Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity

We investigated the influence of telomere proximity and composition on the expression of an EGFP reporter gene in human cells. In transient transfection assays, telomeric DNA does not repress EGFP but rather slightly increases its expression. In contrast, in stable cell lines, the same reporter cons...

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Vydané v:EMBO reports Ročník 3; číslo 11; s. 1055 - 1061
Hlavní autori: Koering, Catherine Elaine, Pollice, Alessandra, Zibella, Maria Pia, Bauwens, Serge, Puisieux, Alain, Brunori, Michele, Brun, Christine, Martins, Luis, Sabatier, Laure, Pulitzer, John F., Gilson, Eric
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: Chichester, UK John Wiley & Sons, Ltd 01.11.2002
Nature Publishing Group UK
Springer Nature B.V
EMBO Press
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ISSN:1469-221X, 1469-3178
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Abstract We investigated the influence of telomere proximity and composition on the expression of an EGFP reporter gene in human cells. In transient transfection assays, telomeric DNA does not repress EGFP but rather slightly increases its expression. In contrast, in stable cell lines, the same reporter construct is repressed when inserted at a subtelomeric location. The telomeric repression is transiently alleviated by increasing the dosage of the TTAGGG repeat factor 1 (TRF1). Upon a prolongated treatment with trichostatin A, the derepression of the subtelomeric reporter gene correlates with the delocalization of HP1α and HP1β. In contrast, treating the cells with 5 azacytidin, a demethylating agent, or with sirtinol, an inhibitor of the Sir2 family of deacetylase, has no apparent effect on telomeric repression. Overall, position effects at human chromosome ends are dependent on a specific higher‐order organization of the telomeric chromatin. The possible involvement of HP1 isoforms is discussed.
AbstractList We investigated the influence of telomere proximity and composition on the expression of an EGFP reporter gene in human cells. In transient transfection assays, telomeric DNA does not repress EGFP but rather slightly increases its expression. In contrast, in stable cell lines, the same reporter construct is repressed when inserted at a subtelomeric location. The telomeric repression is transiently alleviated by increasing the dosage of the TTAGGG repeat factor 1 (TRF1). Upon a prolongated treatment with trichostatin A, the derepression of the subtelomeric reporter gene correlates with the delocalization of HP1[alpha] and HP1[beta]. In contrast, treating the cells with 5 azacytidin, a demethylating agent, or with sirtinol, an inhibitor of the Sir2 family of deacetylase, has no apparent effect on telomeric repression. Overall, position effects at human chromosome ends are dependent on a specific higher-order organization of the telomeric chromatin. The possible involvement of HP1 isoforms is discussed.
We investigated the influence of telomere proximity and composition on the expression of an EGFP reporter gene in human cells. In transient transfection assays, telomeric DNA does not repress EGFP but rather slightly increases its expression. In contrast, in stable cell lines, the same reporter construct is repressed when inserted at a subtelomeric location. The telomeric repression is transiently alleviated by increasing the dosage of the TTAGGG repeat factor 1 (TRF1). Upon a prolongated treatment with trichostatin A, the derepression of the subtelomeric reporter gene correlates with the delocalization of HP1alpha and HP1beta. In contrast, treating the cells with 5 azacytidin, a demethylating agent, or with sirtinol, an inhibitor of the Sir2 family of deacetylase, has no apparent effect on telomeric repression. Overall, position effects at human chromosome ends are dependent on a specific higher-order organization of the telomeric chromatin. The possible involvement of HP1 isoforms is discussed.
We investigated the influence of telomere proximity and composition on the expression of an EGFP reporter gene in human cells. In transient transfection assays, telomeric DNA does not repress EGFP but rather slightly increases its expression. In contrast, in stable cell lines, the same reporter construct is repressed when inserted at a subtelomeric location. The telomeric repression is transiently alleviated by increasing the dosage of the TTAGGG repeat factor 1 (TRF1). Upon a prolongated treatment with trichostatin A, the derepression of the subtelomeric reporter gene correlates with the delocalization of HP1α and HP1β. In contrast, treating the cells with 5 azacytidin, a demethylating agent, or with sirtinol, an inhibitor of the Sir2 family of deacetylase, has no apparent effect on telomeric repression. Overall, position effects at human chromosome ends are dependent on a specific higher‐order organization of the telomeric chromatin. The possible involvement of HP1 isoforms is discussed.
