Histone Variant H2A.L.2 Guides Transition Protein-Dependent Protamine Assembly in Male Germ Cells

Sophie Barral; Yuichi Morozumi; Hiroki Tanaka; Emilie Montellier; Jérôme Govin; Maud de Dieuleveult; Guillaume Charbonnier; Yohann Couté; Denis Puthier; Thierry Buchou; Fayçal Boussouar; Takashi Urahama; François Fenaille; Sandrine Curtet; Patrick Héry; Nicolas Fernandez-Nunez; Hitoshi Shiota; Matthieu Gérard; Sophie Rousseaux; Hitoshi Kurumizaka; Saadi Khochbin

doi:10.1016/j.molcel.2017.02.025

Histone Variant H2A.L.2 Guides Transition Protein-Dependent Protamine Assembly in Male Germ Cells

Sophie Barral, Yuichi Morozumi, Hiroki Tanaka, Emilie Montellier, Jérôme Govin, Maud de Dieuleveult, Guillaume Charbonnier, Yohann Couté, Denis Puthier, Thierry Buchou, Fayçal Boussouar, Takashi Urahama, François Fenaille, Sandrine Curtet, Patrick Héry, Nicolas Fernandez-Nunez, Hitoshi Shiota, Matthieu Gérard, Sophie Rousseaux, Hitoshi KurumizakaSaadi Khochbin^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

91 Citations (Scopus)

Abstract

Histone replacement by transition proteins (TPs) and protamines (Prms) constitutes an essential step for the successful production of functional male gametes, yet nothing is known on the underlying functional interplay between histones, TPs, and Prms. Here, by studying spermatogenesis in the absence of a spermatid-specific histone variant, H2A.L.2, we discover a fundamental mechanism involved in the transformation of nucleosomes into nucleoprotamines. H2A.L.2 is synthesized at the same time as TPs and enables their loading onto the nucleosomes. TPs do not displace histones but rather drive the recruitment and processing of Prms, which are themselves responsible for histone eviction. Altogether, the incorporation of H2A.L.2 initiates and orchestrates a series of successive transitional states that ultimately shift to the fully compacted genome of the mature spermatozoa. Hence, the current view of histone-to-nucleoprotamine transition should be revisited and include an additional step with H2A.L.2 assembly prior to the action of TPs and Prms.

Original language	English
Pages (from-to)	89-101.e8
Journal	Molecular Cell
Volume	66
Issue number	1
DOIs	https://doi.org/10.1016/j.molcel.2017.02.025
Publication status	Published - 2017 Apr 6

Keywords

Brdt
H2A.Z
MCM
Nap1L4
Npm3
spermiogenesis
SRCAP
subnucleosome
TH2B
Tip60

ASJC Scopus subject areas

Molecular Biology
Cell Biology

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Barral, S., Morozumi, Y., Tanaka, H., Montellier, E., Govin, J., de Dieuleveult, M., Charbonnier, G., Couté, Y., Puthier, D., Buchou, T., Boussouar, F., Urahama, T., Fenaille, F., Curtet, S., Héry, P., Fernandez-Nunez, N., Shiota, H., Gérard, M., Rousseaux, S., ... Khochbin, S. (2017). Histone Variant H2A.L.2 Guides Transition Protein-Dependent Protamine Assembly in Male Germ Cells. Molecular Cell, 66(1), 89-101.e8. https://doi.org/10.1016/j.molcel.2017.02.025

Barral, S, Morozumi, Y, Tanaka, H, Montellier, E, Govin, J, de Dieuleveult, M, Charbonnier, G, Couté, Y, Puthier, D, Buchou, T, Boussouar, F, Urahama, T, Fenaille, F, Curtet, S, Héry, P, Fernandez-Nunez, N, Shiota, H, Gérard, M, Rousseaux, S, Kurumizaka, H & Khochbin, S 2017, 'Histone Variant H2A.L.2 Guides Transition Protein-Dependent Protamine Assembly in Male Germ Cells', Molecular Cell, vol. 66, no. 1, pp. 89-101.e8. https://doi.org/10.1016/j.molcel.2017.02.025

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abstract = "Histone replacement by transition proteins (TPs) and protamines (Prms) constitutes an essential step for the successful production of functional male gametes, yet nothing is known on the underlying functional interplay between histones, TPs, and Prms. Here, by studying spermatogenesis in the absence of a spermatid-specific histone variant, H2A.L.2, we discover a fundamental mechanism involved in the transformation of nucleosomes into nucleoprotamines. H2A.L.2 is synthesized at the same time as TPs and enables their loading onto the nucleosomes. TPs do not displace histones but rather drive the recruitment and processing of Prms, which are themselves responsible for histone eviction. Altogether, the incorporation of H2A.L.2 initiates and orchestrates a series of successive transitional states that ultimately shift to the fully compacted genome of the mature spermatozoa. Hence, the current view of histone-to-nucleoprotamine transition should be revisited and include an additional step with H2A.L.2 assembly prior to the action of TPs and Prms.",

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AU - Barral, Sophie

AU - Morozumi, Yuichi

AU - Tanaka, Hiroki

AU - Montellier, Emilie

AU - Govin, Jérôme

AU - de Dieuleveult, Maud

AU - Charbonnier, Guillaume

AU - Couté, Yohann

AU - Puthier, Denis

AU - Buchou, Thierry

AU - Boussouar, Fayçal

AU - Urahama, Takashi

AU - Fenaille, François

AU - Curtet, Sandrine

AU - Héry, Patrick

AU - Fernandez-Nunez, Nicolas

AU - Shiota, Hitoshi

AU - Gérard, Matthieu

AU - Rousseaux, Sophie

AU - Kurumizaka, Hitoshi

AU - Khochbin, Saadi

PY - 2017/4/6

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AB - Histone replacement by transition proteins (TPs) and protamines (Prms) constitutes an essential step for the successful production of functional male gametes, yet nothing is known on the underlying functional interplay between histones, TPs, and Prms. Here, by studying spermatogenesis in the absence of a spermatid-specific histone variant, H2A.L.2, we discover a fundamental mechanism involved in the transformation of nucleosomes into nucleoprotamines. H2A.L.2 is synthesized at the same time as TPs and enables their loading onto the nucleosomes. TPs do not displace histones but rather drive the recruitment and processing of Prms, which are themselves responsible for histone eviction. Altogether, the incorporation of H2A.L.2 initiates and orchestrates a series of successive transitional states that ultimately shift to the fully compacted genome of the mature spermatozoa. Hence, the current view of histone-to-nucleoprotamine transition should be revisited and include an additional step with H2A.L.2 assembly prior to the action of TPs and Prms.

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ER -

Histone Variant H2A.L.2 Guides Transition Protein-Dependent Protamine Assembly in Male Germ Cells

Abstract

Keywords

ASJC Scopus subject areas

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