Spermatozoa DNA methylation patterns differ due to peripubertal age in bulls

Lambert, Simon A.; Blondin, Patrick; Vigneault, Christian; Labrecque, Rémi; Dufort, Isabelle; Sirard, Marc‐André

doi:10.1016/j.theriogenology.2017.10.006

Cited by 41 publications

(51 citation statements)

References 32 publications

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“…Moreover, in the mouse, the global reprogramming during early embryonic development does not erase all methylation marks from the sperm, leaving a few regions for inter or transgenerational inheritance [32]. In our study mentioned above, there were over 2,600 differentially methylated regions between sperm of bulls at 10 and 16 months of age, including one of them located on an imprinted gene [11]. Recently, contradictory evidence cast some doubts on whether sperm DNA methylation is either the primary or the persistent epigenetic carrier of paternally acquired traits [33,34].…”

Section: Sncrnas As Epigenetic Inheritance Factorsmentioning

confidence: 52%

“…Epigenetic information in sperm was proven to translate the environmental experiences of the father who could then transfer these acquired traits to his progeny [31]. In a previous study from our lab, sperm from prepubertal bulls were characterized to bear a different DNA methylation pattern compared to sperm from post-pubertal bulls [11]. Moreover, in the mouse, the global reprogramming during early embryonic development does not erase all methylation marks from the sperm, leaving a few regions for inter or transgenerational inheritance [32].…”

Section: Sncrnas As Epigenetic Inheritance Factorsmentioning

confidence: 99%

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Sperm miRNAs— potential mediators of bull age and early embryo development

Blondin

Vigneault

et al. 2020

Preprint

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Background: Sperm miRNAs were reported to regulate spermatogenesis and early embryonic development in some mammals including bovine. The dairy cattle breeding industry now tends to collect semen from younger bulls under high selection pressure at a time when semen quality may be suboptimal compared to adult bulls. Whether the patterns of spermatic miRNAs are affected by paternal age and/or impact early embryogenesis is not clear. Hence, we generated small non-coding RNA libraries of sperm collected from same bulls at 10, 12, and 16 months of age, using 16 months as control for differential expression and functional analysis. Results: We firstly excluded all miRNAs present in measurable quantity in oocytes according to the literature. Of the remaining miRNAs, ten sperm-borne miRNAs were significantly differentially expressed in younger bulls (four in the 10 vs 16 months contrast and six in the 12 vs 16 months contrast). Targets of miRNAs were identified and compared to the transcriptomic database of two-cell embryos, to genes related to two-cell competence, and to the transcriptomic database of blastocysts. Ingenuity pathway analysis of the targets of these miRNAs suggested potential influence on the developmental competence of two-cell embryos and on metabolism and protein synthesis in blastocysts. Conclusions: The results showed that miRNA patterns in sperm are affected by the age of the bull and may mediate the effects of paternal age on early embryonic development.

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Section: Sncrnas As Epigenetic Inheritance Factorsmentioning

confidence: 52%

Section: Sncrnas As Epigenetic Inheritance Factorsmentioning

confidence: 99%

Sperm miRNAs— potential mediators of bull age and early embryo development

Blondin

Vigneault

et al. 2020

Preprint

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“…DNA methylation can be assessed by microarray analysis, which allows the comparison of treatments or status such as age and the identification of DMRs in embryos. Our group contributed to the development of the EmbryoGENE epigenetic platform, which was previously used to assess the influence of the environment on embryo development (Lambert et al, 2018; Salilew‐Wondim et al, 2015; Tremblay, Dufort, & Sirard, 2018).…”

Section: Methodsmentioning

confidence: 99%

DNA methylation status of bovine blastocysts obtained from peripubertal oocyte donors

Morin-Doré

Blondin²,

Vigneault³

et al. 2020

Molecular Reproduction Devel

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In the dairy industry, the high selection pressure combined with the increased efficiency of assisted reproduction technologies (ART) are leading toward the use of younger females for reproduction purposes, with the aim to reduce the interval between generations. This situation could impair embryo quality, decreasing the success rate of the ART procedures and the values of resulting offspring. Young Holstein heifers (n = 10) were subjected to ovarian stimulation and oocyte collection at 8, 11, and 14 months of age. All the oocytes were fertilized in vitro with semen from one adult bull, generating three pools of embryos per animal. Each animal was its own control for the evaluation of the effects of age. The EmbryoGENE platform was used to compare the DNA methylation status of blastocysts obtained from oocytes collected at 8 versus 14 and 11 versus 14 months of age. Age‐related contrast analysis identified 5,787 and 3,658 differentially methylated regions (DMRs) in blastocysts from heifers at 8 versus 14 and 11 versus 14 months of age, respectively. For both contrasts, the DMRs were distributed nonrandomly in the different DNA regions. The DNA from embryos from 8‐month‐old donors was more hypermethylated, while the DNA from embryos from 11‐month‐old donors displayed an intermediate phenotype. According to Ingenuity Pathway Analysis, the upstream regulator genes cellular tumor antigen p53, transforming growth factor β1, tumor necrosis factor, and hepatocyte nuclear factor 4α are particularly associated with methylation sensitive targets, which were more hypermethylated in embryos from younger donors.

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“…Indeed, lower levels of DNA condensation, protamine exchange, and higher DNA damage have been observed in sperm from lower fertility bulls in comparison to higher fertility bulls (Dogan et al, 2015). In addition, a recent study focusing on the epigenetic profiles of young bulls highlighted that 10-month-old bulls have a different sperm DNA methylation pattern compared with both 12-and 16-monthold bulls (Lambert et al, 2018). Given the current trend of using semen from elite genomically selected bulls, this study demonstrates that such bulls not only have poorer sperm motility and morphology but also an altered epigenetic profile that has the potential to influence embryonic development as well as the genotype and the phenotype of the subsequent offspring.…”

Section: Sperm Transport In the Female Tractmentioning

confidence: 99%

Review: Understanding the causes of variation in reproductive wastage among bulls

Fair

Lonergan

2018

Animal

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The ability to predict the fertility of bulls before semen is released into the field has been a long-term objective of the animal breeding industry. However, the recent shift in the dairy industry towards the intensive use of young genomically selected bulls has increased its urgency. Such bulls, which are often in the highest demand, are frequently only used intensively for one season and consequently there is limited time to track their field fertility. A more pressing issue is that they produce fewer sperm per ejaculate than mature bulls and therefore there is a need to reduce the sperm number per straw to the minimum required without a concomitant reduction in fertility. However, as individual bulls vary in the minimum number of sperm required to achieve their maximum fertility, this cannot be currently achieved without extensive field-testing. Although an in vitro semen quality test, or combination of tests, which can accurately and consistently determine a bull's fertility and the optimum sperm number required represent the 'holy grail' in terms of semen assessment, this has not been achieved to date. Understanding the underlying causes of variation in bull fertility is a key prerequisite to achieving this goal. In this review, we consider the reliability of sire conception rate estimates and then consider where along the pregnancy establishment axis the variation in reproductive loss between bulls occurs. We discuss the aetiology of these deficiencies in sperm function and propose avenues for future investigation.

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Spermatozoa DNA methylation patterns differ due to peripubertal age in bulls

Cited by 41 publications

References 32 publications

Sperm miRNAs— potential mediators of bull age and early embryo development

Sperm miRNAs— potential mediators of bull age and early embryo development

DNA methylation status of bovine blastocysts obtained from peripubertal oocyte donors

Review: Understanding the causes of variation in reproductive wastage among bulls

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