A Decade of Exploring the Mammalian Sperm Epigenome: Paternal Epigenetic and Transgenerational Inheritance

Champroux, Alexandre; Cocquet, Julie; Henry-Berger, Joëlle; Drevet, Joël R.; Kocer, Ayhan

doi:10.3389/fcell.2018.00050

Cited by 132 publications

(133 citation statements)

References 248 publications

(310 reference statements)

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“…SPZ-borne RNAs constitute a heterogeneous family of both coding and ncRNAs [41]. According to their size, ncRNAs may be grouped in long or small ncRNAs [42,43].…”

Section: Sperm Rna Codementioning

confidence: 99%

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

Chioccarelli

Pierantoni

Manfrevola

et al. 2020

JCM

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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.

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“…SPZ-borne RNAs constitute a heterogeneous family of both coding and ncRNAs [41]. According to their size, ncRNAs may be grouped in long or small ncRNAs [42,43].…”

Section: Sperm Rna Codementioning

confidence: 99%

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

Chioccarelli

Pierantoni

Manfrevola

et al. 2020

JCM

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“…It is possible that the sperm epigenome keeps memory of diet during pre-pubertal period in genes critical for sperm function. However, more and more studies in humans have demonstrated the ability of paternal environment to influence the epigenetic/non-genetic information transmission carried by sperm cells and modify the trajectory of offspring [39][40][41] .…”

Section: Discussionmentioning

confidence: 99%

Enhanced pre-pubertal nutrition upregulates mitochondrial function in testes and sperm of post-pubertal Holstein bulls

Johnson

Dance

Kovalchuk

et al. 2020

Sci Rep

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Supplemental energy and protein during calf-hood (2-30 wk) in dairy bulls hastened puberty (~1 mo), upregulated steroid biosynthesis, concentrations of reproductive hormones and Sertoli cell maturation, with larger testes and greater sperm production (~25%) in mature bulls. The objective was to evaluate effects of feeding high (20.0% crude protein [CP], 67.9% total digestible nutrients [TDN]), control/ medium (17.0% CP, 66.0% TDN) and low (12.2% CP, 62.9% TDN) diets from 2 to 30 wk on post-pubertal testes of Holstein bulls. Based on RNA sequencing, 497 and 2961 genes were differentially expressed (p < 0.1) in high-vs low-and high-vs medium-diet groups, respectively. According to KEGG analysis, oxidative phosphorylation and ribosome pathways were upregulated in high-vs medium-and low-diet groups, with majority of upregulated genes encoding for essential subunits of complex I, III, IV and V of OXYPHOS pathway. In addition, mitochondrial translation, mitotic nuclear division and cell division were enriched in high-vs medium-diet groups. Consistent with these results, a greater percentage of sperm from high-diet bulls were progressively motile and had normal mitochondrial function compared to medium-diet sperm (p < 0.1). Thus, enhanced early life nutrition upregulated mitochondrial function in testes and sperm of post-pubertal Holstein bulls.Enhanced early-life nutrition hastens puberty, with ~25% increases in testis size and sperm production in dairy and beef bulls 1,2 . The underlying endocrine basis is profound increases in luteinizing hormone (LH) pulse frequency and insulin like growth factor (IGF-I) concentrations in blood 3,4 . In a cohort-based study in Sweden, low nutrition during the pre-pubertal period in men reduced susceptibility to heart disease in their offspring 5 , consistent with developmental programming in male germ cells that extends well into early post-natal life 6 . Therefore, nutritional modulation during early life affects testicular development, with apparent epigenetic effects on post-pubertal sperm function.We reported increased cholesterol/steroid biosynthesis and Sertoli cell maturation in testicular tissues of high-diet bulls at 16 and 24 wk, respectively 7 . Although a wide range in pre-pubertal diets had no significant effects on routine analyses of sperm morphology and function 8 , molecular-level analyses should be done, to ensure no deleterious effects are transmitted to the next generation. Our objective was to determine effects of pre-pubertal dietary modulations on post-pubertal testes of Holstein bulls. ResultsmRNA profile of testes. Approximately 340 × 10 6 reads were obtained from the 24 libraries sequenced. On average, 14,357,890 (SD = 2,267,076) reads were obtained per library and 13,565,597 (SD = 2,148,261) mapped to the Ensemble gene annotation database. On average 13,710,936 (SD = 3,098,630), 13,120,341 (SD = 1,219,498) and 13,865,513 (SD = 1,929,109) reads were mapped from HD, MD and LD groups respectively. A total of 18,288 genes were detected in testicular tissue and...

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“…However, no follow‐up on offspring born has been reported. Therefore, a reasonable possibility exists that an unknown percentage of children born to fathers without a fertility diagnosis may have occult paternally transmitted imprinting errors—and these children may in turn transmit the errors to their future offspring (Champroux et al , ).…”

Section: Beyond the Male Genomementioning

confidence: 99%

The present crisis in male reproductive health: an urgent need for a political, social, and research roadmap

Jonge

Barratt

2019

Andrology

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Background: There is a global crisis in male reproductive health. Evidence comes from globally declining sperm counts and increasing male reproductive system abnormalities, such as cryptorchidism, germ cell tumors, and onset of puberty. Male factor infertility occurs in~40% of couples experiencing infertility. Data demonstrate an association between male infertility and overall health. Associated significant health conditions include diabetes mellitus, metabolic disorders, and cardiovascular disease. Adding to the complexity is that men typically do not seek health care unless there is acute medical need or, as in the case of the infertile couple, the male goes for a reproductive examination and semen analysis. However, 25% of the time a reproductive health examination does not occur. Couples are increasingly utilizing IVF at more advanced ages, and advanced paternal age is associated with increased risk for (i) adverse perinatal outcomes for both offspring and mother; (ii) early child mortality, cancer, and mental health issues. In addition to age, paternal lifestyle factors, such as obesity and smoking, impact not only the male fertility but also the offspring wellness.Objectives: The purpose of this paper was (i) to spotlight emerging and concerning data on male reproductive health, the relationship(s) between male reproductive and somatic health, and the heritable conditions father can pass to offspring, and (ii) to present a strategic roadmap with the goals of increasing (a) the awareness of men and society on the aforementioned, (b) the participation of men in healthcare seeking, and (c) advocacy to invigorate policy and funding agencies to support increased research into male reproductive biology. Conclusions: The Male Reproductive Health Initiative (MRHI) is a newly established and rapidly growing global consortium of key opinion leaders in research, medicine, funding and policy agencies, and patient support groups that are moving forward the significant task of accomplishing the goals of the strategic roadmap.

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A Decade of Exploring the Mammalian Sperm Epigenome: Paternal Epigenetic and Transgenerational Inheritance

Cited by 132 publications

References 248 publications

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

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

Enhanced pre-pubertal nutrition upregulates mitochondrial function in testes and sperm of post-pubertal Holstein bulls

The present crisis in male reproductive health: an urgent need for a political, social, and research roadmap

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