Distinct roles of haspin in stem cell division and male gametogenesis

Abstract The kinase haspin phosphorylates histone H3 at threonine-3 (H3T3ph) during mitosis. H3T3ph provides a docking site for the Chromosomal Passenger Complex at the centromere, enabling correction of erratic microtubule-chromosome contacts. Although this mechanism is operational in all dividing...

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Autores principales: Katerina Soupsana, Eleftheria Karanika, Fani Kiosse, Anastasia Christogianni, Yiorgos Sfikas, Pantelis Topalis, Anna Batistatou, Zoi Kanaki, Apostolos Klinakis, Anastasia S. Politou, Spyros Georgatos
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Publicado: Nature Portfolio 2021
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spelling oai:doaj.org-article:55980d2f4450420aa4ca54db29566fe12021-12-02T18:37:08ZDistinct roles of haspin in stem cell division and male gametogenesis10.1038/s41598-021-99307-82045-2322https://doaj.org/article/55980d2f4450420aa4ca54db29566fe12021-10-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-99307-8https://doaj.org/toc/2045-2322Abstract The kinase haspin phosphorylates histone H3 at threonine-3 (H3T3ph) during mitosis. H3T3ph provides a docking site for the Chromosomal Passenger Complex at the centromere, enabling correction of erratic microtubule-chromosome contacts. Although this mechanism is operational in all dividing cells, haspin-null mice do not exhibit developmental anomalies, apart from aberrant testis architecture. Investigating this problem, we show here that mouse embryonic stem cells that lack or overexpress haspin, albeit prone to chromosome misalignment during metaphase, can still divide, expand and differentiate. RNA sequencing reveals that haspin dosage affects severely the expression levels of several genes that are involved in male gametogenesis. Consistent with a role in testis-specific expression, H3T3ph is detected not only in mitotic spermatogonia and meiotic spermatocytes, but also in non-dividing cells, such as haploid spermatids. Similarly to somatic cells, the mark is erased in the end of meiotic divisions, but re-installed during spermatid maturation, subsequent to methylation of histone H3 at lysine-4 (H3K4me3) and arginine-8 (H3R8me2). These serial modifications are particularly enriched in chromatin domains containing histone H3 trimethylated at lysine-27 (H3K27me3), but devoid of histone H3 trimethylated at lysine-9 (H3K9me3). The unique spatio-temporal pattern of histone H3 modifications implicates haspin in the epigenetic control of spermiogenesis.Katerina SoupsanaEleftheria KaranikaFani KiosseAnastasia ChristogianniYiorgos SfikasPantelis TopalisAnna BatistatouZoi KanakiApostolos KlinakisAnastasia S. PolitouSpyros GeorgatosNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-20 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Katerina Soupsana
Eleftheria Karanika
Fani Kiosse
Anastasia Christogianni
Yiorgos Sfikas
Pantelis Topalis
Anna Batistatou
Zoi Kanaki
Apostolos Klinakis
Anastasia S. Politou
Spyros Georgatos
Distinct roles of haspin in stem cell division and male gametogenesis
description Abstract The kinase haspin phosphorylates histone H3 at threonine-3 (H3T3ph) during mitosis. H3T3ph provides a docking site for the Chromosomal Passenger Complex at the centromere, enabling correction of erratic microtubule-chromosome contacts. Although this mechanism is operational in all dividing cells, haspin-null mice do not exhibit developmental anomalies, apart from aberrant testis architecture. Investigating this problem, we show here that mouse embryonic stem cells that lack or overexpress haspin, albeit prone to chromosome misalignment during metaphase, can still divide, expand and differentiate. RNA sequencing reveals that haspin dosage affects severely the expression levels of several genes that are involved in male gametogenesis. Consistent with a role in testis-specific expression, H3T3ph is detected not only in mitotic spermatogonia and meiotic spermatocytes, but also in non-dividing cells, such as haploid spermatids. Similarly to somatic cells, the mark is erased in the end of meiotic divisions, but re-installed during spermatid maturation, subsequent to methylation of histone H3 at lysine-4 (H3K4me3) and arginine-8 (H3R8me2). These serial modifications are particularly enriched in chromatin domains containing histone H3 trimethylated at lysine-27 (H3K27me3), but devoid of histone H3 trimethylated at lysine-9 (H3K9me3). The unique spatio-temporal pattern of histone H3 modifications implicates haspin in the epigenetic control of spermiogenesis.
format article
author Katerina Soupsana
Eleftheria Karanika
Fani Kiosse
Anastasia Christogianni
Yiorgos Sfikas
Pantelis Topalis
Anna Batistatou
Zoi Kanaki
Apostolos Klinakis
Anastasia S. Politou
Spyros Georgatos
author_facet Katerina Soupsana
Eleftheria Karanika
Fani Kiosse
Anastasia Christogianni
Yiorgos Sfikas
Pantelis Topalis
Anna Batistatou
Zoi Kanaki
Apostolos Klinakis
Anastasia S. Politou
Spyros Georgatos
author_sort Katerina Soupsana
title Distinct roles of haspin in stem cell division and male gametogenesis
title_short Distinct roles of haspin in stem cell division and male gametogenesis
title_full Distinct roles of haspin in stem cell division and male gametogenesis
title_fullStr Distinct roles of haspin in stem cell division and male gametogenesis
title_full_unstemmed Distinct roles of haspin in stem cell division and male gametogenesis
title_sort distinct roles of haspin in stem cell division and male gametogenesis
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/55980d2f4450420aa4ca54db29566fe1
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