Behavioural traits propagate across generations via segregated iterative-somatic and gametic epigenetic mechanisms

Parental behavioural traits can be transmitted by non-genetic mechanisms to the offspring. Although trait transmission via sperm has been extensively researched, epidemiological studies indicate the exclusive/prominent maternal transmission of many non-genetic traits. Since maternal conditions impac...

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Bibliographic Details
Published in:	Nature communications Vol. 7; no. 1; pp. 11492 - 16
Main Authors:	Mitchell, Emma, Klein, Shifra L., Argyropoulos, Kimon V., Sharma, Ali, Chan, Robin B., Toth, Judit Gal, Barboza, Luendreo, Bavley, Charlotte, Bortolozzi, Analia, Chen, Qiuying, Liu, Bingfang, Ingenito, Joanne, Mark, Willie, Dudakov, Jarrod, Gross, Steven, Di Paolo, Gilbert, Artigas, Francesc, van den Brink, Marcel, Toth, Miklos
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 13-05-2016 Nature Publishing Group Nature Portfolio
Subjects:	38/22 38/23 38/39 38/91 631/208/1515 631/208/729 631/378/2584/2585 64/60 692/308 8-Hydroxy-2-(di-n-propylamino)tetralin - pharmacology 82/58 82/80 Alzheimer's disease Animals Anxiety Anxiety - genetics Anxiety - psychology Behavior Behavior, Animal - physiology Comorbidity Disease Models, Animal DNA methylation DNA Methylation - genetics Epigenesis, Genetic Epigenetics Female Gametogenesis - physiology Genomic Imprinting - physiology Genotype & phenotype Germ Cells - physiology Humanities and Social Sciences Hypothermia - chemically induced Hypothermia - genetics Hypothermia - psychology Male Maternal Inheritance - physiology Metabolomics - methods Mice Mice, Knockout Models, Animal multidisciplinary Mutation Penetrance Phenotype Propagation Receptor, Serotonin, 5-HT1A - genetics Receptor, Serotonin, 5-HT1A - metabolism Science Science (multidisciplinary) Serotonin Receptor Agonists - pharmacology Sperm Stress Stress, Psychological - genetics Stress, Psychological - psychology New York United States > US Spain
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Summary:	Parental behavioural traits can be transmitted by non-genetic mechanisms to the offspring. Although trait transmission via sperm has been extensively researched, epidemiological studies indicate the exclusive/prominent maternal transmission of many non-genetic traits. Since maternal conditions impact the offspring during gametogenesis and through fetal/early-postnatal life, the resultant phenotype is likely the aggregate of consecutive germline and somatic effects; a concept that has not been previously studied. Here, we dissected a complex maternally transmitted phenotype, reminiscent of comorbid generalized anxiety/depression, to elementary behaviours/domains and their transmission mechanisms in mice. We show that four anxiety/stress-reactive traits are transmitted via independent iterative-somatic and gametic epigenetic mechanisms across multiple generations. Somatic/gametic transmission alters DNA methylation at enhancers within synaptic genes whose functions can be linked to the behavioural traits. Traits have generation-dependent penetrance and sex specificity resulting in pleiotropy. A transmission-pathway-based concept can refine current inheritance models of psychiatric diseases and facilitate the development of better animal models and new therapeutic approaches. Physiological effects of psychological stress and infection in mothers can increase the incidence of anxiety and psychiatric diseases in offsprings and in subsequent generation. Here, Miklos Toth and colleagues show that intergenerational inheritance of neurological traits is propagated across multiple generations independently by parallel non-genetic mechanisms involving independent segregation of epigenetic specific loci.
ISSN:	2041-1723 2041-1723
DOI:	10.1038/ncomms11492