Abstract
Stress refers to a dynamic process in which the homeostasis of an organism is challenged, the outcome depending on the type, severity, and duration of stressors involved, the stress responses triggered, and the stress resilience of the organism. Importantly, the relationship between stress and the immune system is bidirectional, as not only stressors have an impact on immune function, but alterations in immune function themselves can elicit stress responses. Such bidirectional interactions have been prominently identified to occur in the gastrointestinal tract in which there is a close cross-talk between the gut microbiota and the local immune system, governed by the permeability of the intestinal mucosa. External stressors disturb the homeostasis between microbiota and gut, these disturbances being signaled to the brain via multiple communication pathways constituting the gut–brain axis, ultimately eliciting stress responses and perturbations of brain function. In view of these relationships, the present article sets out to highlight some of the interactions between peripheral immune activation, especially in the visceral system, and brain function, behavior, and stress coping. These issues are exemplified by the way through which the intestinal microbiota as well as microbe-associated molecular patterns including lipopolysaccharide communicate with the immune system and brain, and the mechanisms whereby overt inflammation in the GI tract impacts on emotional-affective behavior, pain sensitivity, and stress coping. The interactions between the peripheral immune system and the brain take place along the gut–brain axis, the major communication pathways of which comprise microbial metabolites, gut hormones, immune mediators, and sensory neurons. Through these signaling systems, several transmitter and neuropeptide systems within the brain are altered under conditions of peripheral immune stress, enabling adaptive processes related to stress coping and resilience to take place. These aspects of the impact of immune stress on molecular and behavioral processes in the brain have a bearing on several disturbances of mental health and highlight novel opportunities of therapeutic intervention.
Highlights
In a general context, stress is considered to be a dynamic process in which the physical and/or mental homeostasis of an organism is challenged, the outcome depending on the type, severity, and duration of stimuli involved, the stress responses triggered and the stress susceptibility/resilience of the organism
This disturbance of gut homeostasis is signaled to the central nervous system (CNS) via multiple communication pathways constituting the gut–brain axis, eliciting stress responses and perturbations of brain function [5]
The gut microbiota is a rich source of potential messenger molecules: primary metabolites generated by microbial cells, microbe-associated molecular patterns (MAMPs), and Pathogen-associated molecular patterns (PAMPs) shed from microbial cells, and secondary metabolites generated by microbial fermentation of food components or transformation of host molecules such as bile acids [27, 51,52,53,54,55]
Summary
Stress is considered to be a dynamic process in which the physical and/or mental homeostasis of an organism is challenged, the outcome depending on the type, severity, and duration of stimuli (stressors) involved, the stress responses triggered and the stress susceptibility/resilience of the organism. In addition, been argued that there are dormant bacterial reservoirs in the blood and certain tissues, including the brain, and that PAMP production in these reservoirs may contribute to chronic inflammatory disease [25] In view of these facts and conditions, the present article sets out to highlight some of the interactions between peripheral immune activation, especially in the visceral system, and brain function, behavior, and stress coping. A number of gut hormones including PYY, GLP-1, and ghrelin signal to the brain to affect appetite and energy homeostasis and impact on mood and emotional-affective behavior [29, 32,33,34] This messaging is accomplished via a circulatory route and through activation of vagal afferent neurons [5, 41]. GI interoception includes a wide range of conscious sensations, such as pain, nausea, GI discomfort, GI tension, hunger, and thirst, as well as signaling processes that go virtually unnoticed they impact on emotional-affective and cognitive processes [48,49,50]
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