The epigenome of male germ cells and the programming of phenotypes in cattle

Kiefer, Hélène; Sellem, Eli; Bonnet-Garnier, Amélie; Pannetier, Maëlle; Costes, Valentin; Schibler, Laurent; Jammes, Hélène

doi:10.1093/af/vfab062

Cited by 12 publications

(8 citation statements)

References 62 publications

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“…Sperm epigenomes (e.g., DNA methylation, chromatin-associated proteins and non-coding RNAs) will be partly transmitted to the embryo, leading to the so-called intergenerational and transgenerational epigenetic inheritance, to influence the early development and health of offspring [ 2 ]. Furthermore, selection, breeding, and semen processing practices for AI may potentially cause epigenetic alterations of sperms, whereas other practices like embryo technology or hormonal treatments may influence sperm epigenome in the long-term period [ 3 ]. Undoubtedly, the understanding of bovine sperm epigenome and the identification of epigenetic biomarkers of sperm quality can help the selection of superior bulls in terms of both male fertility and genetic values of other economic traits reflected in the offspring (e.g., milk production and health) [ 4 – 6 ].…”

Section: The Epigenome Of Bovine Spermmentioning

confidence: 99%

“…2 ). The toroid-shaped structure of DNA is finally formed with arginine-rich protamines to enable a higher level of chromatin compaction [ 3 ], which helps to reduce nuclear volume and avoids oxidation during migration for fertilization of an oocyte. Therefore, spermatozoa are usually transcriptionally inactive, and their epigenome is unique as the ultimate form of male germ cell differentiation [ 16 ].…”

Section: The Epigenome Of Bovine Spermmentioning

confidence: 99%

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Harnessing male germline epigenomics for the genetic improvement in cattle

Wang

Feng

et al. 2023

J Animal Sci Biotechnol

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Sperm is essential for successful artificial insemination in dairy cattle, and its quality can be influenced by both epigenetic modification and epigenetic inheritance. The bovine germline differentiation is characterized by epigenetic reprogramming, while intergenerational and transgenerational epigenetic inheritance can influence the offspring’s development through the transmission of epigenetic features to the offspring via the germline. Therefore, the selection of bulls with superior sperm quality for the production and fertility traits requires a better understanding of the epigenetic mechanism and more accurate identifications of epigenetic biomarkers. We have comprehensively reviewed the current progress in the studies of bovine sperm epigenome in terms of both resources and biological discovery in order to provide perspectives on how to harness this valuable information for genetic improvement in the cattle breeding industry.

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Section: The Epigenome Of Bovine Spermmentioning

confidence: 99%

Section: The Epigenome Of Bovine Spermmentioning

confidence: 99%

Harnessing male germline epigenomics for the genetic improvement in cattle

Wang

Feng

et al. 2023

J Animal Sci Biotechnol

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“…The programming role of the paternal environment has been revealed in the past decade, with effects of paternal nutrition or exposure to environmental disruptors being reported in their offspring for several generations (Oshio et al, 2020;Soubry, 2018aSoubry, , 2018b. Briefly, genome-wide erasure and re-apposition of DNA methylation take place during pregnancy in the foetal male primordial germ cells and pro-spermatogonia, with different timing relative to conception in mice and cattle (Kiefer et al, 2021). This is an important window of epigenetic plasticity that can be altered by gestational conditions, with modifications of the sperm methylome that in mice have been shown to affect subsequent offspring fertility (Lambrot et al, 2013) and metabolism (Martinez et al, 2014).…”

