Histone Post-Translational Modifications and CircRNAs in Mouse and Human Spermatozoa: Potential Epigenetic Marks to Assess Human Sperm Quality

Overview

Journal J Clin Med

Specialty General Medicine

Date 2020 Mar 4

PMID 32121034

Citations 32

Authors

Teresa Chioccarelli

Riccardo Pierantoni

Francesco Manfrevola

Veronica Porreca

Silvia Fasano

Rosanna Chianese

Gilda Cobellis

Affiliations

Soon will be listed here.

Abstract

Spermatozoa (SPZ) are motile cells, characterized by a cargo of epigenetic information including histone post-translational modifications (histone PTMs) and non-coding RNAs. Specific histone PTMs are present in developing germ cells, with a key role in spermatogenic events such as self-renewal and commitment of spermatogonia (SPG), meiotic recombination, nuclear condensation in spermatids (SPT). Nuclear condensation is related to chromatin remodeling events and requires a massive histone-to-protamine exchange. After this event a small percentage of chromatin is condensed by histones and SPZ contain nucleoprotamines and a small fraction of nucleohistone chromatin carrying a landascape of histone PTMs. Circular RNAs (circRNAs), a new class of non-coding RNAs, characterized by a nonlinear back-spliced junction, able to play as microRNA (miRNA) sponges, protein scaffolds and translation templates, have been recently characterized in both human and mouse SPZ. Since their abundance in eukaryote tissues, it is challenging to deepen their biological function, especially in the field of reproduction. Here we review the critical role of histone PTMs in male germ cells and the profile of circRNAs in mouse and human SPZ. Furthermore, we discuss their suggested role as novel epigenetic biomarkers to assess sperm quality and improve artificial insemination procedure.

Citing Articles

Circular RNAs as a novel class of potential therapeutic and diagnostic biomarkers in reproductive biology/diseases.

Song W, Chen X, Wu H, Rahimian N Eur J Med Res. 2024; 29(1):643.

PMID: 39741306 PMC: 11689626. DOI: 10.1186/s40001-024-02230-7.

Unfolding the complexity of epigenetics in male reproductive aging: a review of therapeutic implications.

Ajayi A, Oyovwi M, Olatinwo G, Phillips A Mol Biol Rep. 2024; 51(1):881.

PMID: 39085654 DOI: 10.1007/s11033-024-09823-9.

Variation of sperm quality and circular RNA content in men exposed to environmental contamination with heavy metals in 'Land of Fires', Italy.

Mele V, Chioccarelli T, Diano N, Cappetta D, Ferraro B, Telesca M Hum Reprod. 2024; 39(8):1628-1644.

PMID: 38885964 PMC: 11291948. DOI: 10.1093/humrep/deae109.

Sperm epigenetics and male infertility: unraveling the molecular puzzle.

Hosseini M, Khalafiyan A, Zare M, Karimzadeh H, Bahrami B, Hammami B Hum Genomics. 2024; 18(1):57.

PMID: 38835100 PMC: 11149391. DOI: 10.1186/s40246-024-00626-4.

Expression profiles of circular RNAs in spermatozoa from aging men.

Zhou Q, Liu A, Ji H, Ji J, Sun J, Ling Z Mol Biol Rep. 2023; 50(10):8081-8088.

PMID: 37540460 DOI: 10.1007/s11033-023-08705-w.

References

Beaujean N . Histone post-translational modifications in preimplantation mouse embryos and their role in nuclear architecture. Mol Reprod Dev. 2013; 81(2):100-12. DOI: 10.1002/mrd.22268. View

Pryor A, Tung L, Yang Z, Kapadia F, Chang T, Johnson L . Growth-regulated expression and G0-specific turnover of the mRNA that encodes URH49, a mammalian DExH/D box protein that is highly related to the mRNA export protein UAP56. Nucleic Acids Res. 2004; 32(6):1857-65. PMC: 390356. DOI: 10.1093/nar/gkh347. View

Grabarz A, Barascu A, Guirouilh-Barbat J, Lopez B . Initiation of DNA double strand break repair: signaling and single-stranded resection dictate the choice between homologous recombination, non-homologous end-joining and alternative end-joining. Am J Cancer Res. 2012; 2(3):249-68. PMC: 3365807. View

Ivanov A, Memczak S, Wyler E, Torti F, Porath H, Orejuela M . Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep. 2015; 10(2):170-7. DOI: 10.1016/j.celrep.2014.12.019. View

