Epigenetics and the origins of paternal effects.
TL;DR: This review will explore the potential role of paternally induced maternal investment, highlight the literature illustrating the transgenerational impact of paternal experiences, and discuss the evidence supporting the role of epigenetic mechanisms in maintaining paternal effects both within and across generations.
About: This article is published in Hormones and Behavior.The article was published on 2011-03-01 and is currently open access. It has received 356 citations till now. The article focuses on the topics: Paternal Exposure.
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TL;DR: It is demonstrated that paternal experience across the lifespan can induce germ cell epigenetic reprogramming and impact offspring HPA stress axis regulation, and may therefore offer novel insight into factors influencing neuropsychiatric disease risk.
Abstract: Neuropsychiatric disease frequently presents with an underlying hyporeactivity or hyperreactivity of the HPA stress axis, suggesting an exceptional vulnerability of this circuitry to external perturbations Parental lifetime exposures to environmental challenges are associated with increased offspring neuropsychiatric disease risk, and likely contribute to stress dysregulation While maternal influences have been extensively examined, much less is known regarding the specific role of paternal factors To investigate the potential mechanisms by which paternal stress may contribute to offspring hypothalamic-pituitary-adrenal (HPA) axis dysregulation, we exposed mice to 6 weeks of chronic stress before breeding As epidemiological studies support variation in paternal germ cell susceptibility to reprogramming across the lifespan, male stress exposure occurred either throughout puberty or in adulthood Remarkably, offspring of sires from both paternal stress groups displayed significantly reduced HPA stress axis responsivity Gene set enrichment analyses in offspring stress regulating brain regions, the paraventricular nucleus (PVN) and the bed nucleus of stria terminalis, revealed global pattern changes in transcription suggestive of epigenetic reprogramming and consistent with altered offspring stress responsivity, including increased expression of glucocorticoid-responsive genes in the PVN In examining potential epigenetic mechanisms of germ cell transmission, we found robust changes in sperm microRNA (miR) content, where nine specific miRs were significantly increased in both paternal stress groups Overall, these results demonstrate that paternal experience across the lifespan can induce germ cell epigenetic reprogramming and impact offspring HPA stress axis regulation, and may therefore offer novel insight into factors influencing neuropsychiatric disease risk
657 citations
TL;DR: The findings discussed indicate that identification of environmental chemicals that dysregulate the prenatal epigenome should be a priority in health research and disease prevention.
514 citations
Cites background from "Epigenetics and the origins of pate..."
...However, recent evidence suggests that paternal factors (nutritional, toxicological, age, and phenotypic variation) can affect offspring and in some cases grandoffspring [43]....
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TL;DR: In this paper, the authors propose a method for measuring the performance of a single node in a set of images.ING and INDEXING, e.g., this paper.
406 citations
TL;DR: The moderation of paternal PTSD effects by maternal PTSD suggests different mechanisms for the intergenerational transmission of trauma-related vulnerabilities.
Abstract: Important differences in the expression and effect of maternal and paternal PTSD were found when examining parental PTSD in the offspring of Holocaust survivors and methylation of the glucocorticoid receptor gene exon 1F.
390 citations
Additional excerpts
..., paternally driven maternal effects) (40)....
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TL;DR: The methylomes of human and chimp sperm revealed a subset of differentially methylated promoters and strikingly divergent methylation in retrotransposon subfamilies, with an evolutionary impact that is apparent in the underlying genomic sequence.
373 citations
Cites background from "Epigenetics and the origins of pate..."
...There has been much discussion regarding the role of germline transmission of epigenetic marks in interindividual variation (Curley et al., 2011)....
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References
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Book•
01 Jan 1991
TL;DR: This paper examined the evolution of variation in egg and neonate size, of viviparity and other forms of bearing, and of differences in the duration of incubation, gestation, and lactation.
Abstract: Synthesizing studies of parental care in a wide variety of animals, this book is the first attempt to provide general answers to the following important questions: Why does the extent of parental care vary so widely between species? Why do only females care for eggs and young in some animals, only males in others, and both parents in a few? To what extent is parental care adjusted to variation in its benefits to offspring and its costs to parents? How do parents divide their resources between their sons and daughters? In this book separate chapters examine the evolution of variation in egg and neonate size, of viviparity and other forms of bearing, and of differences in the duration of incubation, gestation, and lactation. The book reviews theoretical and empirical predictions concerning the evolution of parental care and examines the extent to which these are supported by empirical evidence. The author examines the distribution of parental care among offspring, reviews the empirical evidence that parents invest to different extents in their sons and daughters, and discusses the degree to which parents manipulate the sex ratio of their progeny in relation to the availability of resources.
3,341 citations
TL;DR: Older monozygous twins exhibited remarkable differences in their overall content and genomic distribution of 5-methylcytosine DNA and histone acetylation, affecting their gene-expression portrait, indicating how an appreciation of epigenetics is missing from the understanding of how different phenotypes can be originated from the same genotype.
Abstract: Monozygous twins share a common genotype. However, most monozygotic twin pairs are not identical; several types of phenotypic discordance may be observed, such as differences in susceptibilities to disease and a wide range of anthropomorphic features. There are several possible explanations for these observations, but one is the existence of epigenetic differences. To address this issue, we examined the global and locus-specific differences in DNA methylation and histone acetylation of a large cohort of monozygotic twins. We found that, although twins are epigenetically indistinguishable during the early years of life, older monozygous twins exhibited remarkable differences in their overall content and genomic distribution of 5-methylcytosine DNA and histone acetylation, affecting their gene-expression portrait. These findings indicate how an appreciation of epigenetics is missing from our understanding of how different phenotypes can be originated from the same genotype.