Section: Paternalenvironmentmentioning

confidence: 99%

Intra‐uterine programming of future fertility

Chavatte‐Palmer,

Couturier‐Tarrade,

Rousseau‐Ralliard

2023

Reprod Domestic Animals

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The developmental origins of health and disease (DOHaD) shows that a relationship exists between parental environment at large, foeto‐placental development and the risk for the offspring to develop non‐transmittable disease(s) in adulthood. This concept has been validated in both humans and livestock. In mammals, after fertilization and time spent free in the maternal reproductive tract, the embryo develops a placenta that, in close relationship with maternal endometrium, is the organ responsible for exchanges between dam and foetus. Any modification of the maternal environment can lead to adaptive mechanisms affecting placental morphology, blood flow, foetal‐maternal exchanges (transporters) and/or endocrine function, ultimately modifying placental efficiency. Among deleterious environments, undernutrition, protein restriction, overnutrition, micronutrient deficiencies and food contaminants can be outlined. When placental adaptive capacities become insufficient, foetal growth and organ formation is no longer optimal, including foetal gonadal formation and maturation, which can affect subsequent offspring fertility. Since epigenetic mechanisms have been shown to be key to foetal programming, epigenetic modifications of the gametes may also occur, leading to inter‐generational effects. After briefly describing normal gonadal development in domestic species and inter‐species differences, this review highlights the current knowledge on intra‐uterine programming of offspring fertility with a focus on domestic animals and underlines the importance to assess transgenerational effects on offspring fertility at a time when new breeding systems are developed to face the current climate changes.

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“…The structure of the seminiferous epithelium is such that the youngest developmental stages of sperm are present outside of the blood-testis barrier, and as they advance in developmental age they reposition closer to the lumen of the seminiferous tubule before being released during spermiation. Therefore, the age of developing sperm affects both the physical contact with components outside of the blood-testis barrier (with spermatogonia and sperm stem cells being outside of the blood testis barrier) and the specific type of epigenetic alterations that are able to occur given the dynamic changes in sperm DNA packaging at the different stages of development ( Marcho et al, 2020 ; Kiefer et al, 2021 ).…”

Section: Timing Of Alterationsmentioning

confidence: 99%

Paternal effects on fetal programming

Dahlen,

Amat,

Caton

et al. 2023

Anim. Reprod.

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Paternal programming is the concept that the environmental signals from the sire’s experiences leading up to mating can alter semen and ultimately affect the phenotype of resulting offspring. Potential mechanisms carrying the paternal effects to offspring can be associated with epigenetic signatures (DNA methylation, histone modification and non-coding RNAs), oxidative stress, cytokines, and the seminal microbiome. Several opportunities exist for sperm/semen to be influenced during development; these opportunities are within the testicle, the epididymis, or accessory sex glands. Epigenetic signatures of sperm can be impacted during the pre-natal and pre-pubertal periods, during sexual maturity and with advancing sire age. Sperm are susceptible to alterations as dictated by their developmental stage at the time of the perturbation, and sperm and seminal plasma likely have both dependent and independent effects on offspring. Research using rodent models has revealed that many factors including over/under nutrition, dietary fat, protein, and ingredient composition (e.g., macro- or micronutrients), stress, exercise, and exposure to drugs, alcohol, and endocrine disruptors all elicit paternal programming responses that are evident in offspring phenotype. Research using livestock species has also revealed that sire age, fertility level, plane of nutrition, and heat stress can induce alterations in the epigenetic, oxidative stress, cytokine, and microbiome profiles of sperm and/or seminal plasma. In addition, recent findings in pigs, sheep, and cattle have indicated programming effects in blastocysts post-fertilization with some continuing into post-natal life of the offspring. Our research group is focused on understanding the effects of common management scenarios of plane of nutrition and growth rates in bulls and rams on mechanisms resulting in paternal programming and subsequent offspring outcomes. Understanding the implication of paternal programming is imperative as short-term feeding and management decisions have the potential to impact productivity and profitability of our herds for generations to come.

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The epigenome of male germ cells and the programming of phenotypes in cattle

Cited by 12 publications

References 62 publications

Harnessing male germline epigenomics for the genetic improvement in cattle

Harnessing male germline epigenomics for the genetic improvement in cattle

Intra‐uterine programming of future fertility

Paternal effects on fetal programming

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