Prepubertal nutritional modulation in the bull and its impact on sperm DNA methylation

Johnson, Chinju; Kiefer, Hélène; Chaulot-Talmon, Aurélie; Dance, Alysha; Sellem, Eli; Jouneau, Luc; Jammes, Hélène; Kastelic, John P.; Thundathil, Jacob C.

doi:10.1007/s00441-022-03659-0

Cited by 6 publications

(3 citation statements)

References 77 publications

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“…An additional report in sheep indicated that prenatal ewe nutrition can have an impact on offspring epigenetic marks in sperm at reproductive maturity ( Toschi et al, 2020 ). Sperm methylation patterns in post-pubertal bulls are influenced by their respective plane of nutritional management during the first 24 ( Perrier et al, 2020 ), or 32 ( Johnson et al, 2022 ) weeks of age, which also encompasses the period of major Sertoli cell proliferation and the subsequent early increase in the number of germ cells (Negrin et al, unpublished). Perhaps spermatogonial stem cells are particularly susceptible to epigenetic alterations during this early period of rapid proliferation.…”

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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Section: Timing Of Alterationsmentioning

confidence: 99%

Paternal effects on fetal programming

Dahlen,

Amat,

Caton

et al. 2023

Anim. Reprod.

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“…Interestingly, different aspects of lifestyle such as diet, toxicant exposure, air pollution, smoking, or work conditions affect the pattern of DNA and histone methylation, in human and mouse models, which may impact in the etiology of sperm pathologies such as globozoospermia (Comhaire et al, 2017;Dong et al, 2017;Lu et al, 2019). In fact, different studies have found significant differences in the rate of hyper and hypomethylation in different DNA regions between fertile and infertile men (Johnson et al, 2022;Momeni et al, 2020;Sujit et al, 2018Sujit et al, , 2020. Interestingly, SPATA4, SPATA5, and SPATA6 genes are highly hypermethylated in oligozoospermic patients in comparison to controls, but there is no evidence that, other members of the SPATA family, such as SPATA16, undergo similar or other epigenetic modifications (Sujit et al, 2020).…”

Section: Epigenetic Regulation Of Acrosome Biogenesismentioning

confidence: 99%

Human globozoospermia‐related genes and their role in acrosome biogenesis

Moreno

2022

WIREs Mechanisms of Disease

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The mammalian acrosome is a secretory vesicle attached to the sperm nucleus whose fusion with the overlying plasma membrane is required to achieve fertilization. Acrosome biogenesis starts during meiosis, but it lasts through the entire process of haploid cell differentiation (spermiogenesis). Acrosome biogenesis is a stepwise process that involves membrane traffic from the Golgi apparatus, but it also seems that the lysosome/endosome system participates in this process. Defective sperm head morphology is accompanied by defective acrosome shape and function, and patients with these characteristics are infertile or subfertile. The most extreme case of acrosome biogenesis failure is globozoospermia syndrome, which is primarily characterized by the presence of round‐headed spermatozoa without acrosomes with cytoskeleton defects around the nucleus and infertility. Several genes participating in acrosome biogenesis have been uncovered using genetic deletions in mice, but only a few of them have been found to be deleted or modified in patients with globozoospermia. Understanding acrosome biogenesis is crucial to uncovering the molecular basis of male infertility and developing new diagnostic tools and assisted reproductive technologies that may help infertile patients through more effective treatment techniques. This article is categorized under: Reproductive System Diseases > Environmental Factors Infectious Diseases > Stem Cells and Development Reproductive System Diseases > Molecular and Cellular Physiology

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“…There is also evidence that supports cellular senescence caused by oxidative stress and macromolecular damage [21][22][23]. Epigenetic changes that program gene expression in later life are important for nutritional programming [24][25][26][27]. Restricting dietary yeast extract during development can extend the lifespan of the fruit fly itself and its conspecific neighbors by reducing the production of lipid autotoxins [16].…”

Section: Introductionmentioning

confidence: 99%

Nutritional Programming of the Lifespan of Male Drosophila by Activating FOXO on Larval Low-Nutrient Diet

et al. 2023

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Nutrition during the developmental stages has long-term effects on adult physiology, disease and lifespan, and is termed nutritional programming. However, the underlying molecular mechanisms of nutritional programming are not yet well understood. In this study, we showed that developmental diets could regulate the lifespan of adult Drosophila in a way that interacts with various adult diets during development and adulthood. Importantly, we demonstrated that a developmental low-yeast diet (0.2SY) extended both the health span and lifespan of male flies under nutrient-replete conditions in adulthood through nutritional programming. Males with a low-yeast diets during developmental stages had a better resistance to starvation and lessened decline of climbing ability with age in adulthood. Critically, we revealed that the activity of the Drosophila transcription factor FOXO (dFOXO) was upregulated in adult males under developmental low-nutrient conditions. The knockdown of dFOXO, with both ubiquitous and fat-body-specific patterns, can completely abolish the lifespan-extending effect from the larval low-yeast diet. Ultimately, we identify that the developmental diet achieved the nutritional programming of the lifespan of adult males by modulating the activity of dFOXO in Drosophila. Together, these results provide molecular evidence that the nutrition in the early life of animals could program the health of their later life and their longevity.

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Prepubertal nutritional modulation in the bull and its impact on sperm DNA methylation

Cited by 6 publications

References 77 publications

Paternal effects on fetal programming

Paternal effects on fetal programming

Human globozoospermia‐related genes and their role in acrosome biogenesis

Nutritional Programming of the Lifespan of Male Drosophila by Activating FOXO on Larval Low-Nutrient Diet

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