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Human sperm chromatin epigenetic potential: genomics, proteomics, and male infertility.

Castillo J, Estanyol JM, Ballesc√° JL, Oliva R - Asian J. Androl. (2015 Jul-Aug)

Bottom Line: Interestingly, recent proteomic studies have shown that sperm chromatin contains many additional proteins, in addition to the abundant histones and protamines, with specific modifications and chromatin affinity features which are also delivered to the oocyte.Both gene and protein signatures seem to be altered in infertile patients and, as such, are consistent with the potential involvement of the sperm chromatin landscape in early embryo development.As a complement, we provide experimental evidence for the detection of phosphorylations and acetylations in human protamine 1 using a mass spectrometry approach.

View Article: PubMed Central - PubMed

Affiliation: Human Genetics Research Group, IDIBAPS, Faculty of Medicine, University of Barcelona, Casanova 143; Biochemistry and Molecular Genetics Service, Biomedical Diagnostic Centre, Hospital Clinic, Villarroel 170, 08036 Barcelona, Spain.

ABSTRACT
The classical idea about the function of the mammalian sperm chromatin is that it serves to transmit a highly protected and transcriptionally inactive paternal genome, largely condensed by protamines, to the next generation. In addition, recent sperm chromatin genome-wide dissection studies indicate the presence of a differential distribution of the genes and repetitive sequences in the protamine-condensed and histone-condensed sperm chromatin domains, which could be potentially involved in regulatory roles after fertilization. Interestingly, recent proteomic studies have shown that sperm chromatin contains many additional proteins, in addition to the abundant histones and protamines, with specific modifications and chromatin affinity features which are also delivered to the oocyte. Both gene and protein signatures seem to be altered in infertile patients and, as such, are consistent with the potential involvement of the sperm chromatin landscape in early embryo development. This present work reviews the available information on the composition of the human sperm chromatin and its epigenetic potential, with a particular focus on recent results derived from high-throughput genomic and proteomic studies. As a complement, we provide experimental evidence for the detection of phosphorylations and acetylations in human protamine 1 using a mass spectrometry approach. The available data indicate that the sperm chromatin is much more complex than what it was previously thought, raising the possibility that it could also serve to transmit crucial paternal epigenetic information to the embryo.

No MeSH data available.


Related in: MedlinePlus

Gene and protein composition of the human sperm chromatin. Hypothetical model of human sperm chromatin showing the histone-associated DNA constitution (a) and protein contents (b). The model is drawn at a scale and inspired by the known nucleo-protamine toroidal structures124 and the high-throughput sequencing data obtained from the analysis of retained human sperm nucleosomes after micrococcal nuclease digestion.4344455152
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Figure 1: Gene and protein composition of the human sperm chromatin. Hypothetical model of human sperm chromatin showing the histone-associated DNA constitution (a) and protein contents (b). The model is drawn at a scale and inspired by the known nucleo-protamine toroidal structures124 and the high-throughput sequencing data obtained from the analysis of retained human sperm nucleosomes after micrococcal nuclease digestion.4344455152

Mentions: The main function of the sperm cell is to transmit to the embryo the paternal genetic message encoded in the DNA sequence together with the presence of appropriate epigenetic information.1234 The most well-studied mechanism of epigenetic inheritance is the reversible methylation of cytosine residues in cytosine-guanine dinucleotides at imprinted genes, which is involved in gene expression regulation.56 However, additional potential sperm epigenetic information is also constituted by the presence of histone modifications, presence of other chromatin-associated proteins and their modifications, RNAs, a unique chromatin structure (Figure 1), and chromosome territories in the nucleus.789101112131415 As compared to somatic cells, not much is known so far about the potential role of these additional forms of epigenetic information in the sperm, despite that it is an emerging subject of increasing interest.31016171819 Thus, the present review aims to cover these newer forms of epigenetic information, being focused on the chromatin structure, gene distribution and presence of chromatin proteins and their modifications in the sperm cell (Figure 1). Therefore, it does not aim to cover the topics of sperm DNA methylation and the presence of sperm RNAs, for which the reader is referred to other excellent reviews.572021 Furthermore, the present review does not intend to cover related issues concerning the potential origins and consequences of sperm DNA damage, for which recent reviews are also available.2223242526


Human sperm chromatin epigenetic potential: genomics, proteomics, and male infertility.

