Early-life experiences and the development of adult diseases with a focus on mental illness: The Human Birth Theory

Maccari, Stefania; Polese, Daniela; Reynaert, Marie-Line; Amici, Tiziana; Morley‐Fletcher, Sara; Fagioli, Francesca

doi:10.1016/j.neuroscience.2016.05.042

Cited by 77 publications

(75 citation statements)

References 161 publications

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“…Many studies show the critical importance of the postnatal period for individual development because stress in this period can have delayed effects on cognition, individual behavior, neuronal plasticity and epigenetics . Nevertheless, the mouse and rat studies on MS and HD effects on cognition in adult females are limited.…”

Section: Discussionmentioning

confidence: 99%

Stress early in life leads to cognitive impairments, reduced numbers of CA3 neurons and altered maternal behavior in adult female mice

Reshetnikov

Ковнер

Lepeshko

et al. 2018

Genes Brain and Behavior

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The hippocampus is a crucial part of the limbic system involved both in cognitive processing and in the regulation of responses to stress. Adverse experiences early in life can disrupt hippocampal development and lead to impairment of the hypothalamic‐pituitary‐adrenal axis response to subsequent stressors. In our study, two types of early‐life stress were used: prolonged separation of pups from their mothers (for 3 hours/day, maternal separation, MS) and brief separation (for 15 minutes/day, handling, HD). In the first part of our study, we found that adult female mice (F0) who had experienced MS showed reduced locomotor activity and impairment of long‐term spatial and recognition memory. Analysis of various hippocampal regions showed that MS reduced the number of mature neurons in CA3 of females, which is perhaps a crucial hippocampal region for learning and memory; however, neurogenesis remained unchanged. In the second part, we measured maternal care in female mice with a history of early‐life stress (F0) as well as the behavior of their adult offspring (F1). Our results indicated that MS reduced the level of maternal care in adult females (F0) toward their own progeny and caused sex‐specific changes in the social behavior of adult offspring (F1). In contrast to MS, HD had no influence on female behavior or hippocampal plasticity. Overall, our results suggest that prolonged MS early in life affects the adult behavior of F0 female mice and hippocampal neuronal plasticity, whereas the mothers' previous experience has effects on the behavior of their F1 offspring through disturbances of mother‐infant interactions.

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Section: Discussionmentioning

confidence: 99%

Stress early in life leads to cognitive impairments, reduced numbers of CA3 neurons and altered maternal behavior in adult female mice

Reshetnikov

Ковнер

Lepeshko

et al. 2018

Genes Brain and Behavior

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“…Alterations in environmentally sensitive epigenetic modifications are emerging as important factors in the long-term biological trajectories leading to stress-related psychiatric disorders (Hunter et al, 2009; Maccari et al, 2016). DNA methylation (5-methylcytosine (5mC)) is an epigenetic modification with important roles in chromatin remolding, gene silencing, embryonic development, cellular differentiation, and the maintenance of cellular identity (Chouliaras et al, 2013; Mellen et al, 2012; Tollervey and Lunyak, 2012).…”

Section: Introductionmentioning

confidence: 99%

Sex-specific hippocampal 5-hydroxymethylcytosine is disrupted in response to acute stress

Papale

Madrid

et al. 2016

Neurobiology of Disease

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Environmental stress is among the most important contributors to increased susceptibility to develop psychiatric disorders. While it is well known that acute environmental stress alters gene expression, the molecular mechanisms underlying these changes remain largely unknown. 5-hydroxymethylcytosine (5hmC) is a novel environmentally sensitive epigenetic modification that is highly enriched in neurons and is associated with active neuronal transcription. Recently, we reported a genome-wide disruption of hippocampal 5hmC in male mice following acute stress that was correlated to altered transcript levels of genes in known stress related pathways. Since sex-specific endocrine mechanisms respond to environmental stimulus by altering the neuronal epigenome, we examined the genome-wide profile of hippocampal 5hmC in female mice following exposure to acute stress and identified 363 differentially hydroxymethylated regions (DhMRs) linked to known (e.g., Nr3c1 and Ntrk2) and potentially novel genes associated with stress response and psychiatric disorders. Integration of hippocampal expression data from the same female mice found stress-related hydroxymethylation correlated to altered transcript levels. Finally, characterization of stress-induced sex-specific 5hmC profiles in the hippocampus revealed 778 sex-specific acute stress-induced DhMRs some of which were correlated to altered transcript levels that produce sex-specific isoforms in response to stress. Together, the alterations in 5hmC presented here provide a possible molecular mechanism for the adaptive sex-specific response to stress that may augment the design of novel therapeutic agents that will have optimal effectiveness in each sex.

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“…[2; 3; 223] Stress or adversity during different developmental stages can produce different neuroanatomical and behavioral consequences. [2] In addition, ELS at different ages can influence the risk of subsequent medical conditions, such as cardiovascular disease, [120] gastrointestinal disorders, [157; 217] and chronic pain. [27; 149] ii) severity of ELS.…”

Section: Contributing Factorsmentioning

confidence: 99%

“…[3] Throughout this manuscript biological dichotomous 'sex' differences will be referred to, rather than the more psychosocially based continuous variable of gender. [73] Although often not specifically assessed, [188] sex-dependent differences are relevant to the presentation and severity of a number of diseases associated with ELS, including mental health and mood disorders, [2] cardiovascular disease, [120] and visceral pain. [157] vii) variable patterns of hyper-and/or hypo-activity.…”

Section: Contributing Factorsmentioning

confidence: 99%

Translational studies identify long-term impact of prior neonatal pain experience

Walker

2017

PAIN

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Early-life experiences and the development of adult diseases with a focus on mental illness: The Human Birth Theory

Cited by 77 publications

References 161 publications

Stress early in life leads to cognitive impairments, reduced numbers of CA3 neurons and altered maternal behavior in adult female mice

Stress early in life leads to cognitive impairments, reduced numbers of CA3 neurons and altered maternal behavior in adult female mice

Sex-specific hippocampal 5-hydroxymethylcytosine is disrupted in response to acute stress

Translational studies identify long-term impact of prior neonatal pain experience

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