In the Human Sperm Nucleus, Nucleosomes Form Spatially Restricted Domains Consistent with Programmed Nucleosome Positioning

Overview

Journal Biol Open

Specialty Biology

Date 2019 Jul 3

PMID 31262721

Authors

Mei-Zi Zhang

Xiao-Min Cao

Feng-Qin Xu

Xiao-Wei Liang

Long-Long Fu

Bao Li

Wei-Guang Liu

Shuo-Guo Li

Fang-Zhen Sun

Xiu-Ying Huang

Wei-Hong Huang

Affiliations

Soon will be listed here.

Abstract

In human sperm, a fraction of its chromatin retains nucleosomes that are positioned on specific sequences containing genes and regulatory units essential for embryonic development. This nucleosome positioning (NP) feature provides an inherited epigenetic mark for sperm. However, it is not known whether there is a structural constraint for these nucleosomes and, if so, how they are localized in a three-dimensional (3D) context of the sperm nucleus. In this study, we examine the 3D organization of sperm chromatin and specifically determine its 3D localization of nucleosomes using structured illumination microscopy. A fraction of the sperm chromatin form nucleosome domains (NDs), visible as microscopic puncta ranging from 40 μm to 700 μm in diameter, and these NDs are precisely localized in the post acrosome region (PAR), outside the sperm's core chromatin. Further, NDs exist mainly in sperm from fertile men in a pilot survey with a small sample size. Together, this study uncovers a new spatially-restricted sub-nuclear structure containing NDs that are consistent with NPs of the sperm, which might represent a novel mark for healthy sperm in human.

References

Hiura H, Okae H, Chiba H, Miyauchi N, Sato F, Sato A . Imprinting methylation errors in ART. Reprod Med Biol. 2014; 13(4):193-202. PMC: 4182590. DOI: 10.1007/s12522-014-0183-3. View

Botezatu A, Socolov R, Socolov D, Iancu I, Anton G . Methylation pattern of methylene tetrahydrofolate reductase and small nuclear ribonucleoprotein polypeptide N promoters in oligoasthenospermia: a case-control study. Reprod Biomed Online. 2013; 28(2):225-31. DOI: 10.1016/j.rbmo.2013.10.010. View

van der Heijden G, Derijck A, Ramos L, Giele M, van der Vlag J, de Boer P . Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Dev Biol. 2006; 298(2):458-69. DOI: 10.1016/j.ydbio.2006.06.051. View

Ajduk A, Yamauchi Y, Ward M . Sperm chromatin remodeling after intracytoplasmic sperm injection differs from that of in vitro fertilization. Biol Reprod. 2006; 75(3):442-51. DOI: 10.1095/biolreprod.106.053223. View

Flechon J, Pavlok A . Ultrastructural study of the interactions and fusion of ram spermatozoa with zona-free hamster oocytes. Reprod Nutr Dev (1980). 1986; 26(4):999-1008. DOI: 10.1051/rnd:19860607. View

Kobayashi H, Sato A, Otsu E, Hiura H, Tomatsu C, Utsunomiya T . Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet. 2007; 16(21):2542-51. DOI: 10.1093/hmg/ddm187. View

Yanagimachi R, Noda Y . Ultrastructural changes in the hamster sperm head during fertilization. J Ultrastruct Res. 1970; 31(5-6):465-85. DOI: 10.1016/s0022-5320(70)90163-2. View

Royo H, Stadler M, Peters A . Alternative Computational Analysis Shows No Evidence for Nucleosome Enrichment at Repetitive Sequences in Mammalian Spermatozoa. Dev Cell. 2016; 37(1):98-104. DOI: 10.1016/j.devcel.2016.03.010. View

Govin J, Escoffier E, Rousseaux S, Kuhn L, Ferro M, Thevenon J . Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis. J Cell Biol. 2007; 176(3):283-94. PMC: 2063955. DOI: 10.1083/jcb.200604141. View

10.

MacKenna A . Contribution of the male factor to unexplained infertility: a review. Int J Androl. 1995; 18 Suppl 1:58-61. DOI: 10.1111/j.1365-2605.1995.tb00640.x. View

11.

Thompson E, Legouy E, Christians E, Renard J . Progressive maturation of chromatin structure regulates HSP70.1 gene expression in the preimplantation mouse embryo. Development. 1995; 121(10):3425-37. DOI: 10.1242/dev.121.10.3425. View

12.

Teperek M, Simeone A, Gaggioli V, Miyamoto K, Allen G, Erkek S . Sperm is epigenetically programmed to regulate gene transcription in embryos. Genome Res. 2016; 26(8):1034-46. PMC: 4971762. DOI: 10.1101/gr.201541.115. View

13.

Gatewood J, Cook G, Balhorn R, Schmid C, Bradbury E . Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. J Biol Chem. 1990; 265(33):20662-6. View

14.

Kobayashi N, Miyauchi N, Tatsuta N, Kitamura A, Okae H, Hiura H . Factors associated with aberrant imprint methylation and oligozoospermia. Sci Rep. 2017; 7:42336. PMC: 5301220. DOI: 10.1038/srep42336. View

15.

Miller D, Paradowska A . Evaluating the localization and DNA binding complexity of histones in mature sperm. Methods Mol Biol. 2012; 927:459-75. DOI: 10.1007/978-1-62703-038-0_40. View

16.

Ausio J, Soley J, Burger W, Lewis J, Barreda D, Cheng K . The histidine-rich protamine from ostrich and tinamou sperm. A link between reptile and bird protamines. Biochemistry. 1999; 38(1):180-4. DOI: 10.1021/bi981621w. View

17.

Zayed F, Lenton E, Cooke I . Comparison between stimulated in-vitro fertilization and stimulated intrauterine insemination for the treatment of unexplained and mild male factor infertility. Hum Reprod. 1998; 12(11):2408-13. DOI: 10.1093/humrep/12.11.2408. View

18.

Yamaguchi K, Hada M, Fukuda Y, Inoue E, Makino Y, Katou Y . Re-evaluating the Localization of Sperm-Retained Histones Revealed the Modification-Dependent Accumulation in Specific Genome Regions. Cell Rep. 2018; 23(13):3920-3932. DOI: 10.1016/j.celrep.2018.05.094. View

19.

Adenot P, Mercier Y, Renard J, Thompson E . Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development. 1997; 124(22):4615-25. DOI: 10.1242/dev.124.22.4615. View

20.

Hammoud S, Nix D, Zhang H, Purwar J, Carrell D, Cairns B . Distinctive chromatin in human sperm packages genes for embryo development. Nature. 2009; 460(7254):473-8. PMC: 2858064. DOI: 10.1038/nature08162. View