Castillo J, Estanyol JM, Ballesc√° JL, Oliva R - Asian J. Androl. (2015 Jul-Aug)

Gene and protein composition of the human sperm chromatin. Hypothetical model of human sperm chromatin showing the histone-associated DNA constitution (a) and protein contents (b). The model is drawn at a scale and inspired by the known nucleo-protamine toroidal structures124 and the high-throughput sequencing data obtained from the analysis of retained human sperm nucleosomes after micrococcal nuclease digestion.4344455152
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4492051&req=5

Figure 1: Gene and protein composition of the human sperm chromatin. Hypothetical model of human sperm chromatin showing the histone-associated DNA constitution (a) and protein contents (b). The model is drawn at a scale and inspired by the known nucleo-protamine toroidal structures124 and the high-throughput sequencing data obtained from the analysis of retained human sperm nucleosomes after micrococcal nuclease digestion.4344455152
Mentions: The main function of the sperm cell is to transmit to the embryo the paternal genetic message encoded in the DNA sequence together with the presence of appropriate epigenetic information.1234 The most well-studied mechanism of epigenetic inheritance is the reversible methylation of cytosine residues in cytosine-guanine dinucleotides at imprinted genes, which is involved in gene expression regulation.56 However, additional potential sperm epigenetic information is also constituted by the presence of histone modifications, presence of other chromatin-associated proteins and their modifications, RNAs, a unique chromatin structure (Figure 1), and chromosome territories in the nucleus.789101112131415 As compared to somatic cells, not much is known so far about the potential role of these additional forms of epigenetic information in the sperm, despite that it is an emerging subject of increasing interest.31016171819 Thus, the present review aims to cover these newer forms of epigenetic information, being focused on the chromatin structure, gene distribution and presence of chromatin proteins and their modifications in the sperm cell (Figure 1). Therefore, it does not aim to cover the topics of sperm DNA methylation and the presence of sperm RNAs, for which the reader is referred to other excellent reviews.572021 Furthermore, the present review does not intend to cover related issues concerning the potential origins and consequences of sperm DNA damage, for which recent reviews are also available.2223242526

Bottom Line: Interestingly, recent proteomic studies have shown that sperm chromatin contains many additional proteins, in addition to the abundant histones and protamines, with specific modifications and chromatin affinity features which are also delivered to the oocyte.Both gene and protein signatures seem to be altered in infertile patients and, as such, are consistent with the potential involvement of the sperm chromatin landscape in early embryo development.As a complement, we provide experimental evidence for the detection of phosphorylations and acetylations in human protamine 1 using a mass spectrometry approach.

View Article: PubMed Central - PubMed

Affiliation: Human Genetics Research Group, IDIBAPS, Faculty of Medicine, University of Barcelona, Casanova 143; Biochemistry and Molecular Genetics Service, Biomedical Diagnostic Centre, Hospital Clinic, Villarroel 170, 08036 Barcelona, Spain.

ABSTRACT
The classical idea about the function of the mammalian sperm chromatin is that it serves to transmit a highly protected and transcriptionally inactive paternal genome, largely condensed by protamines, to the next generation. In addition, recent sperm chromatin genome-wide dissection studies indicate the presence of a differential distribution of the genes and repetitive sequences in the protamine-condensed and histone-condensed sperm chromatin domains, which could be potentially involved in regulatory roles after fertilization. Interestingly, recent proteomic studies have shown that sperm chromatin contains many additional proteins, in addition to the abundant histones and protamines, with specific modifications and chromatin affinity features which are also delivered to the oocyte. Both gene and protein signatures seem to be altered in infertile patients and, as such, are consistent with the potential involvement of the sperm chromatin landscape in early embryo development. This present work reviews the available information on the composition of the human sperm chromatin and its epigenetic potential, with a particular focus on recent results derived from high-throughput genomic and proteomic studies. As a complement, we provide experimental evidence for the detection of phosphorylations and acetylations in human protamine 1 using a mass spectrometry approach. The available data indicate that the sperm chromatin is much more complex than what it was previously thought, raising the possibility that it could also serve to transmit crucial paternal epigenetic information to the embryo.

No MeSH data available.


Related in: MedlinePlus