlCrossRefPubMedWeb of Science
    1. Eissenberg, J. C.,
    2. Morris, G. D.,
    3. Reuter, G. and
    4. Hartnett, T.
    ( 1992). The heterochromatin-associated protein HP-1 is an essential protein in Drosophila with dosage-dependent effects on position-effect variegation. Genetics 131, 345– 352
    OpenUrlAbstract/FREE Full Text
    1. Eissenberg, J. C. and
    2. Elgin, S. C.
    ( 2000). The HP1 protein family: getting a grip on chromatin. Curr. Opin. Genet. Dev 10, 204– 210
    OpenUrlCrossRefPubMedWeb of Science
    1. Elgin, S. C.
    ( 1996). Heterochromatin and gene regulation in Drosophila. Curr. Opin. Genet. Dev 6, 193– 202
    OpenUrlCrossRefPubMedWeb of Science
    1. Fanti, L.,
    2. Giovinazzo, G.,
    3. Berloco, M. and
    4. Pimpinelli, S.
    ( 1998). The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol. Cell 2, 527– 538
    OpenUrl
    1. Fields, S. and
    2. Song, O.
    ( 1989). A novel genetic system to detect protein-protein interactions. Nature 340, 245– 246
    OpenUrlCrossRefPubMedWeb of Science
    1. Frankel, S.,
    2. Sigel, E. A.,
    3. Craig, C.,
    4. Elgin, S. C.,
    5. Mooseker, M. S. and
    6. Artavanis-Tsakonas, S.
    ( 1997). An actin-related protein in Drosophila colocalizes with heterochromatin protein 1 in pericentric heterochromatin. J. Cell Sci 110, 1999– 2012
    OpenUrlAbstract/FREE Full Text
    1. Gyuris, J.,
    2. Golemis, E.,
    3. Chertkov, H. and
    4. Brent, R.
    ( 1993). Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 75, 791– 803
    OpenUrlCrossRefPubMedWeb of Science
    1. Hearn, M. G.,
    2. Hedrick, A.,
    3. Grigliatti, T. A. and
    4. Wakimoto, B. T.
    ( 1991). The effect of modifiers of position-effect variegation on the variegation of heterochromatic genes of Drosophila melanogaster. Genetics 128, 785– 797
    OpenUrlAbstract/FREE Full Text
    1. Henikoff, S.
    ( 1997). Nuclear organization and gene expression: homologous pairing and long-range interactions. Curr. Opin. Cell Biol 9, 388– 395
    OpenUrlCrossRefPubMedWeb of Science
    1. James, T. C.,
    2. Eissenberg, J. C.,
    3. Craig, C.,
    4. Dietrich, V.,
    5. Hobson, A. and
    6. Elgin, S. C.
    ( 1989). Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. Eur. J. Cell Biol 50, 170– 80
    OpenUrlPubMedWeb of Science
    1. Kellum, R.,
    2. Raff, J. W. and
    3. Alberts, B. M.
    ( 1995). Heterochromatin protein 1 distribution during development and during the cell cycle in Drosophila embryos. J. Cell Sci 108, 1407– 1418
    OpenUrlAbstract/FREE Full Text
    1. Le Douarin, B.,
    2. Nielsen, A. L.,
    3. Garnier, J. M.,
    4. Ichinose, H.,
    5. Jeanmougin, F.,
    6. Losson, R. and
    7. Chambon, P.
    ( 1996). A possible involvement of TIF1 alpha and TIF1 beta in the epigenetic control of transcription by nuclear receptors. EMBO J 15, 6701– 6715
    OpenUrlPubMedWeb of Science
    1. Lehming, N.,
    2. Le Saux, A.,
    3. Schuller, J. and
    4. Ptashne, M.
    ( 1998). Chromatin components as part of a putative transcriptional repressing complex. Proc. Nat. Acad. Sci. USA 95, 7322– 7326
    OpenUrlAbstract/FREE Full Text
    1. Murzina, N.,
    2. Verreault, A.,
    3. Laue, E. and
    4. Stillman, B.
    ( 1999). Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol. Cell 4, 529– 540
    OpenUrlCrossRefPubMedWeb of Science
    1. Pak, D. T.,
    2. Pflumm, M.,
    3. Chesnokov, I.,
    4. Huang, D. W.,
    5. Kellum, R.,
    6. Marr, J.,
