Stress at the intestinal surface: catecholamines and mucosa–bacteria interactions

Abstract

Psychological stress has profound effects on gastrointestinal function, and investigations over the past few decades have examined the mechanisms by which neural and hormonal stress mediators act to modulate gut motility, epithelial barrier function and inflammatory states. With its cellular diversity and large commensal bacterial population, the intestinal mucosa and its overlying mucous environment constitute a highly interactive environment for eukaryotic host cells and prokaryotic bacteria. The elaboration of stress mediators, particularly norepinephrine, at this interface influences host cells engaged in mucosal protection and the bacteria which populate the mucosal surface and gut lumen. This review will address growing evidence that norepinephrine and, in some cases, other mediators of the adaptation to stress modulate mucosal interactions with enteric bacteria. Stress-mediated changes in this delicate interplay may shift the microbial colonization patterns on the mucosal surface and alter the susceptibility of the host to infection. Moreover, changes in host-microbe interactions in the digestive tract may also influence ongoing neural activity in stress-responsive brain areas.

Visceral Pain and Gastrointestinal Microbiome

“…Restraint stress is shown to disrupt the microbiome in mice leading to an increase in colonization by Citrobacter rodentium, possibly by altering the local mucosal microenvironment, so that bacterial adherence patterns change. 24,25 More recently, it was demonstrated that exposure to as little as 2 hours of a social stressor (placement of a young C57BL/6 mouse in a cage with an Figure. This figure illustrates the interactions between microbiome, gut and brain which modulate responses to visceral pain. These interactions occur at the level of the gastrointestinal mucosa, and via local neural, endocrine or immune activity, as well as by the production of factors transported through the circulatory system, like bacterial metabolites or hormones.…”

Chemotaxis of Escherichia coli to Norepinephrine (NE) Requires Conversion of NE to 3,4-Dihydroxymandelic Acid

“…In particular, the bacterial quorum sensor kinase QseC has been implicated in the NE-induced expression of genes whose products are involved in adherence, motility, and pathogenesis (4, 5). However, the concentrations of NE required for effective induction of virulence genes, 50 M in one recent study (6), are higher than those that are expected to occur in the intestinal lumen (7,8). Thus, for NE to activate expression of virulence factors, bacteria would have to navigate to regions of the intestinal epithelium that have locally high concentrations of NE.…”

Glucocorticoids and the Intestinal Environment

“…These studies gathered the evidence that catecholamines stimulate the growth of a wide variety of gramnegative bacterial species, including those of medical importance [27,196,[204][205][206][207][208][209]. Furthermore, catecholamines were also found to be able to induce E.coli to produce a heatstable autoinducer of growth [19,27,204,210] as well as for adhesion required K99 pilus and shigella-like toxins I and II, which may have important roles in its pathogenic activity [210].…”

“…This system has many cellular targets for the stress mediators such as catecholamines, glucocorticoids and CRF [17][18][19]. The association between stress and various gastrointestinal diseases, including functional bowel disorders, inflammatory bowel disease (IBD), peptic ulcer disease and gastroeosophageal reflux disease, is being actively investigated [15,17].…”

“…They all together are called as gastrointestinal microbiota, and form the great part of the system. The microbiotahost interactions play an active role in many physiologic and pathophysiologic processes of the host [19,23,24]. While gastrointestinal microbiota could affect the stress response [25] and intestinal structure and functions of the host [23,24], stress hormones of the host organism such as the catecholamines can also alter directly growth, motility, biofilm formation and/or virulence of pathogens and commensal bacteria [19,26,27] or they may affect their microbiota indirectly by changing the intestinal environment [20].…”