Chromatin-to-nucleoprotamine transition is controlled by the histone H2B variant TH2B

Genes and Development

Volumn 27, Issue 15, 2013, Pages 1680-1692

  Montellier, Emilie ^a   Boussouar, Fayçal ^a   Rousseaux, Sophie ^a   Zhang, Kai ^b   Buchou, Thierry ^a   Fenaille, François ^c   Shiota, Hitoshi ^a   Debernardi, Alexandra ^a   Héry, Patrick ^d   Curtet, Sandrine ^a   Jamshidikia, Mahya ^a   Barral, Sophie ^a   Holota, Hélène ^a,e   Bergon, Aurélie ^a,e   Lopez, Fabrice ^a,e   Guardiola, Philippe ^f   Pernet, Karin ^g   Imbert, Jean ^a,e   Petosa, Carlo ^h   Tan, Minjia ^i,j   Zhao, Yingming ^i,j   Gérard, Matthieu ^d   Khochbin, Saadi ^a   more..

^a INSERM   (France)

^b NANKAI UNIVERSITY   (China)

^c DIF   (France)

^d SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^e Aix Marseille university   (France)

^f UNIVERSITÉ D'ANGERS   (France)

^g GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^h UNIV GRENOBLE ALPES   (France)

ⁱ UNIVERSITY OF CHICAGO   (United States)

^j SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

more..

Author keywords

BRDT; H2AZ; Histone eviction; Male contraception; Male infertility; Reprogramming; Sex chromosome inactivation

Indexed keywords

ARGININE; HISTONE H2B; HISTONE TH2B; NUCLEOPROTAMINE; PROTAMINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CHROMATIN; EPIGENETICS; FERTILIZATION; GENETIC ASSOCIATION; HISTONE MODIFICATION; MALE; METHYLATION; MOUSE; NONHUMAN; NUCLEOSOME; PHASE TRANSITION; PRIORITY JOURNAL; PRONUCLEUS; PROTEIN EXPRESSION; SPERMATID; SPERMATOGENESIS; UPREGULATION;

BRDT; H2AZ; HISTONE EVICTION; MALE CONTRACEPTION; MALE INFERTILITY; REPROGRAMMING; SEX CHROMOSOME INACTIVATION;

ANIMALS; CHROMATIN; EPIGENESIS, GENETIC; FEMALE; FERTILIZATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HISTONES; MALE; MEIOSIS; MICE; NUCLEOSOMES; PROTAMINES; SPERMATOGENESIS; TESTIS;

EID: 84881062290     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.220095.113     Document Type: Article

References (36)