    7. Romanowski, P. and
    8. Botchan, M. R.
    ( 1997). Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 91, 311– 323
    OpenUrlCrossRefPubMedWeb of Science
    1. Platero, J. S.,
    2. Hartnett, T. and
    3. Eissenberg, J. C.
    ( 1995). Functional analysis of the chromo domain of HP1. EMBO J 14, 3977– 3986
    OpenUrlPubMedWeb of Science
    1. Platero, J. S.,
    2. Csink, A. K.,
    3. Quintanilla, A. and
    4. Henikoff, S.
    ( 1998). Changes in chromosomal localization of heterochromatin-binding proteins during the cell cycle in Drosophila. J. Cell Biol 140, 1297– 1306
    OpenUrlAbstract/FREE Full Text
    1. Powers, J. A. and
    2. Eissenberg, J. C.
    ( 1993). Overlapping domains of the heterochromatin-associated protein HP1 mediate nuclear localization and heterochromatin binding. J. Cell Biol 120, 291– 299
    OpenUrlAbstract/FREE Full Text
    1. Real, M. D.,
    2. Ferre, J. and
    3. Mensua, J. L.
    ( 1985). Quantitative estimation of the red (drosopterins) and brown (xanthommatins) eye pigments of Drosophila melanogaster. DIS 61, 198– 199
    OpenUrl
    1. Reuter, G.,
    2. Giarre, M.,
    3. Farah, J.,
    4. Gausz, J.,
    5. Spierer, A. and
    6. Spierer, P.
    ( 1990). Dependence of position-effect variegation in Drosophila on dose of a gene encoding an unusual zinc-finger protein. Nature 344, 219– 223
    OpenUrlCrossRefPubMed
    1. Reuter, G. and
    2. Spierer, P.
    ( 1992). Position effect variegation and chromatin proteins. BioEssays 14, 605– 612
    OpenUrlCrossRefPubMedWeb of Science
    1. Ryan, R. F.,
    2. Schultz, D. C.,
    3. Ayyanathan, K.,
    4. Singh, P. B.,
    5. Friedman, J. R.,
    6. Fredericks, W. J. and
    7. Rauscher, F. J.
    ( 1999). KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Kruppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol. Cell Biol 19, 4366– 4378
    OpenUrlAbstract/FREE Full Text
    1. Saunders, W. S.,
    2. Chue, C.,
    3. Goebl, M.,
    4. Craig, C.,
    5. Clark, R. F.,
    6. Powers, J. A.,
    7. Eissenberg, J. C.,
    8. Elgin, S. C.,
    9. Rothfield, N. F. and
    10. Earnshaw, W. C.
    ( 1993). Molecular cloning of a human homologue of Drosophila heterochromatin protein HP1 using anti-centromere autoantibodies with anti-chromo specificity. J. Cell Sci 104, 573– 582
    OpenUrlAbstract/FREE Full Text
    1. Seeler, J. S.,
    2. Marchio, A.,
    3. Sitterlin, D.,
    4. Transy, C. and
    5. Dejean, A.
    ( 1998). Interaction of SP100 with HP1 proteins: a link between the promyelocytic leukemia-associated nuclear bodies and the chromatin compartment. Proc. Nat. Acad. Sci. USA 95, 7316– 7321
    OpenUrlAbstract/FREE Full Text
    1. Singh, P. B.,
    2. Miller, J. R.,
    3. Pearce, J.,
    4. Kothary, R.,
    5. Burton, R. D.,
    6. Paro, R.,
    7. James, T. C. and
    8. Gaunt, S. J.
    ( 1991). A sequence motif found in a Drosophila heterochromatin protein is conserved in animals and plants. Nucl. Acids Res 19, 789– 794
    OpenUrlAbstract/FREE Full Text
    1. Slatis, H. M.
    ( 1955). A reconsideration of the brown -dominant position effect. Genetics 40, 246– 251
    OpenUrlFREE Full Text
    1. Smothers, J. F. and
    2. Henikoff, S.
    ( 2000). The HP1 chromo shadow domain binds a consensus peptide pentamer. Curr. Biol 10, 27– 30
    OpenUrlCrossRefPubMedWeb of Science
    1. Talbert, P. B. and
    2. Henikoff, S.
    ( 2000). A reexamination of spreading of position-effect variegation in the white-roughest region of Drosophila melanogaster. Genetics 154, 259– 272
