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LINE-1 transcription in round spermatids is associated with accretion of 5-carboxylcytosine in their open reading frames

Blythe, Martin J.; Kocer, Ayhan; Rubio-Roldan, Alejandro; Giles, Tom; Abakir, Abdulkadir; Ialy-Radio, Côme; Wheldon, Lee M.; Bereshchenko, Oxana; Bruscoli, Stefano; Kondrashov, Alexander; Drevet, Joël R.; Emes, Richard D.; Johnson, Andrew D.; McCarrey, John R.; Gackowski, Daniel; Olinski, Ryszard; Cocquet, Julie; Garcia-Perez, Jose L.; Ruzov, Alexey

LINE-1 transcription in round spermatids is associated with accretion of 5-carboxylcytosine in their open reading frames Thumbnail


Authors

Martin J. Blythe

Ayhan Kocer

Alejandro Rubio-Roldan

Tom Giles

Abdulkadir Abakir

Côme Ialy-Radio

Lee M. Wheldon

Oxana Bereshchenko

Stefano Bruscoli

Joël R. Drevet

Richard D. Emes

Andrew D. Johnson

John R. McCarrey

Daniel Gackowski

Ryszard Olinski

Julie Cocquet

Jose L. Garcia-Perez

Alexey Ruzov



Abstract

Chromatin of male and female gametes undergoes a number of reprogramming events during the transition from germ cell to embryonic developmental programs. Although the rearrangement of DNA methylation patterns occurring in the zygote has been extensively characterized, little is known about the dynamics of DNA modifications during spermatid maturation. Here, we demonstrate that the dynamics of 5-carboxylcytosine (5caC) correlate with active transcription of LINE-1 retroelements during murine spermiogenesis. We show that the open reading frames of active and evolutionary young LINE-1s are 5caC-enriched in round spermatids and 5caC is eliminated from LINE-1s and spermiogenesis-specific genes during spermatid maturation, being simultaneously retained at promoters and introns of developmental genes. Our results reveal an association of 5caC with activity of LINE-1 retrotransposons suggesting a potential direct role for this DNA modification in fine regulation of their transcription.

Citation

Blythe, M. J., Kocer, A., Rubio-Roldan, A., Giles, T., Abakir, A., Ialy-Radio, C., …Ruzov, A. (2021). LINE-1 transcription in round spermatids is associated with accretion of 5-carboxylcytosine in their open reading frames. Communications Biology, 4, Article 691. https://doi.org/10.1038/s42003-021-02217-8

Journal Article Type Article
Acceptance Date May 14, 2021
Online Publication Date Jun 7, 2021
Publication Date Jun 7, 2021
Deposit Date May 26, 2021
Publicly Available Date Jun 7, 2021
Journal Communications Biology
Electronic ISSN 2399-3642
Publisher Nature Publishing Group
Peer Reviewed Peer Reviewed
Volume 4
Article Number 691
DOI https://doi.org/10.1038/s42003-021-02217-8
Public URL https://nottingham-repository.worktribe.com/output/5573477
Publisher URL https://www.nature.com/articles/s42003-021-02217-8

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