1. Bonisch C., Hake SB. 2012. Histone H2A variants in nucleosomes and chromatin: More or less stable? Nucleic Acids Res 40: 10719-10741.
2. Boussouar F., Rousseaux S, Khochbin S. 2008. A new insight into male genome reprogramming by histone variants and histone code. Cell Cycle 7: 3499-3502.
3. Branson R. E, Grimes SR Jr, Yonuschot G, Irvin JL. 1975. The histones of rat testis. Arch Biochem Biophys 168: 403-412.
4. BrockWA, Trostle PK, Meistrich ML. 1980. Meiotic synthesis of testis histones in the rat. Proc Natl Acad Sci 77: 371-375.
5. Choi Y. C, Chae CB. 1993. Demethylation of somatic and testisspecific histone H2A and H2B genes in F9 embryonal carcinoma cells. Mol Cell Biol 13: 5538-5548.
6. Contrepois K., Ezan E, Mann C, Fenaille F. 2010. Ultra-high performance liquid chromatography-mass spectrometry for the fast profiling of histone post-translational modifications. J Proteome Res 9: 5501-5509.
7. Gaucher J., Reynoird N, Montellier E, Boussouar F, Rousseaux S, Khochbin S. 2010. From meiosis to postmeiotic events: The secrets of histone disappearance. FEBS J 277: 599-604.
8. Gaucher J., Boussouar F, Montellier E, Curtet S, Buchou T, Bertrand S., Hery P, Jounier S, Depaux A, Vitte AL, et al. 2012. Bromodomain-dependent stage-specific male genome programming by Brdt. EMBO J 31: 3809-3820.
9. Govin J., Caron C, Lestrat C, Rousseaux S, Khochbin S. 2004. The role of histones in chromatin remodelling during mammalian spermiogenesis. Eur J Biochem 271: 3459-3469.
10. Govin J., Escoffier E, Rousseaux S, Kuhn L, Ferro M, Thevenon J, Catena R., Davidson I, Garin J, Khochbin S, et al. 2007. Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis. J Cell Biol 176: 283-294.
11. Greaves I. K, Rangasamy D, Devoy M, Marshall Graves JA, Tremethick DJ. 2006. The X and Y chromosomes assemble into H2A. Z-containing [corrected] facultative heterochromatin [corrected] following meiosis. Mol Cell Biol 26: 5394-5405.
12. Hainer S. J, Martens JA. 2011. Identification of histone mutants that are defective for transcription-coupled nucleosome occupancy. Mol Cell Biol 31: 3557-3568.
13. Hazzouri M., Pivot-Pajot C, Faure AK, Usson Y, Pelletier R, Sele B, Khochbin S, Rousseaux S. 2000. Regulated hyperacetylation of core histones during mouse spermatogenesis: Involvement of histone deacetylases. Eur J Cell Biol 79: 950-960.
14. Huh N. E, Hwang IW, Lim K, You KH, Chae CB. 1991. Presence of a bi-directional S phase-specific transcription regulatory element in the promoter shared by testis-specific TH2A and TH2B histone genes. Nucleic Acids Res 19: 93-98.
15. Hyland E. M, Cosgrove MS, Molina H, Wang D, Pandey A, Cottee RJ, Boeke JD. 2005. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol Cell Biol 25: 10060-10070.
16. Iwasaki W., Tachiwana H, Kawaguchi K, Shibata T, Kagawa W, Kurumizaka H. 2011. Comprehensive structural analysis of mutant nucleosomes containing lysine to glutamine (KQ) substitutions in the H3 and H4 histone-fold domains. Biochemistry 50: 7822-7832.
17. Li A., Maffey AH, Abbott WD, Conde e Silva N, Prunell A, Siino J, Churikov D, Zalensky AO, Ausio J. 2005. Characterization of nucleosomes consisting of the human testis/spermspecific histone H2B variant (hTSH2B). Biochemistry 44: 2529-2535.
18. Liu P., Jenkins NA, Copeland NG. 2003. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 13: 476-484.
19. Manohar M., Mooney AM, North JA, Nakkula RJ, Picking JW, Edon A., Fishel R, Poirier MG, Ottesen JJ. 2009. Acetylation of histone H3 at the nucleosome dyad alters DNA-histone binding. J Biol Chem 284: 23312-23321.
20. Marushige Y., Marushige K. 1983. Proteolysis of somatic type histones in transforming rat spermatid chromatin. Biochim Biophys Acta 761: 48-57.
21. Montellier E., Rousseaux S, Zhao Y, Khochbin S. 2012. Histone crotonylation specifically marks the haploid male germ cell gene expression program: Post-meiotic male-specific gene expression. Bioessays 34: 187-193.
22. Moriniere J., Rousseaux S, Steuerwald U, Soler-Lopez M, Curtet S, Vitte AL, Govin J, Gaucher J, Sadoul K, Hart DJ, et al. 2009. Cooperative binding of two acetylation marks on a histone tail by a single bromodomain. Nature 461: 664-668.
23. Pivot-Pajot C, Caron C, Govin J, Vion A, Rousseaux S, Khochbin S. 2003. Acetylation-dependent chromatin reorganization by BRDT, a testis-specific bromodomain-containing protein. Mol Cell Biol 23: 5354-5365.
24. Rao B. J, Rao MR. 1987. DNase I site mapping and micrococcal nuclease digestion of pachytene chromatin reveal novel structural features. J Biol Chem 262: 4472-4476.
25. Rao B. J, Brahmachari SK, Rao MR. 1983. Structural organization of the meiotic prophase chromatin in the rat testis. J Biol Chem 258: 13478-13485.
26. Shires A., Carpenter MP, Chalkley R. 1975. New histones found in mature mammalian testes. Proc Natl Acad Sci 72: 2714-2718.
27. Soboleva T. A, Nekrasov M, Pahwa A, Williams R, Huttley GA, Tremethick DJ. 2012. A unique H2A histone variant occupies the transcriptional start site of active genes. Nat Struct Mol Biol 19: 25-30.
28. Talbert P. B, Henikoff S. 2010. Histone variants-ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11: 264-275.
29. Talbert P. B, Ahmad K, Almouzni G, Ausio J, Berger F, Bhalla PL, Bonner W. M, Cande WZ, Chadwick BP, Chan SW, et al. 2012. A unified phylogeny-based nomenclature for histone variants. Epigenetics Chromatin 5: 7.
30. Tan M., Luo H, Lee S, Jin F, Yang JS, Montellier E, Buchou T, Cheng Z., Rousseaux S, Rajagopal N, et al. 2011. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146: 1016-1028.
31. Torres-Padilla ME, Bannister AJ, Hurd PJ, Kouzarides T, Zernicka-Goetz M. 2006. Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int J Dev Biol 50: 455-461.
32. Tropberger P., Pott S, Keller C, Kamieniarz-Gdula K, Caron M, Richter F., Li G, Mittler G, Liu ET, Buhler M, et al. 2013. Regulation of transcription through acetylation of H3K122 on the lateral surface of the histone octamer. Cell 152: 859-872.
33. van der Heijden GW, Derijck AA, Posfai E, Giele M, Pelczar P, Ramos L., Wansink DG, van der Vlag J, Peters AH, de Boer P. 2007. Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nat Genet 39: 251-258.
34. Wu F., Caron C, De Robertis C, Khochbin S, Rousseaux S. 2008. Testis-specific histone variants H2AL1/2 rapidly disappear from paternal heterochromatin after fertilization. J Reprod Dev 54: 413-417.
35. Ye T., Krebs AR, Choukrallah MA, Keime C, Plewniak F, Davidson I., Tora L. 2011. seqMINER: An integrated ChIP-seq data interpretation platform. Nucleic Acids Res 39: e35.
36. Zhao M., Shirley CR, Hayashi S, Marcon L, Mohapatra B, Suganuma R., Behringer RR, Boissonneault G, Yanagimachi R, Meistrich ML. 2004. Transition nuclear proteins are required for normal chromatin condensation and functional sperm development. Genesis 38: 200-213.