Cited by 45Gut microbiota and healthBirth, Development, and HealthMetabolomics and Mass Spectrometry Studies

Microbiota signatures relating to reduced memory and exploratory behaviour in the offspring of overweight mothers in a murine model

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Sanguinetti, Elena, Guzzardi, Maria Angela, Tripodi, Maria, Panetta, Daniele, Selma-Royo, Marta, Zega, Alessandro, Telleschi, Mauro, Collado, Maria Carmen +1 more·2019·Scientific Reports

Abstract

An elevated number of women of reproductive age are overweight, predisposing their offspring to metabolic and neuropsychiatric disorders. Gut microbiota is influenced by maternal factors, and has been implicated in the pathogenesis of neurodegenerative diseases. Our aim was to explore the effects of maternal high-fat feeding on the relationship linking gut microbiota and cognitive development in the offspring. Murine offspring born to dams undergoing normal diet (NDm) and high-fat diet (HFDm) were studied at 1 or 6 months of age to assess cognitive function by Y-maze test, cerebral glucose metabolism and insulin sensitivity by Positron Emission Tomography, brain density by Computed Tomography, microbiota profile (colon, caecum) and inferred metabolic pathways (KEGG analysis) by 16S ribosomal RNA sequencing. From 3 weeks post-weaning, mice born to HFDm developed hyperphagia and overweight, showing reduction in memory and exploratory behaviour, and brain insulin resistance in adulthood. We identified a panel of bacteria characterizing offspring born to HFD dams from early life, and correlating with dysfunction in memory and exploratory behaviour in adults (including Proteobacteria phylum, Parabacteroides and unclassified Rikenellaceae genera). Microbiota-derived metabolic pathways involved in fatty acid, essential aminoacid and vitamin processing, sulphur metabolism, glutaminergic activation and Alzheimer's disease were differently present in the HFDm and NDm offspring groups. Our results document tight relationships between gut dysbiosis and memory and behavioural impairment in relation to maternal HFD. Persistent bacterial signatures induced by maternal HFD during infancy can influence cognition during adulthood, opening the possibility of microbiota-targeted strategies to contrast cognitive decline.

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  • Evidence from animal models suggests that the gut microbiota could be an underlying factor linking maternal diet to neurodevelopment.

    “In recent years, evidence from animal models suggests that the gut microbiota could be an underlying factor linking maternal diet to neurodevelopment (244-246).”
  • Investigations into the effect of high-fat or Western diets revealed that some diet-induced shifts in the microbial profile mediated behavioral and cognitive impairments in the offspring.

    “Investigations into the effect of high-fat or Western diets revealed that some dietinduced shifts in the microbial profile mediated behavioral and cognitive impairments in the offspring (244-246),”

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Authors
Sanguinetti, E., Guzzardi, M. A., Tripodi, M., Panetta, D., Selma-Royo, M., Zega, A., Telleschi, M., Collado, M. C., & Iozzo, P.
Affiliations
  • Scuola Superiore Sant'Anna (IT)
  • Istituto di Fisiologia Clinica (IT)
Corresponding author
Iozzo, Patricia
Venue
Scientific Reports
Published
2019-08-30
Volume
9
Issue
1
Pages
12609-12609
ISSN
2045-2322 (ISSN-L)
OpenAlex
W2971014020
Cited by
45
References
76
Citations by year
2026: 2 · 2025: 5 · 2024: 2 · 2023: 5 · 2022: 10 · 2021: 11 · 2020: 8 · 2019: 1
FWCI
2.48
Type
journal article
Language
en
Open access
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Horizon 2020 Framework Programme
  • FP7 Health (278603)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
Keywords
maternal high-fat diet, gut microbiota, offspring cognitive function, memory impairment, exploratory behavior, hyperphagia, brain insulin resistance, brain glucose metabolism, gut dysbiosis, Parabacteroides, Rikenellaceae, Proteobacteria, Alzheimer's disease, sulfur metabolism, maternal obesity, brain development
MeSH terms
Gastrointestinal Microbiome, Animals, Cognition, Disease Models, Animal, Exploratory Behavior, Female, Humans, Insulin Resistance, Memory, Mother-Child Relations, Obesity, Pregnancy, Prenatal Exposure Delayed Effects, Maternal Nutritional Physiological Phenomena, Overweight, Mice, Diet, High-Fat

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