3,330 citations
"Epigenetics and the origins of pate..." refers background in this paper
...DNA methylation changes can also accumulate with increasing paternal age in multiple tissues including the gametes (Flanagan et al., 2006; Fraga et al., 2005; Oakes et al., 2003)....
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TL;DR: The ability of an environmental factor to reprogram the germ line and to promote a transgenerational disease state has significant implications for evolutionary biology and disease etiology.
Abstract: Transgenerational effects of environmental toxins require either a chromosomal or epigenetic alteration in the germ line. Transient exposure of a gestating female rat during the period of gonadal sex determination to the endocrine disruptors vinclozolin (an antiandrogenic compound) or methoxychlor (an estrogenic compound) induced an adult phenotype in the F1 generation of decreased spermatogenic capacity (cell number and viability) and increased incidence of male infertility. These effects were transferred through the male germ line to nearly all males of all subsequent generations examined (that is, F1 to F4). The effects on reproduction correlate with altered DNA methylation patterns in the germ line. The ability of an environmental factor (for example, endocrine disruptor) to reprogram the germ line and to promote a transgenerational disease state has significant implications for evolutionary biology and disease etiology.
2,280 citations
TL;DR: The analysis of data shows that epigenetic inheritance is ubiquitous and suggests lines of research that go beyond present approaches to the subject, as well as pointing to the importance of recognizing and understanding epigenetics for practical and theoretical issues in biology.
Abstract: This review describes new developments in the study of transgenerational epigenetic inheritance, a component of epigenetics. We start by examining the basic concepts of the field and the mechanisms that underlie epigenetic inheritance. We present a comprehensive review of transgenerational cellular epigenetic inheritance among different taxa in the form of a table, and discuss the data contained therein. The analysis of these data shows that epigenetic inheritance is ubiquitous and suggests lines of research that go beyond present approaches to the subject. We conclude by exploring some of the consequences of epigenetic inheritance for the study of evolution, while also pointing to the importance of recognizing and understanding epigenetic inheritance for practical and theoretical issues in biology.
1,423 citations
"Epigenetics and the origins of pate..." refers background in this paper
...Further, depending on where these mutations occur, it is possible to influence the epigenetic structure of specific genes or of the entire genome (particularly if genes coding for epigenetic machinery are affected) (Jablonka and Raz, 2009; Mohn and Schubeler, 2009)....
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...Mutational events or DNA damage has the potential to induce heritable epigenetic marks (Jablonka and Raz, 2009)....
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...Conversely, there is the potential for epigenetic marks (i.e. loose chromatin structure) to increase the probability of mutation, transposition, and/or the recombination of DNA sequences (Jablonka and Lamb, 1995; Jablonka and Raz, 2009)....
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...transposition, and/or the recombination of DNA sequences (Jablonka and Lamb, 1995; Jablonka and Raz, 2009)....
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TL;DR: It is demonstrated here that this maternal epigenetic effect is not the result of a maternally contributed environment, and results from incomplete erasure of an epigenetic modification when a silenced Avy allele is passed through the female germ line, with consequent inheritance of the epigenetic modified.
Abstract: Epigenetic modifications have effects on phenotype, but they are generally considered to be cleared on passage through the germ line in mammals, so that only genetic traits are inherited. Here we describe the inheritance of an epigenetic modification at the agouti locus in mice. In viable yellow ( Avy/a) mice, transcription originating in an intra-cisternal A particle (IAP) retrotransposon inserted upstream of the agouti gene ( A) causes ectopic expression of agouti protein, resulting in yellow fur, obesity, diabetes and increased susceptibility to tumours1. The pleiotropic effects of ectopic agouti expression are presumably due to effects of the paracrine signal on other tissues. Avy mice display variable expressivity because they are epigenetic mosaics for activity of the retrotransposon: isogenic Avy mice have coats that vary in a continuous spectrum from full yellow, through variegated yellow/agouti, to full agouti (pseudoagouti). The distribution of phenotypes among offspring is related to the phenotype of the dam; when an Avy dam has the agouti phenotype, her offspring are more likely to be agouti2,3. We demonstrate here that this maternal epigenetic effect is not the result of a maternally contributed environment. Rather, our data show that it results from incomplete erasure of an epigenetic modification when a silenced Avy allele is passed through the female germ line, with consequent inheritance of the epigenetic modification. Because retrotransposons are abundant in mammalian genomes, this type of inheritance may be common.
1,351 citations
"Epigenetics and the origins of pate..." refers background in this paper
...tion) and environmental toxicants (bisphenol A) and is inherited by offspring via thematernal line (Cropley et al., 2006; Dolinoy et al., 2007; Morgan et al., 1999)....
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...Similarly, the insertion of an IAP element into an exon of the agouti gene (A) results in a number of phenotypic effects; including a range of coat color pigmentations and the propensity to develop obesity (Morgan et al., 1999)....
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...Like in the AxinFu mouse, the epigenetic state of Avy can be modified by environmental factors such as diet (methyl supplementation) and environmental toxicants (bisphenol A) and is inherited by offspring via thematernal line (Cropley et al., 2006; Dolinoy et al., 2007; Morgan et al., 1999)....
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...Similarly, the insertion of an IAP element into an exon of the agouti gene (Avy) results in a number of phenotypic effects; including a range of coat color pigmentations and the propensity to develop obesity (Morgan et al., 1999)....
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