Champroux A, Cocquet J, Henry-Berger J, Drevet J, Kocer A . A Decade of Exploring the Mammalian Sperm Epigenome: Paternal Epigenetic and Transgenerational Inheritance. Front Cell Dev Biol. 2018; 6:50. PMC: 5962689. DOI: 10.3389/fcell.2018.00050. View

Kouzarides T . Chromatin modifications and their function. Cell. 2007; 128(4):693-705. DOI: 10.1016/j.cell.2007.02.005. View

Loher P, Telonis A, Rigoutsos I . MINTmap: fast and exhaustive profiling of nuclear and mitochondrial tRNA fragments from short RNA-seq data. Sci Rep. 2017; 7:41184. PMC: 5318995. DOI: 10.1038/srep41184. View

Brunner A, Nanni P, Mansuy I . Epigenetic marking of sperm by post-translational modification of histones and protamines. Epigenetics Chromatin. 2014; 7(1):2. PMC: 3904194. DOI: 10.1186/1756-8935-7-2. View

Stiavnicka M, Garcia-Alvarez O, Ulcova-Gallova Z, Sutovsky P, Abril-Parreno L, Dolejsova M . H3K4me2 accompanies chromatin immaturity in human spermatozoa: an epigenetic marker for sperm quality assessment. Syst Biol Reprod Med. 2019; 66(1):3-11. DOI: 10.1080/19396368.2019.1666435. View

10.

Parvanov E, Petkov P, Paigen K . Prdm9 controls activation of mammalian recombination hotspots. Science. 2010; 327(5967):835. PMC: 2821451. DOI: 10.1126/science.1181495. View

11.

Cacciola G, Chioccarelli T, Altucci L, Ledent C, Mason J, Fasano S . Low 17beta-estradiol levels in CNR1 knock-out mice affect spermatid chromatin remodeling by interfering with chromatin reorganization. Biol Reprod. 2013; 88(6):152. DOI: 10.1095/biolreprod.112.105726. View

12.

Chianese R, Ciaramella V, Scarpa D, Fasano S, Pierantoni R, Meccariello R . Anandamide regulates the expression of GnRH1, GnRH2, and GnRH-Rs in frog testis. Am J Physiol Endocrinol Metab. 2012; 303(4):E475-87. DOI: 10.1152/ajpendo.00086.2012. View

13.

Meccariello R, Chianese R, Chioccarelli T, Ciaramella V, Fasano S, Pierantoni R . Intra-testicular signals regulate germ cell progression and production of qualitatively mature spermatozoa in vertebrates. Front Endocrinol (Lausanne). 2014; 5:69. PMC: 4021137. DOI: 10.3389/fendo.2014.00069. View

14.

Myrick D, Christopher M, Scott A, Simon A, Donlin-Asp P, Kelly W . KDM1A/LSD1 regulates the differentiation and maintenance of spermatogonia in mice. PLoS One. 2017; 12(5):e0177473. PMC: 5428937. DOI: 10.1371/journal.pone.0177473. View

15.

Bell E, Nagamori I, Williams E, Del Rosario A, Bryson B, Watson N . SirT1 is required in the male germ cell for differentiation and fecundity in mice. Development. 2014; 141(18):3495-504. PMC: 4197722. DOI: 10.1242/dev.110627. View

16.

Kato Y, Alavattam K, Sin H, Meetei A, Pang Q, Andreassen P . FANCB is essential in the male germline and regulates H3K9 methylation on the sex chromosomes during meiosis. Hum Mol Genet. 2015; 24(18):5234-49. PMC: 4550819. DOI: 10.1093/hmg/ddv244. View

17.

Tamburini B, Tyler J . Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol Cell Biol. 2005; 25(12):4903-13. PMC: 1140608. DOI: 10.1128/MCB.25.12.4903-4913.2005. View

18.

Aravin A, Sachidanandam R, Girard A, Fejes-Toth K, Hannon G . Developmentally regulated piRNA clusters implicate MILI in transposon control. Science. 2007; 316(5825):744-7. DOI: 10.1126/science.1142612. View

19.

Zhou T, Xie X, Li M, Shi J, Zhou J, Knox K . Rat BodyMap transcriptomes reveal unique circular RNA features across tissue types and developmental stages. RNA. 2018; 24(11):1443-1456. PMC: 6191709. DOI: 10.1261/rna.067132.118. View

20.

Krishnamoorthy T, Chen X, Govin J, Cheung W, Dorsey J, Schindler K . Phosphorylation of histone H4 Ser1 regulates sporulation in yeast and is conserved in fly and mouse spermatogenesis. Genes Dev. 2006; 20(18):2580-92. PMC: 1578680. DOI: 10.1101/gad.1457006. View