Functional characterization of oxazolone-induced colitis and survival improvement by vagus nerve stimulation

Meroni, Elisa; Stakenborg, Nathalie; Gomez‐Pinilla, Pedro J.; Hertogh, Gert De; Goverse, Gera; Matteoli, Gianluca; Verheijden, Simon; Boeckxstaens, Guy E.

doi:10.1371/journal.pone.0197487

Cited by 50 publications

(34 citation statements)

References 45 publications

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“…This effect was associated with a progressive restoration of the colonic architecture together with a marked decrease in TNF‐α and IL‐6 production. Interestingly, we recently demonstrated that a single application of VNS to the cervical vagus nerve in mice significantly improves intestinal inflammation and survival in a mouse model of oxazolone‐induced colitis . VNS applied at the time of induction of oxazolone colitis reduced IL‐6, CXCL1 and TNFα serum levels, and dampened the colonic expression of IL‐6 and CXCL1 (Meroni et al, PLos One, in press).…”

Section: Pharmacological and Electrical Stimulation Of The Vagus Nervmentioning

confidence: 99%

Intestinal macrophages and their interaction with the enteric nervous system in health and inflammatory bowel disease

et al. 2018

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Over the past decades, there has been an increasing understanding of cellular and molecular mechanisms that mediate modulation of the immune system by the autonomic nervous system. The discovery that vagal nerve stimulation (VNS) attenuates endotoxin-induced experimental sepsis paved the way for further studies investigating neuro-immune interaction. In particular, great attention is now given to intestinal macrophages: several studies report the existence of both intrinsic and extrinsic neural mechanisms by which intestinal immune homoeostasis can be regulated in different layers of the intestine, mainly by affecting macrophage activation through neurotransmitter release. Given the important role of inflammation in numerous disease processes, such as inflammatory bowel disease (IBD), cholinergic anti-inflammatory mechanisms are under intense investigation both from a basic and clinical science perspective in immune-mediated diseases such as IBD. This review discusses recent insights on the cross-talk between enteric neurons and the immune system, especially focusing on macrophages, and provides an overview of basic and translational aspects of the cholinergic anti-inflammatory response as therapeutic alternative to reinstall immune homoeostasis in intestinal chronic inflammation.

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Section: Pharmacological and Electrical Stimulation Of The Vagus Nervmentioning

confidence: 99%

Intestinal macrophages and their interaction with the enteric nervous system in health and inflammatory bowel disease

et al. 2018

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“…As we previously showed anti‐inflammatory properties of VNS in colitis and postoperative ileus, we next evaluated the role of VNS on the development of food allergy . To this end, OVA‐sensitized Balb/C mice received VNS or sham stimulations prior to the first oral OVA challenge (Figure A).…”

Section: Resultsmentioning

confidence: 99%

“…Furthermore, it was demonstrated this effect is exerted by activation of enteric cholinergic neurons interacting with resident muscular CX3CR1 hi macrophages via α7 nicotinic acetylcholine receptors (α7nAChR) . To date, several additional studies have evaluated the effect of VNS and pharmacological cholinergic modulation in a range of experimental inflammatory models including endotoxemia, sepsis, inflammatory bowel disease, obesity and arthritis …”

Section: Introductionmentioning

confidence: 99%

Vagus nerve stimulation dampens intestinal inflammation in a murine model of experimental food allergy

Bosmans

Appeltans

Stakenborg

et al. 2019

Allergy

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Background The vagus nerve has emerged as an important modulator of the intestinal immune system. Its anti‐inflammatory properties have been previously shown in innate and Th1/Th17 predominant inflammatory models. To what extent the vagus nerve is of importance in Th2 inflammatory responses like food allergy is still unclear. In this study, we therefore aimed to investigate the effect of vagotomy (VGX) and vagus nerve stimulation (VNS), on the development and severity of experimental food allergy. Methods Balb/C mice were first sensitized with ovalbumin (OVA) in the presence of alum. Prior to oral challenges with OVA, mice were subjected to VGX or VNS. Disease severity was determined by assessing severity and onset of diarrhoea, OVA‐specific antibody production, mast cell number and activity, inflammatory gene expression in duodenal tissue and lamina propria immune cells by flow cytometry analysis. Results When compared to control mice, VGX did not significantly affect the development and severity of the disease in our model of food allergy. VNS, on the other hand, resulted in a significant amelioration of the different inflammatory parameters assessed. This effect was independent of α7nAChR and is possibly mediated through the dampening of mast cells and increased phagocytosis of OVA by CX3CR1hi macrophages. Conclusions These results underscore the anti‐inflammatory properties of the vagus nerve and the potential of neuro‐immune interactions in the intestine. Further insight into the underlying mechanisms could ultimately lead to novel therapeutic approaches in the treatment of not only food allergy but also other immune‐mediated diseases.

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“…108 Acetylcholine binds to a7 nicotinic acetylcholine receptors (a7nAChRs) expressed on macrophages, resulting in the suppressed production of proinflammatory cytokines, such as TNF-a, by macrophages, and suppressed inflammation. 100,109 This anti-inflammatory efferent vagus nervespleen axis has been demonstrated in many inflammatory disease models, including endotoxemia, 100,108,109 colitis, 110 and renal IRI 111 (discussed later). In addition, another antiinflammatory pathway mediated by the efferent vagus nerve has been described ( Figure 2).…”

Section: Neuroimmune Interaction In Regulating Inflammatory Diseasesmentioning

confidence: 94%

Crosstalk between the nervous system and the kidney

Tanaka

Okusa

2020

Kidney International

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Under physiological states, the nervous system and the kidneys communicate with each other to maintain normal body homeostasis. However, pathological states disrupt this interaction as seen in hypertension, and kidney damage can cause impaired renorenal reflex and sodium handling. In acute kidney injury (AKI) and chronic kidney disease (CKD), damaged kidneys can have a detrimental effect on the central nervous system. CKD is an independent risk factor for cerebrovascular disease and cognitive impairment, and many factors, including retention of uremic toxins and phosphate, have been proposed as CKD-specific factors responsible for structural and functional cerebral changes in patients with CKD. However, more studies are needed to determine the precise pathogenesis. Epidemiological studies have shown that AKI is associated with a subsequent risk for developing stroke and dementia. However, recent animal studies have shown that the renal nerve contributes to kidney inflammation and fibrosis, whereas activation of the cholinergic anti-inflammatory pathway, which involves the vagus nerve, the splenic nerve, and immune cells in the spleen, has a significant renoprotective effect. Therefore, elucidating mechanisms of communication between the nervous system and the kidney enables us not only to develop new strategies to ameliorate neurological conditions associated with kidney disease but also to design safe and effective clinical interventions for kidney disease, using the neural and neuroimmune control of kidney injury and disease.

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Functional characterization of oxazolone-induced colitis and survival improvement by vagus nerve stimulation

Cited by 50 publications

References 45 publications

Intestinal macrophages and their interaction with the enteric nervous system in health and inflammatory bowel disease

Intestinal macrophages and their interaction with the enteric nervous system in health and inflammatory bowel disease

Vagus nerve stimulation dampens intestinal inflammation in a murine model of experimental food allergy

Crosstalk between the nervous system and the kidney

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