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

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

doi:10.1038/s42003-021-02217-8

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

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

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6 Scopus citations

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.

Original language	English (US)
Article number	691
Journal	Communications Biology
Volume	4
Issue number	1
DOIs	https://doi.org/10.1038/s42003-021-02217-8
State	Published - Dec 2021
Externally published	Yes

ASJC Scopus subject areas

Medicine (miscellaneous)
General Biochemistry, Genetics and Molecular Biology
General Agricultural and Biological Sciences

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10.1038/s42003-021-02217-8

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Blythe, M. J., Kocer, A., Rubio-Roldan, A., Giles, T., Abakir, A., Ialy-Radio, C., Wheldon, L. M., Bereshchenko, O., Bruscoli, S., Kondrashov, A., Drevet, J. R., Emes, R. D., Johnson, A. D., McCarrey, J. R., Gackowski, D., Olinski, R., Cocquet, J., Garcia-Perez, J. L., & Ruzov, A. (2021). LINE-1 transcription in round spermatids is associated with accretion of 5-carboxylcytosine in their open reading frames. Communications Biology, 4(1), Article 691. https://doi.org/10.1038/s42003-021-02217-8

Blythe, MJ, Kocer, A, Rubio-Roldan, A, Giles, T, Abakir, A, Ialy-Radio, C, Wheldon, LM, Bereshchenko, O, Bruscoli, S, Kondrashov, A, Drevet, JR, Emes, RD, Johnson, AD, McCarrey, JR, Gackowski, D, Olinski, R, Cocquet, J, Garcia-Perez, JL & Ruzov, A 2021, 'LINE-1 transcription in round spermatids is associated with accretion of 5-carboxylcytosine in their open reading frames', Communications Biology, vol. 4, no. 1, 691. https://doi.org/10.1038/s42003-021-02217-8

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

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.",

author = "Blythe, {Martin J.} and Ayhan Kocer and Alejandro Rubio-Roldan and Tom Giles and Abdulkadir Abakir and C{\^o}me Ialy-Radio and Wheldon, {Lee M.} and Oxana Bereshchenko and Stefano Bruscoli and Alexander Kondrashov and Drevet, {Jo{\"e}l R.} and Emes, {Richard D.} and Johnson, {Andrew D.} and McCarrey, {John R.} and Daniel Gackowski and Ryszard Olinski and Julie Cocquet and Garcia-Perez, {Jose L.} and Alexey Ruzov",

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doi = "10.1038/s42003-021-02217-8",

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T1 - LINE-1 transcription in round spermatids is associated with accretion of 5-carboxylcytosine in their open reading frames

AU - Blythe, Martin J.

AU - Kocer, Ayhan

AU - Rubio-Roldan, Alejandro

AU - Giles, Tom

AU - Abakir, Abdulkadir

AU - Ialy-Radio, Côme

AU - Wheldon, Lee M.

AU - Bereshchenko, Oxana

AU - Bruscoli, Stefano

AU - Kondrashov, Alexander

AU - Drevet, Joël R.

AU - Emes, Richard D.

AU - Johnson, Andrew D.

AU - McCarrey, John R.

AU - Gackowski, Daniel

AU - Olinski, Ryszard

AU - Cocquet, Julie

AU - Garcia-Perez, Jose L.

AU - Ruzov, Alexey

PY - 2021/12

Y1 - 2021/12

N2 - 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.

AB - 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.

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

Abstract

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