Grandmaternal smoking during pregnancy is associated with differential DNA methylation in their grandchildren

Sh, Watkins; Iles-Caven, Yasmin; Pembrey, Marcus; Golding, Jean; Suderman, Matthew

doi:10.1101/2021.04.22.440892

Cited by 4 publications

(5 citation statements)

References 39 publications

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“…This study shows a similar association with the PGM smoking by demonstrating a reduced chance of the granddaughter having a religious belief. This accumulating evidence of smoking by a grandmother in pregnancy being associated with a sex-specific outcome is now complemented by results of DNA methylation in the maturing grandchild (age [15][16][17] that indicate different associations depending on the type of grandmother, and the sex of the grandchild [18].…”

Section: Putting the Results In Contextmentioning

confidence: 96%

“…We have shown that the changes associated with potential epigenetic environmental exposures such as grandmother smoking in pregnancy are associated with changes in DNA methylation levels at specific CpG sites, including on the X chromosome of the grandchild [18]. There is also abundant evidence from experimental studies that traumatic events can have effects on the DNA methylome for several generations [e.g.…”

Section: Biomarkers Supporting the Epigenetic Consequences Of Smoking And Traumatic Exposuresmentioning

confidence: 99%

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Grandparents childhood exposures and religious belief in their granddaughters: possible transgenerational associations

Golding¹,

Gregory²,

Northstone³

et al. 2021

Preprint

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The prevalence of religious belief has fallen dramatically. A possible reason is that environmental exposures to previous generations are involved, e.g., evidence of an association between childhood exposures of grandparents and outcomes in their grandchildren including obesity, autistic traits, and survival have been reported. Generally, the associations between the grandparent’s exposure and grandchild’s outcome varied with sex of grandparent, his/her age at exposure and sex of the grandchild.Using data collected by the Avon Longitudinal Study of Parents and Children (ALSPAC) we investigate whether exposures such as smoking and/or traumatic events experienced by any of the grandparents are associated with the likelihood that their adult grandchildren have a religious belief. We show that the granddaughters (but not the grandsons) were more likely to have reported such a belief if one of their maternal grandparents had experienced traumatic events pre-puberty (age 6-11), or their paternal grandmother had experienced such events in adolescence. Conversely if their maternal grandfather had started smoking regularly during childhood or their paternal grandmother had smoked prenatally, the granddaughter was substantially less likely to be a believer. These associations were mutually independent and not explained by demographic factors. They may account for a small proportion of the fall in prevalence of religious belief over time, but the association needs confirming in other studies.

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Section: Putting the Results In Contextmentioning

confidence: 96%

Section: Biomarkers Supporting the Epigenetic Consequences Of Smoking And Traumatic Exposuresmentioning

confidence: 99%

Grandparents childhood exposures and religious belief in their granddaughters: possible transgenerational associations

Golding¹,

Gregory²,

Northstone³

et al. 2021

Preprint

Self Cite

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show abstract

“…This raises the possibility that an epigenetic effect involving the X chromosome may be involved. Intriguingly, it has recently been shown that the smoking of the paternal grandmother is, as predicted, associated with differences in DNA methylation at CpG sites on the X chromosome of the granddaughter but not the grandson [ 7 ].…”

Section: Discussionmentioning

confidence: 93%

“…Thus, there is evidence of sex-specific transgenerational associations in grandchildren when the paternal grandmother has smoked in pregnancy. In parallel-specific DNA, methylation changes have been shown in granddaughters (but not grandsons), whose paternal grandmothers smoked in pregnancy [ 7 ]; in early-onset myopia, these changes were particularly linked to genes known to be associated with myopia, thus indicating possible biological plausibility for the myopia association [ 3 ].…”

Section: Introductionmentioning

confidence: 99%

Paternal grandmother’s smoking in pregnancy is associated with extreme aversion to bitter taste in their grandchildren