We investigated the influence of telomere proximity and composition on the expression of an EGFP reporter gene in human cells. In transient transfection assays, telomeric DNA does not repress EGFP but rather slightly increases its expression. In contrast, in stable cell lines, the same reporter construct is repressed when inserted at a subtelomeric location. The telomeric repression is transiently alleviated by increasing the dosage of the TTAGGG repeat factor 1 (TRF1). Upon a prolongated treatment with trichostatin A, the derepression of the subtelomeric reporter gene correlates with the delocalization of HP1α and HP1β. In contrast, treating the cells with 5 azacytidin, a demethylating agent, or with sirtinol, an inhibitor of the Sir2 family of deacetylase, has no apparent effect on telomeric repression. Overall, position effects at human chromosome ends are dependent on a specific higher-order organization of the telomeric chromatin. The possible involvement of HP1 isoforms is discussed.
We investigated the influence of telomere proximity and composition on the expression of an EGFP reporter gene in human cells. In transient transfection assays, telomeric DNA does not repress EGFP but rather slightly increases its expression. In contrast, in stable cell lines, the same reporter construct is repressed when inserted at a subtelomeric location. The telomeric repression is transiently alleviated by increasing the dosage of the TTAGGG repeat factor 1 (TRF1). Upon a prolongated treatment with trichostatin A, the derepression of the subtelomeric reporter gene correlates with the delocalization of HP1alpha and HP1beta. In contrast, treating the cells with 5 azacytidin, a demethylating agent, or with sirtinol, an inhibitor of the Sir2 family of deacetylase, has no apparent effect on telomeric repression. Overall, position effects at human chromosome ends are dependent on a specific higher-order organization of the telomeric chromatin. The possible involvement of HP1 isoforms is discussed.We investigated the influence of telomere proximity and composition on the expression of an EGFP reporter gene in human cells. In transient transfection assays, telomeric DNA does not repress EGFP but rather slightly increases its expression. In contrast, in stable cell lines, the same reporter construct is repressed when inserted at a subtelomeric location. The telomeric repression is transiently alleviated by increasing the dosage of the TTAGGG repeat factor 1 (TRF1). Upon a prolongated treatment with trichostatin A, the derepression of the subtelomeric reporter gene correlates with the delocalization of HP1alpha and HP1beta. In contrast, treating the cells with 5 azacytidin, a demethylating agent, or with sirtinol, an inhibitor of the Sir2 family of deacetylase, has no apparent effect on telomeric repression. Overall, position effects at human chromosome ends are dependent on a specific higher-order organization of the telomeric chromatin. The possible involvement of HP1 isoforms is discussed.
Author Sabatier, Laure
Gilson, Eric
Zibella, Maria Pia
Koering, Catherine Elaine
Pollice, Alessandra
Bauwens, Serge
Brun, Christine
Martins, Luis
Brunori, Michele
Puisieux, Alain
Pulitzer, John F.
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  organization: Laboratoire de Biologie Moléculaire et Cellulaire, UMR5665, Centre National de la Recherche Scientifique, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, cedex 07, 69364, Lyon, France
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  givenname: Alessandra
  surname: Pollice
  fullname: Pollice, Alessandra
  email: eric.gilson@ens-lyon.fr
  organization: Università degli Studi di Napoli Federico II, Dipartimento di Genetica, Biologia Generale e Molecolare, via Mezzocannone 8, 80134, Naples, Italy
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  givenname: Maria Pia
  surname: Zibella
  fullname: Zibella, Maria Pia
  organization: Università degli Studi di Napoli Federico II, Dipartimento di Genetica, Biologia Generale e Molecolare, via Mezzocannone 8, 80134, Naples, Italy
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  surname: Bauwens
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  organization: Unite d'Oncologie Moleculaire, Centre Leon Berard, 28 rue Laennec, cedex 08, 69373, Lyon, France
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  fullname: Puisieux, Alain
  organization: Unite d'Oncologie Moleculaire, Centre Leon Berard, 28 rue Laennec, cedex 08, 69373, Lyon, France
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  surname: Brunori
  fullname: Brunori, Michele
  organization: Laboratoire de Biologie Moléculaire et Cellulaire, UMR5665, Centre National de la Recherche Scientifique, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, cedex 07, 69364, Lyon, France
– sequence: 7
  givenname: Christine
  surname: Brun
  fullname: Brun, Christine
  organization: Laboratoire de Biologie Moléculaire et Cellulaire, UMR5665, Centre National de la Recherche Scientifique, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, cedex 07, 69364, Lyon, France
– sequence: 8
  givenname: Luis
  surname: Martins
  fullname: Martins, Luis
  organization: CEA (Commissariat a l'Energie Atomique), Laboratoire de Radiobiologie et Oncologie, BP6, Fontenay-aux-Roses, France
– sequence: 9
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  surname: Sabatier
  fullname: Sabatier, Laure
  organization: CEA (Commissariat a l'Energie Atomique), Laboratoire de Radiobiologie et Oncologie, BP6, Fontenay-aux-Roses, France
– sequence: 10
  givenname: John F.
  surname: Pulitzer
  fullname: Pulitzer, John F.
  organization: Università degli Studi di Napoli Federico II, Dipartimento di Genetica, Biologia Generale e Molecolare, via Mezzocannone 8, 80134, Naples, Italy
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  givenname: Eric
  surname: Gilson
  fullname: Gilson, Eric
  email: eric.gilson@ens-lyon.fr
  organization: Laboratoire de Biologie Moléculaire et Cellulaire, UMR5665, Centre National de la Recherche Scientifique, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, cedex 07, 69364, Lyon, France
BackLink https://www.ncbi.nlm.nih.gov/pubmed/12393752$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright European Molecular Biology Organization 2002
Copyright © 2002 European Molecular Biology Organization
Copyright Oxford University Press(England) Nov 15, 2002
Distributed under a Creative Commons Attribution 4.0 International License
Copyright © 2002, European Molecular Biology Organization 2002
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– notice: Copyright © 2002 European Molecular Biology Organization
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– notice: Distributed under a Creative Commons Attribution 4.0 International License
– notice: Copyright © 2002, European Molecular Biology Organization 2002
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References_xml – reference: Harrison, J.J., Anisowicz, A., Gadi, I.K., Raffeld, M. and Sager, R. (1983) Azacytidine-induced tumorigenesis of CHEF/18 cells: correlated DNA methylation and chromosome changes. Proc. Natl Acad. Sci. USA, 80, 6606-6610.
– reference: Chong, L., van Steensel, B., Broccoli, D., Erdjument-Bromage, H., Hanish, J., Tempst, P. and de Lange, T. (1995) A human telomeric protein. Science, 270, 1663-1667.
– reference: Fourel, G., Revardel, E., Koering, C.E. and Gilson, E. (1999) Cohabitation of insulators and silencing elements in yeast subtelomeric regions. EMBO J., 18, 2522-2537.
– reference: Baur, J.A., Zou, Y., Shay, J.W. and Wright, W.E. (2001) Telomere position effect in human cells. Science, 292, 2075-2077.
– reference: Lundblad, V. (2000) DNA ends: maintenance of chromosome termini versus repair of double strand breaks. Mutat. Res., 451, 227-240.
– reference: Gottschling, D.E., Aparicio, O.M., Billington, B.L. and Zakian, V.A. (1990) Position effect at S. cerevisiae telomeres: reversible represssion of Pol II transcription. Cell, 63, 751-762.
– reference: Ofir, R., Wong, A.C., McDermid, H.E., Skorecki, K.L. and Selig, S. (1999) Position effect of human telomeric repeats on replication timing. Proc. Natl Acad. Sci. USA, 96, 11434-11439.
– reference: Waltzer, L., Perricaudet, M., Sergeant, A. and Manet, E. (1996) Epstein-Barr virus EBNA3A and EBNA3C proteins both repress RBP-J κ-EBNA2-activated transcription by inhibiting the binding of RBP-J κ to DNA. J. Virol., 70, 5909-5915.
– reference: Minc, E., Allory, Y., Worman, H.J., Courvalin, J.C. and Buendia, B. (1999) Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma, 108, 220-234.
– reference: Smith, Z.E. and Higgs, D.R. (1999) The pattern of replication at a human telomeric region (16p13.3): its relationship to chromosome structure and gene expression. Hum. Mol. Genet., 8, 1373-1386.
– reference: Cryderman, D.E., Morris, E.J., Biessmann, H., Elgin, S.C. and Wallrath, L.L. (1999) Silencing at Drosophila telomeres: nuclear organization and chromatin structure play critical roles. EMBO J., 18, 3724-3735.
– reference: van Steensel, B. and de Lange, T. (1997) Control of telomere length by the human telomeric protein TRF1. Nature, 385, 740-743.
– reference: Aagaard, L., Schmid, M., Warburton, P. and Jenuwein, T. (2000) Mitotic phosphorylation of SUV39H1, a novel component of active centromeres, coincides with transient accumulation at mammalian centromeres. J. Cell Sci., 113, 817-829.
– reference: Blackburn, E.H. (2000) The end of the (DNA) line. Nat. Struct. Biol., 7, 847-850.
– reference: Bayne, R.A., Broccoli, D., Taggart, M.H., Thomson, E.J., Farr, C.J. and Cooke, H.J. (1994) Sandwiching of a gene within 12 kb of a functional telomere and α satellite does not result in silencing. Hum. Mol. Genet., 3, 539-546.
– reference: Grozinger, C.M., Chao, E.D., Blackwell, H.E., Moazed, D. and Schreiber, S.L. (2001) Identification of a class of small molecule inhibitors of the sirtuin family of NAD-dependent deacetylases by phenotypic screening. J. Biol. Chem., 276, 38837-38843.
– reference: Bilaud, T., Koering, C.E., Binet-Brasselet, E., Ancelin, K., Pollice, A., Gasser, S.M. and Gilson, E. (1996) The telobox, a Myb-related telomeric DNA binding motif found in proteins from yeast, plants and human. Nucleic Acids Res., 24, 1294-1303.
– reference: Hanish, J.P., Yanowitz, J.L. and de Lange, T. (1994) Stringent sequence requirements for the formation of human telomeres. Proc. Natl Acad. Sci. USA, 91, 8861-8865.
– reference: Gabellini, D., Green, M.R. and Tupler, R. (2002) Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscles. Cell, 110, 339-348.
– reference: Vassetzky, N.S., Gaden, F., Brun, C., Gasser, S.M. and Gilson, E. (1999) Taz1p and Teb1p, two telobox proteins in Schizosaccharomyces pombe, recognize different telomere-related DNA sequences. Nucleic Acids Res., 27, 4687-4694.
– reference: Brown, K.E., Guest, S.S., Smale, S.T., Hahm, K., Merkenschlager, M. and Fisher, A.G. (1997) Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell, 91, 845-854.
– reference: Chen, C. and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol., 7, 2745-2752.
– reference: Farr, C., Fantes, J., Goodfellow, P. and Cooke, H. (1991) Functional reintroduction of human telomeres into mammalian cells. Proc. Natl Acad. Sci. USA, 88, 7006-7010.
– reference: Ferguson, B.M. and Fangman, W.L. (1992) A position effect on the time of replication origin activation in yeast. Cell, 68, 333-339.
– reference: Taddei, A., Maison, C., Roche, D. and Almouzni, G. (2001) Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat. Cell Biol., 3, 114-120.
– reference: Nimmo, E.R.N., Cranston, G. and Allshire, R.C. (1994) Telomere-associated chromosome breakage in fission yeast results in variegated expression of adjacent genes. EMBO J., 13, 3801-3811.
– reference: Yoshida, M., Kijima, M., Akita, M. and Beppu, T. (1990) Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J. Biol. Chem., 265, 17174-17179.
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– reference: Wright, W.E., Tesmer, V.M., Liao, M.L. and Shay, J.W. (1999) Normal human telomeres are not late replicating. Exp. Cell Res., 251, 492-499.
– reference: Sprung, C.N., Sabatier, L. and Murnane, J.P. (1996) Effect of telomere length on telomeric gene expression. Nucleic Acids Res., 24, 4336-4340.
– reference: Pryde, F.E. and Louis, E.J. (1999) Limitations of silencing at native yeast telomeres. EMBO J., 18, 2538-2550.
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Snippet We investigated the influence of telomere proximity and composition on the expression of an EGFP reporter gene in human cells. In transient transfection...
We investigated the influence of telomere proximity and composition on the expression of an EGFP reporter gene in human cells. In transient transfection...
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StartPage 1055
SubjectTerms Biochemistry, Molecular Biology
Bioinformatics
Chromatin - metabolism
Chromosomes, Human - metabolism
Computer Science
Gene Expression Regulation
Gene Silencing
Genes, Reporter
Humans
Life Sciences
Molecular biology
Scientific Report
Telomere - metabolism
Telomeric Repeat Binding Protein 1 - genetics
Telomeric Repeat Binding Protein 1 - metabolism
Tumor Cells, Cultured
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Title Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity
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