Profiling of G protein-coupled receptors in vagal afferents reveals novel gut-to-brain sensing mechanisms

Egerod, Kristoffer L.; Petersen, Natalia; Timshel, Pascal N.; Rekling, Jens C.; Wang, Yibing; Liu, Qinghua; Schwartz, Thue W.; Gautron, Laurent

doi:10.1016/j.molmet.2018.03.016

Cited by 191Gastrointestinal motility and disordersIon Channels and ReceptorsRegulation of Appetite and Obesity

Profiling of G protein-coupled receptors in vagal afferents reveals novel gut-to-brain sensing mechanisms

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Egerod, Kristoffer L., Petersen, Natalia, Timshel, Pascal N., Rekling, Jens C., Wang, Yibing, Liu, Qinghua, Schwartz, Thue W., Gautron, Laurent·2018·Molecular Metabolism

DOI 10.1016/j.molmet.2018.03.016PMC PMC6001940

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Abstract

G protein-coupled receptors (GPCRs) act as transmembrane molecular sensors of neurotransmitters, hormones, nutrients, and metabolites. Because unmyelinated vagal afferents richly innervate the gastrointestinal mucosa, gut-derived molecules may directly modulate the activity of vagal afferents through GPCRs. However, the types of GPCRs expressed in vagal afferents are largely unknown. Here, we determined the expression profile of all GPCRs expressed in vagal afferents of the mouse, with a special emphasis on those innervating the gastrointestinal tract. Using a combination of high-throughput quantitative PCR, RNA sequencing, and in situ hybridization, we systematically quantified GPCRs expressed in vagal unmyelinated Nav1.8-expressing afferents. GPCRs for gut hormones that were the most enriched in Nav1.8-expressing vagal unmyelinated afferents included NTSR1, NPY2R, CCK1R, and to a lesser extent, GLP1R, but not GHSR and GIPR. Interestingly, both GLP1R and NPY2R were coexpressed with CCK1R. In contrast, NTSR1 was coexpressed with GPR65, a marker preferentially enriched in intestinal mucosal afferents. Only few microbiome-derived metabolite sensors such as GPR35 and, to a lesser extent, GPR119 and CaSR were identified in the Nav1.8-expressing vagal afferents. GPCRs involved in lipid sensing and inflammation (e.g. CB1R, CYSLTR2, PTGER4), and neurotransmitters signaling (CHRM4, DRD2, CRHR2) were also highly enriched in Nav1.8-expressing neurons. Finally, we identified 21 orphan GPCRs with unknown functions in vagal afferents. Overall, this study provides a comprehensive description of GPCR-dependent sensing mechanisms in vagal afferents, including novel coexpression patterns, and conceivably coaction of key receptors for gut-derived molecules involved in gut-brain communication.

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There are distinct populations and subpopulations of vagal afferents responding to specific stimuli, including stretch or gut hormones.
“evidence suggests that there are distinct populations and subpopulations of vagal afferents responding to specific stimuli, including stretch (Williams et al., 2016a) or gut hormones (Egerod et al., 2018).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Egerod et al., 2018

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Authors: Egerod, K. L., Petersen, N., Timshel, P. N., Rekling, J. C., Wang, Y., Liu, Q., Schwartz, T. W., & Gautron, L.
Affiliations: University of Copenhagen (DK)
The University of Texas Southwestern Medical Center (US)
Corresponding author: Egerod, Kristoffer L.
Gautron, Laurent
ORCID: Egerod, Kristoffer L.
Petersen, Natalia
Timshel, Pascal N.
Rekling, Jens C.
Wang, Yibing
Liu, Qinghua
Schwartz, Thue W.
Venue: Molecular Metabolism
Publisher: Elsevier BV
Published: 2018-06
Volume: 12
Pages: 62-75
ISSN: 2212-8778 (ISSN-L)
DOI: 10.1016/j.molmet.2018.03.016
PMC: PMC6001940
OpenAlex: W2795588855
Cited by: 191
References: 85
Citations by year: 2026: 17 · 2025: 21 · 2024: 36 · 2023: 20 · 2022: 21 · 2021: 29 · 2020: 21 · 2019: 21 · 2018: 5
FWCI: 18.10
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Molecular Metabolism (publishedVersion, cc-by-nc-nd)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by-nc-nd)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Danmarks Frie Forskningsfond (7016-00389A, NNF14OC0016798, NNF15CC0018346, NNF15OC0016798)
Novo Nordisk Fonden (NNF10CC1016515)
Topics: Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords: G protein-coupled receptors, vagal afferents, gut-brain signaling, gastrointestinal hormones, neurotensin receptor 1, NPY2R, GLP-1 receptor, GPR65, GPR35, GPR119, calcium-sensing receptor, gut microbiota metabolites, lipid sensing, inflammation, orphan G protein-coupled receptor, gastrointestinal mucosa, receptor co-expression
MeSH terms: Animals, Brain, Cells, Cultured, Gastrointestinal Hormones, Intestinal Mucosa, Male, Mice, Inbred C57BL, Neurons, Afferent, Vagus Nerve, Signal Transduction, Receptors, G-Protein-Coupled, Mice, NAV1.8 Voltage-Gated Sodium Channel

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Profiling of G protein-coupled receptors in vagal afferents reveals novel gut-to-brain sensing mechanisms

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