Golding

Pembrey

Gregory

et al. 2022

Environmental Epigenetics

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Although there are many examples in the experimental literature of an environmental exposure in one generation impacting on the phenotypes of subsequent generations, there are few studies that can assess whether such associations occur in humans. The Avon Longitudinal Study of Parents and Children (ALSPAC) has, however, been able to determine whether there are associations between grandparental exposures and their grandchildren’s development. Several of our studies, including sensitivity to loud noise, have shown associations between a grandmother smoking in pregnancy and the phenotype of the grandchild. These results were mostly specific to the sex of the grandchild, and to whether the prenatal (i.e. during pregnancy) smoking occurred in the maternal or paternal grandmother. Here we have used ancestral data on prenatal smoking among the grandmothers of the ALSPAC index children to examine possible effects on the grandchild’s ability to detect the bitter taste of PROP (6-n-propylthiouracil), distinguishing between the 10% deemed ‘extreme tasters’ and the rest of the population (total n = 4656 children). We showed that grandchildren whose paternal (but not maternal) grandmothers had smoked in pregnancy were more likely than those of non-smoking grandmothers to be extreme tasters [OR 1.28; 95%CI 1.03, 1.59], and that this was more likely in granddaughters [OR 1.42; 95%CI 1.03, 1.95] than grandsons [OR 1.18; 95%CI 0.88, 1.60]. This pattern of association between paternal fetal exposure and the granddaughter’s development has been found with several other outcomes, suggesting that investigations should be undertaken to investigate possible mechanisms.

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“…Similar intergenerational findings are often thought to be due to epigenetic effects, with DNA methylation being the mechanism most often quoted. Elsewhere, using blood samples from these F3 grandchildren, Watkins et al (2022) have identified different methylation markers associated with smoking in pregnancy of the F1 maternal as well as the F1 paternal grandmothers. However, it is premature to speculate further on possible mechanisms for our findings until confirmatory evidence is available from other cohorts.…”

Section: Discussionmentioning

confidence: 99%

A history of asthma may be associated with grandparents’ exposures to stress and cigarette smoking

Golding,

Tunstall,

Gregory

et al. 2023

Front. Toxicol.

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Introduction: Within human epidemiological studies, associations have been demonstrated between grandparental exposures during childhood and grandchildren’s outcomes. A few studies have assessed whether asthma has ancestral associations with exposure to cigarette smoking, but results have been mixed so far.Material and methods: In this study we used four generations: (F0 great-grandparents, F1 grandparents, F2 parents, F3 study children) of the Avon Longitudinal Study of Parents and Children (ALSPAC) to determine whether there is evidence of associations between asthma in generations F2 or F3 and exposures to severe trauma in childhood and/or active cigarette smoking during the adolescence of grandmothers and grandfathers in generations F0 and F1 respectively, or of a history of a F0 or F1 grandmother smoking during pregnancy.Results: We have shown that: a) stress exemplified by the death of a F1 grandparent’s parent during the grandparents’ childhood was associated with increased risk of asthma in generation F3, especially if the grandparent involved was the paternal grandmother; b) if the grandparents of generations F0 or F1 smoked during adolescence (i.e. < 17 years), their grandchildren in generations F2 and F3 were more likely to have a history of asthma; c) paternal F1 grandmother’s smoking in pregnancy was associated with her F3 grandchild’s asthma at age 7; d) There were differences between the results for the grandsons and granddaughters of the paternal grandmother with exposure to smoking in adolescence and with smoking in pregnancy. e) The addition of all of the individual exposure variables to the different analyses often provided a considerable increase in goodness of fit compared with only adding demographic factors associated with asthma at P < 0.10 such as social class; this was particularly true when all four exposure variables were combined in one model, suggesting possible synergistic effects between them.Discussion: We have shown associations between all four types of exposure to the grandparents to be associated with asthma in the grandchildren, such that the results both depended on whether the male or female line was involved, and the sex of the grandchildren. It was notable that the paternal grandmother was particularly involved in many of the associations. We emphasize that these are exploratory analyses, that asthma diagnostic criteria likely changed over time and may not be consistent between generations, and that the results should be tested in other cohorts.

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Grandmaternal smoking during pregnancy is associated with differential DNA methylation in their grandchildren

Cited by 4 publications

References 39 publications

Grandparents childhood exposures and religious belief in their granddaughters: possible transgenerational associations

Grandparents childhood exposures and religious belief in their granddaughters: possible transgenerational associations

Paternal grandmother’s smoking in pregnancy is associated with extreme aversion to bitter taste in their grandchildren

A history of asthma may be associated with grandparents’ exposures to stress and cigarette smoking

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