Inheritance of paternal lifestyles and exposures through sperm DNA methylation

Greeson, Katherine W.; Crow, Krista M. Symosko; Edenfield, R. Clayton; Easley, Charles A.

doi:10.1038/s41585-022-00708-9

Cited by 16 publications

(6 citation statements)

References 203 publications

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“…More comprehensive studies on non-human mammalian species, focusing on the global epigenome, support this hypothesis, demonstrating significant changes in sperm DNA methylation after cryopreservation [94][95][96][97]. These data give rise to concerns, considering that sperm cryopreservation is frequently used in ART and that sperm DNA methylation may play a decisive role in offspring health [98]. Results on human spermatozoa published so far seem more reassuring because they have not shown significant alterations in the DNA methylation pattern after cryopreservation [99][100][101].…”

Section: Damage To Dnamentioning

confidence: 88%

Cryopreservation of Human Spermatozoa: Functional, Molecular and Clinical Aspects

Traini

Vignozzi

Baldi

et al. 2023

IJMS

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Cryopreservation is an expanding strategy to allow not only fertility preservation for individuals who need such procedures because of gonadotoxic treatments, active duty in dangerous occupations or social reasons and gamete donation for couples where conception is denied, but also for animal breeding and preservation of endangered animal species. Despite the improvement in semen cryopreservation techniques and the worldwide expansion of semen banks, damage to spermatozoa and the consequent impairment of its functions still remain unsolved problems, conditioning the choice of the technique in assisted reproduction procedures. Although many studies have attempted to find solutions to limit sperm damage following cryopreservation and identify possible markers of damage susceptibility, active research in this field is still required in order to optimize the process. Here, we review the available evidence regarding structural, molecular and functional damage occurring in cryopreserved human spermatozoa and the possible strategies to prevent it and optimize the procedures. Finally, we review the results on assisted reproduction technique (ARTs) outcomes following the use of cryopreserved spermatozoa.

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Section: Damage To Dnamentioning

confidence: 88%

Cryopreservation of Human Spermatozoa: Functional, Molecular and Clinical Aspects

Traini

Vignozzi

Baldi

et al. 2023

IJMS

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“…The current accepted model is that the sperm sncRNA pool is modified during the epididymal transit with substantial contribution from the epididymal epithelial cells 4 , 10 , 11 , 13 – 16 and, therefore, environmental perturbations are thought to act primarily on the epididymis. On the other hand, despite the presence of the blood–testis barrier 17 , perturbations targeted to spermatogenesis have intergenerational or even transgenerational consequences 18 , 19 . We focused on the intergenerational sequelae of paternal overweight and attempted to dissect the relative contributions of testicular and epididymal exposures.…”

Section: Mainmentioning

confidence: 99%

Epigenetic inheritance of diet-induced and sperm-borne mitochondrial RNAs

Tomar,

Gomez-Velazquez,

Gerlini

et al. 2024

Nature

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Spermatozoa harbour a complex and environment-sensitive pool of small non-coding RNAs (sncRNAs)1, which influences offspring development and adult phenotypes1–7. Whether spermatozoa in the epididymis are directly susceptible to environmental cues is not fully understood8. Here we used two distinct paradigms of preconception acute high-fat diet to dissect epididymal versus testicular contributions to the sperm sncRNA pool and offspring health. We show that epididymal spermatozoa, but not developing germ cells, are sensitive to the environment and identify mitochondrial tRNAs (mt-tRNAs) and their fragments (mt-tsRNAs) as sperm-borne factors. In humans, mt-tsRNAs in spermatozoa correlate with body mass index, and paternal overweight at conception doubles offspring obesity risk and compromises metabolic health. Sperm sncRNA sequencing of mice mutant for genes involved in mitochondrial function, and metabolic phenotyping of their wild-type offspring, suggest that the upregulation of mt-tsRNAs is downstream of mitochondrial dysfunction. Single-embryo transcriptomics of genetically hybrid two-cell embryos demonstrated sperm-to-oocyte transfer of mt-tRNAs at fertilization and suggested their involvement in the control of early-embryo transcription. Our study supports the importance of paternal health at conception for offspring metabolism, shows that mt-tRNAs are diet-induced and sperm-borne and demonstrates, in a physiological setting, father-to-offspring transfer of sperm mitochondrial RNAs at fertilization.

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“…Nevertheless, the roles of histone and inheritance in living organisms is well chronicled, and the reader is invited to consider several excellent reviews that cover the topic extensively [ 34 , 35 , 36 , 37 , 38 , 39 , 40 ]. DNA methylation is an epigenetic footprint and the topic of its heritability has been covered elsewhere [ 41 , 42 , 43 ]. The biogenesis of small interfering RNAs (siRNAs), Piwi-interacting RNAs (piRNAs), and microRNAs (miRNAs) has been discussed in detail elsewhere (see [ 44 ]); thus, here, we present only a brief overview of the biogenesis and functions of different small RNA classes that have been implicated in epigenetic inheritance.…”

Section: Biogenesis and Functions Of Sncrnasmentioning

confidence: 99%

Inheritance of Stress Responses via Small Non-Coding RNAs in Invertebrates and Mammals

Ow,

Hall

2023

Epigenomes

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While reports on the generational inheritance of a parental response to stress have been widely reported in animals, the molecular mechanisms behind this phenomenon have only recently emerged. The booming interest in epigenetic inheritance has been facilitated in part by the discovery that small non-coding RNAs are one of its principal conduits. Discovered 30 years ago in the Caenorhabditis elegans nematode, these small molecules have since cemented their critical roles in regulating virtually all aspects of eukaryotic development. Here, we provide an overview on the current understanding of epigenetic inheritance in animals, including mice and C. elegans, as it pertains to stresses such as temperature, nutritional, and pathogenic encounters. We focus on C. elegans to address the mechanistic complexity of how small RNAs target their cohort mRNAs to effect gene expression and how they govern the propagation or termination of generational perdurance in epigenetic inheritance. Presently, while a great amount has been learned regarding the heritability of gene expression states, many more questions remain unanswered and warrant further investigation.

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Inheritance of paternal lifestyles and exposures through sperm DNA methylation

Cited by 16 publications

References 203 publications

Cryopreservation of Human Spermatozoa: Functional, Molecular and Clinical Aspects

Cryopreservation of Human Spermatozoa: Functional, Molecular and Clinical Aspects

Epigenetic inheritance of diet-induced and sperm-borne mitochondrial RNAs

Inheritance of Stress Responses via Small Non-Coding RNAs in Invertebrates and Mammals

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