The gastrointestinal tract of a normal fetus is sterile. During the birth process and rapidly thereafter, microbes from the mother and surrounding environment colonize the gastrointestinal tract of the infant until a dense, complex microbiota develops. The succession of microbes colonizing the intestinal tract is most marked in early development, during which the feeding mode shifts from breast-feeding to formula feeding to weaning to the introduction of solid food. Dynamic balances exist between the gastrointestinal microbiota, host physiology, and diet that directly influence the initial acquisition, developmental succession, and eventual stability of the gut ecosystem. In this review, the development of the intestinal microbiota is discussed in terms of initial acquisition and subsequent succession of bacteria in human infants. Intrinsic and extrinsic factors influencing succession and their health significance are discussed. The advantages of modern molecular ecology techniques that provide sensitive and specific, culture-independent evaluation of the gastrointestinal ecosystem are introduced and discussed briefly. Further advances in our understanding of developmental microbial ecology in the neonatal gastrointestinal tract are dependent on the application of these modern molecular techniques.
The gastrointestinal epithelium is covered by a protective mucus gel composed predominantly of mucin glycoproteins that are synthesized and secreted by goblet cells. Changes in goblet cell functions and in the chemical composition of intestinal mucus are detected in response to a broad range of luminal insults, including alterations of the normal microbiota. However, the regulatory networks that mediate goblet cell responses to intestinal insults are poorly defined. The present review summarizes the results of developmental, gnotobiotic, and in vitro studies that showed alterations in mucin gene expression, mucus composition, or mucus secretion in response to intestinal microbes or host-derived inflammatory mediators. The dynamic nature of the mucus layer is shown. Available data indicate that intestinal microbes may affect goblet cell dynamics and the mucus layer directly via the local release of bioactive factors or indirectly via activation of host immune cells. A precise definition of the regulatory networks that interface with goblet cells may have broad biomedical applications because mucus alterations appear to characterize most diseases of mucosal tissues.
Compromising alterations in villus-crypt structure are common in pigs postweaning. Possible contributions of local inflammatory reactions to villus-crypt alterations during the weaning transition have not been described. This study evaluated local inflammatory responses and their relationship with morphological changes in the intestine in 21-d-old pigs (n = 112) killed either at weaning (Day 0) or 0.5, 1, 2, 4 or 7 d after weaning to either milk- or soy-based pelleted diets. Cumulative intake averaged <100 g during the first 2 d postweaning, regardless of diet. During this period of weaning anorexia, inflammatory T-cell numbers and local expression of the matrix metalloproteinase stromelysin increased while jejunal villus height, crypt depth and major histocompatibility complex (MHC) class I RNA expression decreased. Upon resumption of feed intake by the fourth d postweaning, villus height and crypt depth, CD8(+) T cell numbers, MHC class I RNA expression and local expression of stromelysin returned to Day 0 values. Together the results indicate that inadequate feed intake during the immediate postweaning period may contribute to intestinal inflammation and thereby compromise villus-crypt structure and function.
Compromising alterations in gastrointestinal architecture are common during the weaning transition of pigs. The relation between villous atrophy and epithelial barrier function at weaning is not well understood. This study evaluated in vitro transepithelial transport by Ussing metabolic chambers, local alterations in T-cell subsets and villous architecture at low energy intake level and their relation with lactose/protein ratios in the diet. Pigs (n = 66, 26 d old) were sampled either at weaning (d 0), d 1, 2 or 4 postweaning. Piglets received one of three diets at a low energy intake level, which differed in lactose and protein ratio as follows: low lactose/high protein (LL/HP), control (C), or high lactose/low protein (HL/LP). Mean digestible energy intake was 648 kJ/pig on d 1, 1668 kJ/pig on d 2, 1995 kJ/pig on d 3 and 1990 kJ/pig on d 4 postweaning. The CD4(+)/CD8(+) T-lymphocytes ratio decreased after weaning (P < 0.05). Decreased paracellular transport (P < 0.01), greater villous height (P < 0.01), shallower crypts and lower villus/crypt ratios (P < 0.01) were observed on d 2 compared with d 0. Piglets consuming the HL/LP diet tended to have less paracellular transport (P < 0.10) and greater villous height (P < 0.10) compared with piglets fed the other diets. During the first 4 d postweaning, the effect of diet composition on mucosal integrity was not as important as the sequential effects of low energy intake at weaning. Stress and diminished enteral stimulation seem to compromise mucosal integrity as indicated by increased paracellular transport and altered T-cell subsets.
Among the numerous purported health benefits attributed to probiotic bacteria, their capacity to interact with the immune system of the host is now supported by an increasing number of in vitro and in vivo experiments. In addition to these, a few well-controlled human intervention trials aimed at preventing chronic immune dysregulation have been reported. Even though the precise molecular mechanisms governing the cross-talk between these beneficial bacteria and the intestinal ecosystem remain to be discovered, a new and fascinating phase of research has been initiated in this area as demonstrated by a series of recent articles. This article summarizes the status and latest progress of the field in selected areas and aims at identifying key questions that remain to be addressed, especially concerning the translocation of ingested bacteria, the identification of major immunomodulatory compounds of probiotics, and specific aspects of the host-microbe cross-talk. The interaction with immunocompetent cells and the role of secretory IgA in gut homeostasis are also evoked. Finally, a brief overview is provided on the potential use of recombinant DNA technology to enhance the health benefits of probiotic strains and to unravel specific mechanisms of the host-microbe interaction.
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