Paternal alcohol consumption has intergenerational consequences in male offspring

Cambiasso, Maite Yael; Gotfryd, Lucila; Stinson, Marcelo Gabriel; Birolo, Sol; Salamone, Gabriela; Romanato, Marina; Calvo, Juan; Fontana, Vanina Andrea

doi:10.1007/s10815-021-02373-0

Cited by 9 publications

(13 citation statements)

References 59 publications

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“…Whether the environment modulates this form of epigenetic information to heritably influence offspring development is still in the initial stages of investigation. However, research reveals that sperm from males exposed to alcohol, a folic acid-deficient diet, and a high-fat diet all display altered amounts of trimethylated histone H3 lysine 4 (H3K4me3) or dimethylated histone H3 lysine 9 (H3K9me2) (Terashima et al, 2015;Claycombe-Larson et al, 2020;Yoshida et al, 2020;Lismer et al, 2021;Bedi et al, 2022b;Cambiasso et al, 2022;Pepin et al, 2022). Inheritance of these changes may directly impact chromatin accessibility in the developing embryo, impacting the earliest transcriptional programs governing lineage specification and developmental patterning.…”

Section: Histone Posttranslational Modificationsmentioning

confidence: 99%

Paternal epigenetic influences on placental health and their impacts on offspring development and disease

Bhadsavle

Golding

2022

Front. Genet.

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Our efforts to understand the developmental origins of birth defects and disease have primarily focused on maternal exposures and intrauterine stressors. Recently, research into non-genomic mechanisms of inheritance has led to the recognition that epigenetic factors carried in sperm also significantly impact the health of future generations. However, although researchers have described a range of potential epigenetic signals transmitted through sperm, we have yet to obtain a mechanistic understanding of how these paternally-inherited factors influence offspring development and modify life-long health. In this endeavor, the emerging influence of the paternal epigenetic program on placental development, patterning, and function may help explain how a diverse range of male exposures induce comparable intergenerational effects on offspring health. During pregnancy, the placenta serves as the dynamic interface between mother and fetus, regulating nutrient, oxygen, and waste exchange and coordinating fetal growth and maturation. Studies examining intrauterine maternal stressors routinely describe alterations in placental growth, histological organization, and glycogen content, which correlate with well-described influences on infant health and adult onset of disease. Significantly, the emergence of similar phenotypes in models examining preconception male exposures indicates that paternal stressors transmit an epigenetic memory to their offspring that also negatively impacts placental function. Like maternal models, paternally programmed placental dysfunction exerts life-long consequences on offspring health, particularly metabolic function. Here, focusing primarily on rodent models, we review the literature and discuss the influences of preconception male health and exposure history on placental growth and patterning. We emphasize the emergence of common placental phenotypes shared between models examining preconception male and intrauterine stressors but note that the direction of change frequently differs between maternal and paternal exposures. We posit that alterations in placental growth, histological organization, and glycogen content broadly serve as reliable markers of altered paternal developmental programming, predicting the emergence of structural and metabolic defects in the offspring. Finally, we suggest the existence of an unrecognized developmental axis between the male germline and the extraembryonic lineages that may have evolved to enhance fetal adaptation.

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Section: Histone Posttranslational Modificationsmentioning

confidence: 99%

Paternal epigenetic influences on placental health and their impacts on offspring development and disease

Bhadsavle

Golding

2022

Front. Genet.

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“…Finally, the role of paternal physical activity and caffeine use in the pre-conception period is almost unexplored in the current literature. However, regular exercise in male mice has shown increased insulin sensitivity in their offspring, due to the different methylation status of glucose metabolism genes of paternal sperm and skeletal muscle [ 108 ].…”

Section: The Father the Fetus And The Future Offspringmentioning

confidence: 99%

The “Bad Father”: Paternal Role in Biology of Pregnancy and in Birth Outcome

Giannubilo,

Marzioni,

Tossetta

et al. 2024

Biology

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Pregnancy is generally studied as a biological interaction between a mother and a fetus; however, the father, with his characteristics, lifestyle, genetics, and living environment, is by no means unrelated to the outcome of pregnancy. The half of the fetal genetic heritage of paternal derivation can be decisive in cases of inherited chromosomal disorders, and can be the result of de novo genetic alterations. In addition to the strictly pathological aspects, paternal genetics may transmit thrombophilic traits that affect the implantation and vascular construction of the feto-placental unit, lead to placenta-mediated diseases such as pre-eclampsia and fetal growth retardation, and contribute to the multifactorial genesis of preterm delivery. Biological aspects of immunological tolerance to paternal antigens also appear to be crucial for these pathologies. Finally, this review describes the biological findings by which the environment, exposure to pathogens, lifestyle, and nutritional style of the father affect fetal pathophysiological and epigenetic definition.

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Section: Effects Of Paternal Lifestyle On Offspringmentioning

confidence: 99%

“…Paternal alcohol exposure (PAE) is found to cause histological and epigenetic changes, as well as damage in DNA integrity in the testicular germline and sperm, which give rise to deleterious effects on embryonic development and to testicular and spermatic changes in the offspring. 93 , 94 , 95 Besides, PAE can induce several developmental aberrations and alters learning and locomotor activity, affective behavior, and sensitivity to the rewarding properties of alcohol in offspring. 12 Notably, the PAE effects are in a sex‐specific manner with a negative impact on offspring neocortical development, causing deficits in activity and sensorimotor integration deficits and decreased balance, coordination, and short‐term motor learning postnatally.…”

Section: Effects Of Paternal Lifestyle On Offspringmentioning

confidence: 99%

Developmental origins of health and disease: Impact of paternal nutrition and lifestyle

Shi

2023

Pediatric Investigation

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Most epidemiological and experimental studies have focused on maternal influences on offspring's health. The impact of maternal undernutrition, overnutrition, hypoxia, and stress is linked to adverse offspring outcomes across a range of systems including cardiometabolic, respiratory, endocrine, and reproduction among others. During the past decade, it has become evident that paternal environmental factors are also linked to the development of diseases in offspring. In this article, we aim to outline the current understanding of the impact of male health and environmental exposure on offspring development, health, and disease and explore the mechanisms underlying the paternal programming of offspring health. The available evidence suggests that poor paternal pre‐conceptional nutrition and lifestyle, and advanced age can increase the risk of negative outcomes in offspring, via both direct (genetic/epigenetic) and indirect (maternal uterine environment) effects. Beginning at preconception, and during utero and the early life after birth, cells acquire an epigenetic memory of the early exposure which can be influential across the entire lifespan and program a child's health. Potentially not only mothers but also fathers should be advised that maintaining a healthy diet and lifestyle is important to improve offspring health as well as the parental health status. However, the evidence is mostly based on animal studies, and well‐designed human studies are urgently needed to verify findings from animal data.

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Paternal alcohol consumption has intergenerational consequences in male offspring

Cited by 9 publications

References 59 publications

Paternal epigenetic influences on placental health and their impacts on offspring development and disease

Paternal epigenetic influences on placental health and their impacts on offspring development and disease

The “Bad Father”: Paternal Role in Biology of Pregnancy and in Birth Outcome

Developmental origins of health and disease: Impact of paternal nutrition and lifestyle

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