Prenatal and postnatal contributions of the maternal microbiome on offspring programming

• Published in: Frontiers in neuroendocrinology Vol. 55; p. 100797
• Main Authors: Jašarević, Eldin, Bale, Tracy L.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.10.2019
• Subjects: Animals; Brain - growth & development; Brain - immunology; Brain - metabolism; Child Development - physiology; Female; Fetal Development - immunology; Fetal Development - physiology; Gastrointestinal Microbiome - immunology; Humans; Immune; Infant, Newborn; Microbiome; Neurodevelopment; Pregnancy; Prenatal Exposure Delayed Effects - immunology; Prenatal Exposure Delayed Effects - metabolism; Prenatal Exposure Delayed Effects - microbiology; Stress; Vagina - microbiology; Neurodevelopment; Immune; Stress; Microbiome
• ISSN: 0091-3022; 1095-6808
• DOI: 10.1016/j.yfrne.2019.100797

•Maternal gut microbiota and its metabolites influence fetal immune and brain development in a sex-specific manner.•Maternal microbiota is a reservoir for offspring colonization at birth.•Vertical transmission of maternal vaginal and gut microbiota shape postnatal metabolic, immune, and brain development.•Disruption to maternal-to-offspring transmission of microbiota may impact development. The maternal microbiota is positioned to regulate the development of offspring immunity, metabolism, as well as brain function and behavior. The mechanisms by which maternal microbial signals drive these processes are beginning to be elucidated. In this review, we provide a brief overview on the importance of the microbiome in brain function and behavior, define the maternal vaginal and gut microbiota as distinct influences on offspring development, and outline current concepts in microbial origins of offspring health outcomes. We propose that the maternal microbiota influences prenatal and early postnatal offspring development and health outcomes through two overlapping processes. First, during pregnancy maternal gut microbiota provide metabolites and substrates essential for fetal growth through metabolic provisioning, driving expansion and maturation of central and peripheral immune cells, and formation of neural circuits. Second, vertical transmission of maternal microbiota during birth and in the early postnatal window elicits a potent immunostimulatory effect in offspring that induces metabolic and developmental transcriptional programs, primes the immune system for subsequent microbial exposure, and provides substrates for brain metabolism. Finally, we explore the possibility that environmental factors, such as malnutrition, stress and infection, may exert programmatic effects by disrupting the functional contributions of the maternal microbiome during prenatal and postnatal development to influence offspring outcomes across the lifespan.