Neuroimmune interactions in guinea pig stomach and small intestine
Abstract
Enteric neuroimmune interactions in gastrointestinal hypersensitivity responses involve antigen detection by mast cells, mast cell degranulation, release of chemical mediators, and modulatory actions of the mediators on the enteric nervous system (ENS). Electrophysiological methods were used to investigate electrical and synaptic behavior of neurons in the stomach and small intestine during exposure to beta-lactoglobulin in guinea pigs sensitized to cow's milk. Application of beta-lactoglobulin to sensitized preparations depolarized the membrane potential and increased neuronal excitability in small intestinal neurons but not in gastric neurons. Effects on membrane potential and excitability in the small intestine were suppressed by the mast cell stabilizing drug ketotifen, the histamine H(2) receptor antagonist cimetidine, the cyclooxygenase inhibitor piroxicam, and the 5-lipoxygenase inhibitor caffeic acid. Unlike small intestinal ganglion cells, gastric myenteric neurons did not respond to histamine applied exogenously. Antigenic exposure suppressed noradrenergic inhibitory neurotransmission in the small intestinal submucosal plexus. The histamine H(3) receptor antagonist thioperamide and piroxicam, but not caffeic acid, prevented the allergic suppression of noradrenergic inhibitory neurotransmission. Antigenic stimulation of neuronal excitability and suppression of synaptic transmission occurred only in milk-sensitized animals. Results suggest that signaling between mast cells and the ENS underlies intestinal, but not gastric, anaphylactic responses associated with food allergies. Histamine, prostaglandins, and leukotrienes are paracrine signals in the communication pathway from mast cells to the small intestinal ENS.
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Leukotrienes are involved in the secretory response of submucous neurons to food antigens.
“Thus, this study demonstrated the involvement of leukotrienes in the secretory response of submucous neurons to food antigens.”
From Effects of Coffee and Its Components on the Gastrointestinal Tract and the Brain–Gut Axis (2020) · cites this paper as [169]
In a guinea pig model of anaphylactic responses associated with food allergies, CA partially suppresses the hyperexcitability of submucous neurons induced by β-lactoglobulin in the small intestine.
“In the study by Wood et al., CA, which is a 5-lipoxygenase inhibitor [173], was able to partially suppress the hyperexcitability of submucous neurons induced by β-lactoglobulin in the small intestine of guinea pigs, which was used as a model of anaphylactic responses associated with food allergies [169].”
From Effects of Coffee and Its Components on the Gastrointestinal Tract and the Brain–Gut Axis (2020) · cites this paper as [169]
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- Authors
- Liu, S., Hu, H.-Z., Gao, N., Gao, C., Wang, G., Wang, X., Peck, O. C., Kim, G., Gao, X., Xia, Y., & Wood, J. D.
- Affiliations
- The Ohio State University (US)
- Department of Physiology and Cell Biology, Ohio State University, College of Medicine and Public Health, Columbus, Ohio 43210
- Venue
- American Journal of Physiology-Gastrointestinal and Liver Physiology
- Publisher
- American Physiological Society
- Published
- 2003-01-01
- Volume
- 284
- Issue
- 1
- Pages
- G154-G164
- ISSN
- 0193-1857 (ISSN-L)
- 1522-1547
- OpenAlex
- W2137337788
- Cited by
- 84
- References
- 39
- Citations by year
- 2025: 1 · 2023: 2 · 2022: 5 · 2020: 3 · 2019: 1 · 2018: 2 · 2017: 3 · 2016: 5 · 2014: 4 · 2013: 5 · 2012: 5
- FWCI
- 3.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Gastrointestinal and Liver Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-57075, DK-37238, R01DK057075)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Mast cells and histamine
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Medicine › Immunology and Allergy › Food Allergy and Anaphylaxis Research
- Keywords
- neuroimmune interactions, enteric nervous system, mast cells, food allergy, β-lactoglobulin, neuronal excitability, membrane potential, ketotifen, cimetidine, piroxicam, caffeic acid, histamine H3 receptor, submucosal plexus, mast cell degranulation, prostaglandins, leukotrienes, anaphylaxis
- MeSH terms
- Anaphylaxis, Animals, Electrophysiology, Fluorescent Antibody Technique, Guinea Pigs, Histamine, Histamine Antagonists, Intestine, Small, Lactoglobulins, Mast Cells, Membrane Potentials, Milk, Synaptic Transmission, Neurons, Ovalbumin, Serotonin Antagonists, Stomach, Submucous Plexus, Sympathetic Nervous System, Neuroimmunomodulation, Dinoprostone, Leukotriene C4
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