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Gómez R.AuthorViera A.AuthorSuja J.a.Author

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Article

Dynamic localization of SMC5/6 complex proteins during mammalian meiosis and mitosis suggests functions in distinct chromosome processes

Publicated to:JOURNAL OF CELL SCIENCE. 126 (18): 4239-4252 - 2013-09-15 126(18), DOI: 10.1242/jcs.130195

Authors: Gomez, Rocio; Jordan, Philip W; Viera, Alberto; Alsheimer, Manfred; Fukuda, Tomoyuki; Jessberger, Rolf; Llano, Elena; Pendas, Alberto M; Handel, Mary Ann; Suja, Jose A

Affiliations

Departamento de Biología; Universidad Autonoma de Madrid; E-28049 Madrid; Spain - Author
Department of Cell and Developmental Biology; University of Würzburg; D-97074 Würzburg; Germany - Author
Department of Cell and Molecular Biology; Karolinska Institutet; SE-17177 Stockholm; Sweden - Author
Inst Biol Mol & Celular Canc, E-37007 Salamanca, Spain - Author
Institute of Physiological Chemistry; Dresden University of Technology; D-01307 Dresden; Germany - Author
Instituto de Biología Molecular y Celular del Cáncer; E-37007 Salamanca; Spain - Author
Jackson Lab, Bar Harbor, ME 04609 USA - Author
Karolinska Inst, Dept Cell & Mol Biol, SE-17177 Stockholm, Sweden - Author
Tech Univ Dresden, Inst Physiol Chem, D-01307 Dresden, Germany - Author
The Jackson Laboratory; Bar Harbor; Maine 04609; United States - Author
The Jackson Laboratory; Bar Harbor; Maine 04609; United States; Biochemistry and Molecular Biology Department; Johns Hopkins School of Public Health; Baltimore; MD 21205; United States - Author
Univ Autonoma Madrid, Dept Biol, E-28049 Madrid, Spain - Author
Univ Wurzburg, Dept Cell & Dev Biol, D-97074 Wurzburg, Germany - Author
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Abstract

Four members of the structural maintenance of chromosome (SMC) protein family have essential functions in chromosome condensation (SMC2/4) and sister-chromatid cohesion (SMC1/3). The SMC5/6 complex has been implicated in chromosome replication, DNA repair and chromosome segregation in somatic cells, but its possible functions during mammalian meiosis are unknown. Here, we show in mouse spermatocytes that SMC5 and SMC6 are located at the central region of the synaptonemal complex from zygotene until diplotene. During late diplotene both proteins load to the chromocenters, where they colocalize with DNA Topoisomerase IIα, and then accumulate at the inner domain of the centromeres during the first and second meiotic divisions. Interestingly, SMC6 and DNA Topoisomerase IIα colocalize at stretched strands that join kinetochores during the metaphase II to anaphase II transition, and both are observed on stretched lagging chromosomes at anaphase II following treatment with Etoposide. During mitosis, SMC6 and DNA Topoisomerase IIα colocalize at the centromeres and chromatid axes. Our results are consistent with the participation of SMC5 and SMC6 in homologous chromosome synapsis during prophase I, chromosome and centromere structure during meiosis I and mitosis and, with DNA Topoisomerase IIα, in regulating centromere cohesion during meiosis II. © 2013. Published by The Company of Biologists Ltd.

Keywords

centromeredna topoisomerase ii?dna topoisomerase iiαmeiosismitosismousesmc5smc63t3 cellsAnaphaseAnimal cellAnimalsArticleCell cycle proteinsCentromereChromatidChromosomal proteins, non-histoneChromosomeChromosome condensationChromosome pairingChromosome proteinChromosome replicationChromosome segregationDna repairDna topoisomerase (atp hydrolysing)Dna topoisomerase ii?Dna topoisomerase iiαEtoposideGerm cellsHumansMammalsMeiosisMeiotic prophase iMetaphaseMiceMitosisMouseNonhumanPriority journalProphaseProtein expressionProtein localizationSex chromosomeSister chromatidSmc5Smc5 protein, humanSmc6SpermatocyteSpermatogenesisStructural maintenance of chromosome 5Structural maintenance of chromosome 6Synaptonemal complexUnclassified drug

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal JOURNAL OF CELL SCIENCE 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, 2013, it was in position 46/185, thus managing to position itself as a Q1 (Primer Cuartil), in the category Cell Biology.

From a relative perspective, and based on the normalized impact indicator calculated from the Field Citation Ratio (FCR) of the Dimensions source, it yields a value of: 3.82, which 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: Dimensions Jun 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-06-30, the following number of citations:

  • WoS: 41
  • Scopus: 40
  • Europe PMC: 38

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 2025-06-30:

  • 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: 76.
  • 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: 76 (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: 0.5.
  • The number of mentions on the social network X (formerly Twitter): 1 (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: Germany; Sweden; United States of America.

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 (GOMEZ LENCERO, ROCIO) and Last Author (SUJA SANCHEZ, JOSE ANGEL).