Role of histone variants in the reprogramming of parental genomes

WANG Nan HUANG Xing-wei CHENG Xiang-rong JIANG Qi PANG Nan LEI Lei*

doi:10.16098/j.issn.0529-1356.2019.01.023

PDF(1172 KB)

Acta Anatomica Sinica ›› 2019, Vol. 50 ›› Issue (1) : 132-136. DOI: 10.16098/j.issn.0529-1356.2019.01.023

Review

Role of histone variants in the reprogramming of parental genomes

WANG Nan HUANG Xing-wei CHENG Xiang-rong JIANG Qi PANG Nan LEI Lei*

Author information +

History +

Abstract

Oocytes have the ability to reprogram the sperm genome to ensure normal embryonic development. After sperm enters into the egg, the paternal genome undergoes protamine to histone exchange, whole genome demethylation and other processes, which start embryonic development. Histone H3 variant H3.3 can replace canonical histones H3.1 and H3.2 in nucleosomes, thereby modifying chromatin structure and regulate gene expression. The absence of H3.3 during early embryonic development will lead to excessive chromosomal aggregation and mis-isolation. This article reviews the role of histone variant H3.3 and its chaperones in spermatogenesis, fertilization and early embryonic development. In particular, the importance of H3.3 in the reprogramming of the paternal genome is of great significance in understanding the formation of totipotent zygotes after fertilization and their preimplantation development.

Key words

Fertilization / Histone / Reprogramming / Protamine

Cite this article

EndNote

Ris (Procite)

Bibtex

Download Citations

WANG Nan HUANG Xing-wei CHENG Xiang-rong JIANG Qi PANG Nan LEI Lei. Role of histone variants in the reprogramming of parental genomes[J]. Acta Anatomica Sinica. 2019, 50(1): 132-136 https://doi.org/10.16098/j.issn.0529-1356.2019.01.023

References

［1］ Gaucher J, Reynoird N, Montellier E, et al. From meiosis to postmeiotic events: the secrets of histone disappearance ［J］. FEBS J, 2010, 277(3): 599-604.

［2］ Zhang K, Rajput SK, Wang S, et al. CHD1 regulates deposition of histone variant H3.3 during bovine early embryonic development ［J］. Biol Reprod, 2016, 94(6): 140.

［3］ Sailau ZK, Bogolyubov DS, Bogolyubova IO. Nuclear distribution of the chromatin-remodeling protein ATRX in mouse early embryogenesis ［J］. Acta Histochem, 2017, 119(1): 18-25.

［4］ Udugama M, Sanij E, Voon HPJ, et al. Ribosomal DNA copy loss and repeat instability in ATRX-mutated cancers ［J］. Proc Nat Acad Sci USA, 2018, 115(18): 4737-4742.

［5］ Ma Y, Buttitta L. Chromatin organization changes during the establishment and maintenance of the postmitotic state ［J］. Epigenetics Chromatin, 2017, 10(1): 53.

［6］ Penke TJR, McKay DJ, Strahl BD, et al. Functional redundancy of variant and canonical histone H3 lysine 9 modification in drosophila ［J］. Genetics, 2018, 208(1): 229-244.

［7］ Inoue A, Zhang Y. Nucleosome assembly is required for nuclear pore complex assembly in mouse zygotes ［J］. Nat Struct Mol Biol, 2014, 21(7): 609-616.

［8］ Jang CW, Shibata Y, Starmer J, et al. Histone H3.3 maintains genome integrity during mammalian development ［J］. Genes Dev, 2015, 29(13): 1377-1392.

［9］ Lin CJ, Conti M, Ramalho-Santos M. Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development ［J］. Development, 2013, 140(17): 3624-3634.

［10］Holland A, Ohlendieck K. Comparative profiling of the sperm proteome ［J］. Proteomics, 2015, 15(4): 632-648.

［11］Kong Q, Banaszynski LA, Geng F, et al. Histone variant H3.3-mediated chromatin remodeling is essential for paternal genome activation in mouse preimplantation embryos ［J］. J Biol Chem, 2018, 293(10): 3829-3838.

［12］Inoue A, Ogushi S, Saitou M, et al. Involvement of mouse nucleoplasmin 2 in the decondensation of sperm chromatin after fertilization ［J］. Biol Reprod, 2011, 85(1): 70-77.

