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

Martin Blythe (1) , Ayhan Kocer (2) , Alejandro Rubio-Roldan (3) , Tom Giles (1) , Abdulkadir Abakir (1) , Côme Ialy-Radio (4) , Lee Wheldon (1) , Oxana Bereshchenko (5) , Stefano Bruscoli (5) , Alexander Kondrashov (1) , Joël J. Drevet (2) , Richard Emes (1) , Andrew Johnson (1) , John Mccarrey (6) , Daniel Gackowski (7) , Ryszard Olinski (7) , Julie Cocquet (4) , Jose Garcia-Perez (3, 8) , Alexey Ruzov (1)

1 UON - University of Nottingham, UK
2 GReD - Génétique, Reproduction et Développement
3 GENYO - Centre for Genomics and Oncological Research Pfizer [Granada, Spain]
4 IC UM3 (UMR 8104 / U1016) - Institut Cochin
5 UNIPG - Università degli Studi di Perugia = University of Perugia
6 UTSA - The University of Texas at San Antonio
7 Nicolaus Copernicus University [Toruń]
8 Edin. - University of Edinburgh

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.

Domaines: Gamétogenèse; Reproduction sexuée

Martin Blythe, Ayhan Kocer, Alejandro Rubio-Roldan, Tom Giles, Abdulkadir Abakir, et al.. LINE-1 transcription in round spermatids is associated with accretion of 5-carboxylcytosine in their open reading frames. Communications Biology, 2021, 4, pp.691. ⟨10.1038/s42003-021-02217-8⟩. ⟨hal-03670149⟩