Uniformity of Nucleosome Preservation Pattern in Mammalian Sperm and Its Connection to Repetitive DNA Elements

Abstract

Nucleosome-to-protamine exchange during mammalian spermiogenesis is essential for compaction and protection of paternal DNA. It is interesting that, depending on the species, 1% to 15% of nucleosomes are retained, but the generalizability and biological function of this retention are unknown. Here, we show concordantly in human and bovine that nucleosomes remained in sperm chromatin predominantly within distal intergenic regions and introns and associated with centromere repeats and retrotransposons (LINE1 and SINEs). In contrast, nucleosome depletion concerned particularly exons, 5'-UTR, 3'-UTR, TSS, and TTS and was associated with simple and low-complexity repeats. Overlap of human and bovine genes exhibiting nucleosome preservation in the promoter and gene body revealed a significant enrichment of signal transduction and RNA- and protein-processing factors. Our study demonstrates the genome-wide uniformity of the nucleosome preservation pattern in mammalian sperm and its connection to repetitive DNA elements and suggests a function in preimplantation processes for paternally derived nucleosomes.

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“…In the first human dataset (17) the retention prevalence of developmental promoters over the gene poor regions was suggested. Later, a study that utilized fixed chromatin and a smaller amount of micrococcal nuclease concluded that there is a prevalence of the gene-poor regions in the nucleosome fractions (19,20). A careful inspection of the latter datasets from human and bovine sperm nucleosome retaining regions still shows a limited number of promoters present corresponding to genes of signal transduction, protein processing and ATP-binding, suggesting their role in the early zygote development (20).…”

“…Later, a study that utilized fixed chromatin and a smaller amount of micrococcal nuclease concluded that there is a prevalence of the gene-poor regions in the nucleosome fractions (19,20). A careful inspection of the latter datasets from human and bovine sperm nucleosome retaining regions still shows a limited number of promoters present corresponding to genes of signal transduction, protein processing and ATP-binding, suggesting their role in the early zygote development (20). Furthermore, the overlap between human and bovine data showed the significant enrichment in genes associated with signal transduction and RNA and protein processing factors and suggests the conservative mechanism of nucleosome retention (20).…”

“…These studies showed that the promoters in sperm are enriched in H3K4me3 and H3K27me3, and it was suggested that genes with these marks play a particularly important role in epigenetic inheritance (16–18). On the other hand, more recent nucleosome mapping studies showed that sperm nucleosome fraction is enriched in gene-poor regions and is generally depleted from the promoters (19,20). The discrepancy in nucleosome mapping could be explained by different chromatin preparation protocols (21).…”

“…H3K4me3 is found to be strongly associated with both maternal and paternal genomes in mouse, rabbit and bovine zygote (25). The human sperm nucleosome fraction is enriched in Short Interspersed Nuclear Element (SINE) and Long Interspersed Element-1 (LINE) retroelements (20). It was suggested that sperm DNA containing repetitive elements plays a key role in pre-implantation processes (20).…”

“…The human sperm nucleosome fraction is enriched in Short Interspersed Nuclear Element (SINE) and Long Interspersed Element-1 (LINE) retroelements (20). It was suggested that sperm DNA containing repetitive elements plays a key role in pre-implantation processes (20). This view was recently challenged by Royo et al.…”