Potential role of the intestinal microbiota of the mother in neonatal immune education

Abstract

Mucosal dendritic cells are at the heart of decision-making processes that dictate immune reactivity to intestinal microbes. They ensure tolerance to commensal bacteria and a vigorous immune response to pathogens. It has recently been demonstrated that the former involves a limited migration of bacterially loaded dendritic cells from the Peyer's patches to the mesenteric lymph nodes. During lactation, cells from gut-associated lymphoid tissue travel to the breast via the lymphatics and peripheral blood. Here, we show that human peripheral blood mononuclear cells and breast milk cells contain bacteria and their genetic material during lactation. Furthermore, we show an increased bacterial translocation from the mouse gut during pregnancy and lactation and the presence of bacterially loaded dendritic cells in lactating breast tissue. Our observations show bacterial translocation as a unique physiological event, which is increased during pregnancy and lactation. They suggest endogenous transport of intestinally derived bacterial components within dendritic cells destined for the lactating mammary gland. They also suggest neonatal immune imprinting by milk cells containing commensal-associated molecular patterns.

Gut microbiota: a source of novel tools to reduce the risk of human disease?

“…Maternal microbial transmission is known to happen in the entire animal kingdom, including invertebrates and vertebrates (11). Experimental evidence in mice has been reported to support this notion (12,13). Maternal bacteria present in blood would reach the placenta tissue, from which microbes could reach the amniotic fluid and be swallowed by the fetus (3,4,8) or transfer into the fetal circulation, as has been demonstrated from maternal cells (14) and fetal transfer DNA material to maternal serum (15).…”

Human milk and infant intestinal mucosal glycans guide succession of the neonatal intestinal microbiota

“…Parallel investigations performed in mice showed that bacterial translocation increased during pregnancy and lactation. Further studies demonstrated endogenous transport of enteric bacterial components by dendritic cells, suggesting a key role in neonatal immune imprinting, but also providing a carrier mechanism for bacterial components assumed to be destined for the lactating mammary gland (30).…”

Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk

“…Breast milk has been to shown to be a source of microbes such as staphylococci, streptococci, lactic acid bacteria, and bifidobacteria (4). Bacterial translocation has been demonstrated in different parts of the body, including the gut (27,28). Dendritic cells that penetrate the intestinal epithelium take up commensal bacteria from the gut lumen and reach the systemic circulation, retaining even live bacteria for days (29).…”

“…Dendritic cells that penetrate the intestinal epithelium take up commensal bacteria from the gut lumen and reach the systemic circulation, retaining even live bacteria for days (29). More recently, their transfer to the mammary glands has been reported (27,28,30). Bifidobacteria are the hallmark of the gut microbiota in healthy breast-fed infants, and, apart from bifidogenic oligosaccharides, specific and distinctive species of Bifidobacterium are present in breast milk (4).…”