［13］Soboleva TA, Nekrasov M, Pahwa A, et al. A unique H2A histone variant occupies the transcriptional start site of active genes ［J］. Nat Struct Mol Biol, 2011, 19(1): 25-30.

［14］Yuen BT, Bush KM, Barrilleaux BL, et al. Histone H3-3 regulates dynamic chromatin states during spermatogenesis ［J］. Development, 2014, 141(18): 3483-3494.

［15］Santenard A, Ziegler-Birling C, Koch M, et al. Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3 ［J］. Nat Cell Biol, 2010, 12(9): 853-862.

［16］Teperek M, Miyamoto K. Nuclear reprogramming of sperm and somatic nuclei in eggs and oocytes ［J］. Reprod Med Biol, 2013, 12: 133-149.

［17］de Rooij DG. Proliferation and differentiation of spermatogonial stem cells ［J］. Reproduction, 2001, 121(3): 347-354.

［18］Bonnefoy E, Orsi GA, Couble P, et al. The essential role of drosophila HIRA for de novo assembly of paternal chromatin at fertilization ［J］. PLoS Genet, 2007, 3(10): 1991-2006.

［19］Dyer MA, Qadeer ZA, Valle-Garcia D, et al. ATRX and DAXX: mechanisms and mutations ［J］. Cold Spring Harb Perspect Med, 2017, 7(3).

［20］Filipescu D, Szenker E, Almouzni G. Developmental roles of histone H3 variants and their chaperones ［J］. Trends Genet, 2013, 29(11): 630-640.

［21］Fang HT, El Farran CA, Xing QR, et al. Global H3.3 dynamic deposition defines its bimodal role in cell fate transition ［J］. Nat commun, 2018, 9(1): 1537.

［22］Tardat M, Albert M, Kunzmann R, et al. Cbx2 targets PRC1 to constitutive heterochromatin in mouse zygotes in a parent-of-origin-dependent manner ［J］. Mol Cell, 2015, 58(1): 157-171.

［23］Hazzouri M, Pivot-Pajot C, Faure AK, et al. Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone deacetylases ［J］. Eur J Cell Biol, 2000, 79(12): 950-960.

［24］Zhou L, Baibakov B, Canagarajah B, et al. Genetic mosaics and time-lapse imaging identify functions of histone H3.3 residues in mouse oocytes and embryos ［J］. Development, 2017, 144(3): 519-528.

［25］Wright SJ. Sperm nuclear activation during fertilization ［J］. Curr Top Dev Biol, 1999, 46: 133-178.

［26］Lin CJ, Koh FM, Wong P, et al. Hira-mediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote ［J］. Dev Cell, 2014, 30(3): 268-279.

［27］Nashun B, Hill PW, Smallwood SA, et al. Continuous histone replacement by hira is essential for normal transcriptional regulation and de novo DNA methylation during mouse oogenesis ［J］. Mol Cell, 2015, 60(4): 611-625.

［28］Probst AV, Almouzni G. Heterochromatin establishment in the context of genome-wide epigenetic reprogramming ［J］. Trends Genet, 2011, 27(5): 177-185.

［29］Oyama K, El-Nachef D, Fang C, et al. Deletion of HP1gamma in cardiac myocytes affects H4K20me3 levels but does not impact cardiac growth ［J］. Epigenet Chromatin, 2018, 11(1): 18.

［30］Fulka H, Langerova A. The maternal nucleolus plays a key role in centromere satellite maintenance during the oocyte to embryo transition ［J］. Development, 2014, 141(8): 1694-1704.

［31］Buschbeck M, Hake SB. Variants of core histones and their roles in cell fate decisions, development and cancer ［J］. Nat Revi Mol Cell Biol, 2017, 18(5): 299-314.

［32］Rapkin LM, Ahmed K, Dulev S, et al. The histone chaperone DAXX maintains the structural organization of heterochromatin domains ［J］. Epigenet Chromatin, 2015, 8: 44.

［33］Voon HP, Hughes JR, Rode C, et al. ATRX plays a key role in maintaining silencing at interstitial heterochromatic loci and imprinted genes ［J］. Cell Reports, 2015, 11(3): 405-418.

［34］Szenker E, Ray-Gallet D, Almouzni G. The double face of the histone variant H3.3 ［J］. Cell Res, 2011, 21(3): 421-434.