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Lipid-rich enteral nutrition regulates mucosal mast cell activation via the vagal anti-inflammatory reflex.
Am J Physiol Gastrointest Liver Physiol. 2013 Sep 01; 305(5):G383-91.AJ

Abstract

Nutritional stimulation of the cholecystokinin-1 receptor (CCK-1R) and nicotinic acetylcholine receptor (nAChR)-mediated vagal reflex was shown to reduce inflammation and preserve intestinal integrity. Mast cells are important early effectors of the innate immune response; therefore modulation of mucosal mast cells is a potential therapeutic target to control the acute inflammatory response in the intestine. The present study investigates intestinal mast cell responsiveness upon nutritional activation of the vagal anti-inflammatory reflex during acute inflammation. Mucosal mast cell degranulation was induced in C57/Bl6 mice by administration of Salmonella enterica LPS. Lipid-rich enteral feeding prior to LPS significantly decreased circulatory levels of mouse mast cell protease at 30 min post-LPS compared with isocaloric low-lipid nutrition or fasting. CCK-1R blockage reversed the inhibitory effects of lipid-rich feeding, whereas stimulation of the peripheral CCK-1R mimicked nutritional mast cell inhibition. The effects of lipid-rich nutrition were negated by nAChR blockers chlorisondamine and α-bungarotoxin and vagal intestinal denervation. Accordingly, release of β-hexosaminidase by MC/9 mast cells following LPS or IgE-ovalbumin complexes was dose dependently inhibited by acetylcholine and nicotine. Application of GSK1345038A, a specific agonist of the nAChR α7, in bone marrow-derived mast cells from nAChR β2-/- and wild types indicated that cholinergic inhibition of mast cells is mediated by the nAChR α7 and is independent of the nAChR β2. Together, the present study reveals mucosal mast cells as a previously unknown target of the nutritional anti-inflammatory vagal reflex.

Authors+Show Affiliations

Dept. of Surgery at Maastricht Univ. Medical Centre+, Universiteitssingel 50, 6229 ER Maastricht, the Netherlands. w.buurman@maastrichtuniversity.nl.No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

23812038

Citation

de Haan, Jacco J., et al. "Lipid-rich Enteral Nutrition Regulates Mucosal Mast Cell Activation Via the Vagal Anti-inflammatory Reflex." American Journal of Physiology. Gastrointestinal and Liver Physiology, vol. 305, no. 5, 2013, pp. G383-91.
de Haan JJ, Hadfoune M, Lubbers T, et al. Lipid-rich enteral nutrition regulates mucosal mast cell activation via the vagal anti-inflammatory reflex. Am J Physiol Gastrointest Liver Physiol. 2013;305(5):G383-91.
de Haan, J. J., Hadfoune, M., Lubbers, T., Hodin, C., Lenaerts, K., Ito, A., Verbaeys, I., Skynner, M. J., Cailotto, C., van der Vliet, J., de Jonge, W. J., Greve, J. W., & Buurman, W. A. (2013). Lipid-rich enteral nutrition regulates mucosal mast cell activation via the vagal anti-inflammatory reflex. American Journal of Physiology. Gastrointestinal and Liver Physiology, 305(5), G383-91. https://doi.org/10.1152/ajpgi.00333.2012
de Haan JJ, et al. Lipid-rich Enteral Nutrition Regulates Mucosal Mast Cell Activation Via the Vagal Anti-inflammatory Reflex. Am J Physiol Gastrointest Liver Physiol. 2013 Sep 1;305(5):G383-91. PubMed PMID: 23812038.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Lipid-rich enteral nutrition regulates mucosal mast cell activation via the vagal anti-inflammatory reflex. AU - de Haan,Jacco J, AU - Hadfoune,M'hamed, AU - Lubbers,Tim, AU - Hodin,Caroline, AU - Lenaerts,Kaatje, AU - Ito,Akihiko, AU - Verbaeys,Isabelle, AU - Skynner,Michael J, AU - Cailotto,Cathy, AU - van der Vliet,Jan, AU - de Jonge,Wouter J, AU - Greve,Jan-Willem M, AU - Buurman,Wim A, Y1 - 2013/06/27/ PY - 2013/7/2/entrez PY - 2013/7/3/pubmed PY - 2013/10/29/medline KW - cholecystokinin KW - cholinergic anti-inflammatory pathway KW - enteral nutrition KW - nicotinic acetylcholine receptor KW - vagus nerve SP - G383 EP - 91 JF - American journal of physiology. Gastrointestinal and liver physiology JO - Am J Physiol Gastrointest Liver Physiol VL - 305 IS - 5 N2 - Nutritional stimulation of the cholecystokinin-1 receptor (CCK-1R) and nicotinic acetylcholine receptor (nAChR)-mediated vagal reflex was shown to reduce inflammation and preserve intestinal integrity. Mast cells are important early effectors of the innate immune response; therefore modulation of mucosal mast cells is a potential therapeutic target to control the acute inflammatory response in the intestine. The present study investigates intestinal mast cell responsiveness upon nutritional activation of the vagal anti-inflammatory reflex during acute inflammation. Mucosal mast cell degranulation was induced in C57/Bl6 mice by administration of Salmonella enterica LPS. Lipid-rich enteral feeding prior to LPS significantly decreased circulatory levels of mouse mast cell protease at 30 min post-LPS compared with isocaloric low-lipid nutrition or fasting. CCK-1R blockage reversed the inhibitory effects of lipid-rich feeding, whereas stimulation of the peripheral CCK-1R mimicked nutritional mast cell inhibition. The effects of lipid-rich nutrition were negated by nAChR blockers chlorisondamine and α-bungarotoxin and vagal intestinal denervation. Accordingly, release of β-hexosaminidase by MC/9 mast cells following LPS or IgE-ovalbumin complexes was dose dependently inhibited by acetylcholine and nicotine. Application of GSK1345038A, a specific agonist of the nAChR α7, in bone marrow-derived mast cells from nAChR β2-/- and wild types indicated that cholinergic inhibition of mast cells is mediated by the nAChR α7 and is independent of the nAChR β2. Together, the present study reveals mucosal mast cells as a previously unknown target of the nutritional anti-inflammatory vagal reflex. SN - 1522-1547 UR - https://www.unboundmedicine.com/medline/citation/23812038/Lipid_rich_enteral_nutrition_regulates_mucosal_mast_cell_activation_via_the_vagal_anti_inflammatory_reflex_ L2 - https://journals.physiology.org/doi/10.1152/ajpgi.00333.2012?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -