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Ministerio de Economia y Competitividad SAF2013-45111-R Isabel Lopez de SilanesConsejeria de Educacion, Juventud y Deporte, Comunidad de Madrid S2017/BMD-3770 Juan J Montero Maria A BlascoWorld Cancer Research Fund 16-1177 Maria A BlascoFundacion Botin Maria A BlascoMinisterio de Economia y Competitividad SAF2015-72455-EXP Maria A BlascoThe funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Analysis of institutional authors

Grana-Castre, OsvaldoAuthor

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May 10, 2023
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TERRA, regulate the transcriptional landscape of pluripotent cells through TRF1-dependent recruitment of PRC2

Publicated to:Elife. 8 e44656- - 2019-08-20 8(), DOI: 10.7554/eLife.44656

Authors: Maria Marion, Rosa; Montero, Juan J; Lopez de Silanes, Isabel; Grana-Castre, Osvaldo; Martinez, Paula; Schoeftner, Stefan; Alejandro Palacios-Fabrega, Jose; Blasco, Maria A

Affiliations

Astellas Pharma Europe Ltd, Chertsey, England - Author
LNCIB, Gen Stabil Unit, Trieste, Italy - Author
Spanish Natl Canc Ctr CNIO, Bioinformat Unit, Struct Biol Program, Madrid, Spain - Author
Spanish Natl Canc Ctr CNIO, Mol Oncol Program, Telomeres & Telomerase Grp, Madrid, Spain - Author
Univ Trieste, Dept Life Sci, Trieste, Italy - Author
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Abstract

The mechanisms that regulate pluripotency are still largely unknown. Here, we show that Telomere Repeat Binding Factor 1 (TRF1), a component of the shelterin complex, regulates the genome-wide binding of polycomb and polycomb H3K27me3 repressive marks to pluripotency genes, thereby exerting vast epigenetic changes that contribute to the maintenance of mouse ES cells in a naive state. We further show that TRF1 mediates these effects by regulating TERRA, the lncRNAs transcribed from telomeres. We find that TERRAs are enriched at polycomb and stem cell genes in pluripotent cells and that TRF1 abrogation results in increased TERRA levels and in higher TERRA binding to those genes, coincidental with the induction of cell-fate programs and the loss of the naive state. These results are consistent with a model in which TRF1-dependent changes in TERRA levels modulate polycomb recruitment to pluripotency and differentiation genes. These unprecedented findings explain why TRF1 is essential for the induction and maintenance of pluripotency.

Keywords

AnimalsCell differentiationCells, culturedChromosomesDevelopmental regulatorsEpigenesis, geneticEpigenetic regulationGeneGene expressionInduced pluripotent stem cellsLncrnaMammalian telomeresMiceMousePluripotencyPolycombPolycomb complexesPolycomb repressive complex 2ProteinsRegenerative medicineRnaRna, long noncodingSet enrichment analysisStem cellsTelomereTelomere-lengthTelomeric repeat binding protein 1TerraTranscription, geneticTrf1Web server

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Elife due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2019, it was in position 5/93, thus managing to position itself as a Q1 (Primer Cuartil), in the category Biology. Notably, the journal is positioned above the 90th percentile.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 1.84. This indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: ESI Nov 14, 2024)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

  • Weighted Average of Normalized Impact by the Scopus agency: 1.27 (source consulted: FECYT Feb 2024)
  • Field Citation Ratio (FCR) from Dimensions: 5.28 (source consulted: Dimensions Jul 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-07-16, the following number of citations:

  • WoS: 37
  • Scopus: 39
  • Europe PMC: 30

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-07-16:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 72.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 73 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 68.25.
  • The number of mentions on the social network Facebook: 1 (Altmetric).
  • The number of mentions on the social network X (formerly Twitter): 5 (Altmetric).
  • The number of mentions in news outlets: 8 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Italy; United Kingdom.