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Sex-specificities in offspring neurodevelopment and behaviour upon maternal glycation: Putative underlying
Andreia Amaro1, Diana Sousa1, Mariana Sá-Rocha1
1Coimbra Institute for Clinical and Biomedical Research (iCBR), Faculty of Medicine, University of Coimbra, Portugal; Center for Innovative Biomedicine and Biotechnology (CIBB), University of Coimbra, Portugal; Clinical-Academic Center of Coimbra (CACC), Coimbra, Portugal.
Insights
Maternal glycation during lactation alters milk composition, impacting offspring neurodevelopment and leading to sex-specific behavioral changes in adolescence. This highlights lactation as a critical window for metabolic programming and behavior development.
Area of Science:
- Neuroscience
- Developmental Biology
- Metabolic Disease
Background:
- Lactation is a critical period for programming offspring health, influencing long-term metabolic and neuronal outcomes.
- Maternal metabolic health, including glycation, can impact offspring development.
- Understanding sex-specific effects is crucial for targeted interventions.
Purpose of the Study:
- To investigate the impact of maternal glycation during lactation on offspring neurodevelopment and behavior.
- To identify sex differences in the neurodevelopmental and behavioral effects of maternal glycation.
- To explore the molecular mechanisms underlying these changes.
Main Methods:
- Female Wistar rats were administered a Glyoxalase-1 inhibitor (BBGC) or vehicle during lactation.
- Offspring neurodevelopment, behavior (locomotor activity, anxiety, memory), and metabolic parameters were assessed at different life stages.
- Breast milk composition, and hippocampus and prefrontal cortex molecular markers (GABAA, PSD-95, GLO1, AGES) were analyzed.
Main Results:
- Maternal glycation reduced milk triglycerides and antioxidant capacity.
- Offspring showed accelerated neurodevelopmental milestones in infancy.
- Adolescent offspring exhibited sex-specific behavioral alterations, including hyperlocomotion in males and risk-taking in both sexes.
- Increased GABAA receptor levels were observed in the hippocampus of both sexes, with additional changes in the prefrontal cortex of females.
- Reduced GLO1 and increased AGES accumulation occurred in the hippocampus of offspring.
Conclusions:
- Early exposure to maternal glycation during lactation induces significant changes in milk composition.
- These changes lead to neurodevelopmental alterations in infancy and sex-specific behavioral and neurometabolic consequences in adolescence.
- The study reinforces the lactation period as a critical window for metabolic programming and behavioral sculpting, with notable sex differences.
Aim:
Lactation is an important programming window for metabolic disease and neuronal alterations later in life. We aimed to study the effect of maternal glycation during lactation on offspring neurodevelopment and behaviour, assessing possible sex differences and underpinning molecular players.
Methods:
Female Wistar rats were treated with Glyoxalase-1 inhibitor S-p-Bromobenzylguthione cyclopentyl diester (BBGC 5 mg/kg). A control and vehicle group treated with dimethyl sulfoxide were also considered. Male and female offspring were tested at infancy for neurodevelopment hallmarks. After weaning, triglycerides and total antioxidant capacity were measured in breast milk. At adolescence, offspring were tested for locomotor ability, anxious-like behaviour, and recognition memory. Metabolic parameters were assessed, and the hippocampus and prefrontal cortex were collected for molecular analysis.
Key Findings:
Maternal glycation reduced triglycerides and total antioxidant capacity levels in breast milk. At infancy, both male and female offspring presented an anticipation on the achievement of neurodevelopmental milestones. At adolescence, male offspring exposed to maternal glycation presented hyperlocomotion, whereas offspring of both sexes presented a risk-taking phenotype, accompanied by increase GABAA receptor levels in the hippocampus. Females also demonstrated GABAA and PSD-95 changes in prefrontal cortex. Furthermore, lower levels of GLO1 and consequently higher accumulation of AGES were also observed in both male and female offspring hippocampus.
Significance:
Early exposure to maternal glycation induces changes in milk composition leading to neurodevelopment changes at infancy, and sex-specific behavioural and neurometabolic changes at adolescence, further evidencing that lactation period is a critical metabolic programming window and in sculpting behaviour.
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