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Potential of Environmental Enrichment to Prevent Transgenerational Effects of Paternal Trauma.

ABSTRACT: Adverse experiences in early life are risk factors for the development of behavioral and physiological symptoms that can lead to psychiatric and cognitive disorders later in life. Some of these symptoms can be transmitted to the offspring, in some cases by non-genomic mechanisms involving germ cells. Using a mouse model of unpredictable maternal separation and maternal stress, we show that postnatal trauma alters coping behaviors in adverse conditions in exposed males when adult and in their adult male progeny. The behavioral changes are accompanied by increased glucocorticoid receptor (GR) expression and decreased DNA methylation of the GR promoter in the hippocampus. DNA methylation is also decreased in sperm cells of exposed males when adult. Transgenerational transmission of behavioral symptoms is prevented by paternal environmental enrichment, an effect associated with the reversal of alterations in GR gene expression and DNA methylation in the hippocampus of the male offspring. These findings highlight the influence of both negative and positive environmental factors on behavior across generations and the plasticity of the epigenome across life.

SUBMITTER: Gapp K

PROVIDER: S-EPMC5026744 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Potential of Environmental Enrichment to Prevent Transgenerational Effects of Paternal Trauma.

Gapp Katharina K Bohacek Johannes J Grossmann Jonas J Brunner Andrea M AM Manuella Francesca F Nanni Paolo P Mansuy Isabelle M IM

Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology 20160609 11

Adverse experiences in early life are risk factors for the development of behavioral and physiological symptoms that can lead to psychiatric and cognitive disorders later in life. Some of these symptoms can be transmitted to the offspring, in some cases by non-genomic mechanisms involving germ cells. Using a mouse model of unpredictable maternal separation and maternal stress, we show that postnatal trauma alters coping behaviors in adverse conditions in exposed males when adult and in their adu ...[more]

PMID: 27277118

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Project description:BackgroundEvolutionary studies have reported that non-genetic information can be inherited across generations (epigenetic marks, microbiota, cultural inheritance). Non-genetic information is considered to be a key element to explain the adaptation of wild species to environmental constraints because it lies at the root of the transgenerational transmission of environmental effects. The "transmissibility model" was proposed several years ago to better predict the transmissible potential of each animal by taking these diverse sources of inheritance into account in a global transmissible potential. We propose to improve this model to account for the influence of the environment on the global transmissible potential as well. This extension of the transmissibility model is the "transmissibility model with environment" that considers a covariance between transmissibility samplings of animals sharing the same environment. The null hypothesis of "no transmitted environmental effect" can be tested by comparing the two models using a likelihood ratio test (LRT).ResultsWe performed simulations that mimicked an experimental design consisting of two lines of animals with one exposed to a particular environment at a given generation. This enabled us to evaluate the performances of the transmissibility model with environment so as to detect and quantify transgenerational transmitted environmental effects. The power and the realized type I error of the LRT were compared to those of a T-test comparing the phenotype of the two lines, three generations after the environmental exposure for different sets of parameters. The power of the LRT ranged from 45 to 94%, whereas that of the T-test was always lower than 26%. In addition, the realized type I error of the T-test was 15% and that of the LRT was 5%, as expected. Variances, the covariance between transmissibility samplings, and path coefficients of transmission estimated with the transmissibility model with environment were close to their true values for all sets of parameters.ConclusionsThe transmissibility model with environment is effective in modeling vertical transmission of environmental effects.

Project description:Pre-reproductive environmental enrichment of female rats influences sensorimotor development and spatial behavior of the offspring, possibly through the changed maternal nurturing. Nevertheless, maternal care could be not the solely responsible for changing offspring developmental trajectories. To disentangle the specific contribution to the transgenerational inheritance of pre- and post-natal factors, a cross-fostering study was performed. Female rats were reared in an enriched environment from weaning to sexual maturity, while control female rats were reared under standard conditions. Following mating with standard-reared males, all females were housed individually. Immediately after delivery, in- or cross-fostering manipulations were performed so that any foster dams received pups born to another dam of the same (in-fostering) or the opposite (cross-fostering) pre-reproductive rearing condition. In lactating dams maternal care and nesting activities were assessed, while in their male pups spatial abilities were assessed through Morris Water Maze (MWM) test at post-natal day 45. Moreover, the expression of Brain-Derived-Neurotrophic-Factor (BDNF) was evaluated in the hippocampus and frontal cortex of dams and pups at weaning. Pre-reproductive maternal environmental enrichment, followed by adoption procedures, loosened its potential in modifying maternal care and offspring developmental trajectories, as indicated by the lack of differences between in-fostered groups of dams and pups. In addition, enriched dams rearing standard pups showed the least complex maternal repertoire (the highest sniffing duration and the lowest nest quality), and their pups showed a reduced spatial learning in the MWM. Nevertheless, pre-reproductive maternal enrichment kept influencing neurotrophic pattern, with enriched dams expressing increased frontal BDNF levels (regardless of the kind of fostered pups), and their offspring expressing increased hippocampal BDNF levels. The present findings enlighten the crucial importance of the early mother-pups interactions in influencing maternal care and offspring phenotype, with the enriched dam-standard pups couple resulting in the most maladaptive encounter. Our study thus sustains that the bidirectional interactions between mother and pups are able to deeply shape offspring phenotype.

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Potential of Environmental Enrichment to Prevent Transgenerational Effects of Paternal Trauma.

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Potential of Environmental Enrichment to Prevent Transgenerational Effects of Paternal Trauma.

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