    OpenUrlAbstract/FREE Full Text
    1. Tschiersch, B.,
    2. Hofmann, A.,
    3. Krauss, V.,
    4. Dorn, R.,
    5. Korge, G. and
    6. Reuter, G.
    ( 1994). The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J 13, 3822– 3831
    OpenUrlPubMedWeb of Science
    1. Wakimoto, B. T. and
    2. Hearn, M. G.
    ( 1990). The effects of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L of Drosophila melanogaster. Genetics 125, 141– 154
    OpenUrlAbstract/FREE Full Text
    1. Weiler, K. S. and
    2. Wakimoto, B. T.
    ( 1995). Heterochromatin and gene expression in Drosophila. Annu. Rev. Genet 29, 577– 605
    OpenUrlCrossRefPubMedWeb of Science
    1. Wreggett, K. A.,
    2. Hill, F.,
    3. James, P. S.,
    4. Hutchings, A.,
    5. Butcher, G. W. and
    6. Singh, P. B.
    ( 1994). A mammalian homologue of Drosophila heterochromatin protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenet. Cell Genet 66, 99– 103
    OpenUrlCrossRefPubMedWeb of Science
    1. Ye, Q. and
    2. Worman, H. J.
    ( 1996). Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J. Biol. Chem 271, 14653– 14656
    OpenUrlAbstract/FREE Full Text
    1. Ye, Q.,
    2. Callebaut, I.,
    3. Pezhman, A.,
    4. Courvalin, J. C. and
    5. Worman, H. J.
    ( 1997). Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J. Biol. Chem 272, 14983– 14989
    OpenUrlAbstract/FREE Full Text
    1. Zhao, T.,
    2. Heyduk, T.,
    3. Allis, C. D. and
    4. Eissenberg, J. C.
    ( 2000). Heterochromatin protein 1 (HP1 binds to nucleosomes and DNA in vitro. J. Biol Chem 275, 28332– 28338
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
Journal Article
The genomic silencing of position-effect variegation in Drosophila melanogaster: interaction between the heterochromatin-associated proteins Su(var)3-7 and HP1
M. Delattre, A. Spierer, C.H. Tonka, P. Spierer
Journal of Cell Science 2000 113: 4253-4261;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

2020 at The Company of Biologists

Despite the challenges of 2020, we were able to bring a number of long-term projects and new ventures to fruition. While we look forward to a new year, join us as we reflect on the triumphs of the last 12 months.

Mole – The Corona Files

"This is not going to go away, 'like a miracle.' We have to do magic. And I know we can."

Mole continues to offer his wise words to researchers on how to manage during the COVID-19 pandemic.

Cell scientist to watch – Christine Faulkner

In an interview, Christine Faulkner talks about where her interest in plant science began, how she found the transition between Australia and the UK, and shares her thoughts on virtual conferences.

Read & Publish participation extends worldwide

“The clear advantages are rapid and efficient exposure and easy access to my article around the world. I believe it is great to have this publishing option in fast-growing fields in biomedical research.”

Dr Jaceques Behmoaras (Imperial College London) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 60 institutions in 12 countries taking part – find out more and view our full list of participating institutions.

JCS and COVID-19

For more information on measures Journal of Cell Science is taking to support the community during the COVID-19 pandemic, please see here.

If you have any questions or concerns, please do not hestiate to contact the Editorial Office.