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Grant support

This work has been supported by the Spanish Ministry of Economy, Industry and Competitiveness (MEIC) to the EMBL partnership, the Centro de Excelencia Severo Ochoa, the CERCA Programme/Generalitat de Catalunya, and the project PGC2018-101271-B-I00 of the Agencia Estatal de Investigacion (AEI/10.13039/501100011033/FEDER, UE). This work has also been partially supported by the Italian Ministry of Health with Ricerca Corrente and 5x1000 funds. We thank Juan Valcarcel and Fran Supek for their comments and suggestions.

Analysis of institutional authors

Benisty, HCorresponding AuthorHernandez-Alias, XAuthorWeber, MAuthorAnglada-Girotto, MAuthorMantica, FAuthorRadusky, LAuthorCalvet, FAuthorWeghorn, DAuthorIrimia, MAuthorSerrano, LCorresponding Author

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June 7, 2023
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Article

Genes enriched in A/T-ending codons are co-regulated and conserved across mammals

Publicated to:Cell Systems. 14 (4): 312-+ - 2023-04-19 14(4), DOI: 10.1016/j.cels.2023.02.002

Authors: Benisty, H; Hernandez-Alias, X; Weber, M; Anglada-Girotto, M; Mantica, F; Radusky, L; Senger, G; Calvet, F; Weghorn, D; Irimia, M; Schaefer, MH; Serrano, L

Affiliations

Barcelona Inst Sci & Technol, Ctr Genom Regulat CRG, Dr Aiguader 88, Barcelona 08003, Spain - Author
European Inst Oncol IEO IRCCS, Dept Expt Oncol, Via Adamello 16, I-20139 Milan, Italy - Author
ICREA, Pg Lluis Co 23, Barcelona 08010, Spain - Author
Univ Pompeu Fabra UPF, Barcelona 08003, Spain - Author

Abstract

Codon usage influences gene expression distinctly depending on the cell context. Yet, the importance of codon bias in the simultaneous turnover of specific groups of protein-coding genes remains to be investi-gated. Here, we find that genes enriched in A/T-ending codons are expressed more coordinately in general and across tissues and development than those enriched in G/C-ending codons. tRNA abundance measure-ments indicate that this coordination is linked to the expression changes of tRNA isoacceptors reading A/T-ending codons. Genes with similar codon composition are more likely to be part of the same protein complex, especially for genes with A/T-ending codons. The codon preferences of genes with A/T-ending codons are conserved among mammals and other vertebrates. We suggest that this orchestration contributes to tissue -specific and ontogenetic-specific expression, which can facilitate, for instance, timely protein complex for-mation.

Keywords

a/t-ending codonsco-regulationcodon usageconservationdevelopmentmammalsras genessynonymous codonstrnaA/t-ending codonsAdaptationAnimalsCo-regulationCodonCodon usageConservationDevelopmentEvolutionExpressionIsochoresMammalsProliferationRas genesRegionsRna, transferSelectionSynonymous codonsSynonymous mutationsTranslationTranslation efficiencyTrnaUsage biasVertebrates

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Cell Systems 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, 2023, it was in position 28/313, thus managing to position itself as a Q1 (Primer Cuartil), in the category Biochemistry & Molecular 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: 1.37. 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:

  • Field Citation Ratio (FCR) from Dimensions: 7.3 (source consulted: Dimensions Jul 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-07-25, the following number of citations:

  • WoS: 9
  • Europe PMC: 8

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 2025-07-25:

  • 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: 15.
  • 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: 13 (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: 16.7.
  • The number of mentions on the social network X (formerly Twitter): 23 (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.

There is a significant leadership presence as some of the institution’s authors appear as the first or last signer, detailed as follows: First Author (BENISTY, HANNAH) and Last Author (SERRANO PUBUL, LUIS).

the authors responsible for correspondence tasks have been BENISTY, HANNAH and SERRANO PUBUL, LUIS.