Inhibitory effect of glucagon-like peptide-1 on small bowel motility. Fasting but not fed motility inhibited via nitric oxide independently of insulin and somatostatin.

Tolessa, T; Gutniak, M; Holst, J J; Efendic, S; Hellström, P M

doi:10.1172/jci942

Cited by 139Gastrointestinal motility and disordersNeuropeptides and Animal PhysiologyDiabetes Treatment and Management

Inhibitory effect of glucagon-like peptide-1 on small bowel motility. Fasting but not fed motility inhibited via nitric oxide independently of insulin and somatostatin.

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Tolessa, T, Gutniak, M, Holst, J J, Efendic, S, Hellström, P M·1998·Journal of Clinical Investigation

DOI 10.1172/jci942PMC PMC508939

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Abstract

Effects of glucagon-like peptide-1 (GLP-1)(7-36)amide on fasted and fed motility in the rat small intestine were investigated in relation to its dependence on nitric oxide (NO), insulin, and somatostatin.Small bowel electromyography was performed using bipolar electrodes implanted 15, 25, and 35 cm distal to pylorus, and transit was studied with a radioactive marker.In the fasted state, GLP-1 (5-20 pmol kg Ϫ 1 min Ϫ 1 ), reaching physiological plasma levels, prolonged the migrating myoelectric complex (MMC) cycle length along with slowed transit.This effect was antagonized by exendin(9-39)amide.The NO synthase inhibitor N -nitro-L -arginine (L-NNA) also blocked the response to GLP-1, whereas L -arginine restored the response.Insulin (80-200 pmol kg Ϫ 1 min Ϫ 1 ) induced irregular spiking, whereas somatostatin (100-500 pmol kg Ϫ 1 min Ϫ 1 ) increased the MMC cycle length, independently of NO.In the fed state, GLP-1 (20-40 pmol kg Ϫ 1 min Ϫ 1 ) reduced motility, an inhibition unaffected by L-NNA, whereas motility was stimulated by exendin(9-39)amide.Infusion of GLP-1 (20-100 pmol kg Ϫ 1 min Ϫ 1 ) did not affect plasma insulin, but somatostatin was increased.In conclusion, GLP-1 seems to inhibit small bowel motility directly via the GLP-1 receptor.Inhibition of fasting motility is dependent of NO and not mediated via insulin or somatostatin, whereas inhibition of fed motility is independent of NO. ( J. Clin.Invest.1998.102:764-774.)Key words: gastrointestinal motility • glucagon-like peptide-1 • migrating myoelectric complex • rat • small intestine Methods 107 male Sprague-Dawley rats (B&K, Sollentuna, Sweden) weighing 300-350 g were used for the study.The experimental protocol was approved by the local Ethics committee for animal experimentation in northern Stockholm, Sweden.Preparation of rats for electromyography.53 rats were anaesthetized with pentobarbital (50 mg kg Ϫ 1 intraperitoneally; Apoteksbolaget, Umeå, Sweden) and, through a midline incision, three bipolar stainless steel electrodes (SS-5T, Clark Electromedical Instruments, Reading, UK) were implanted into the muscular wall of the small intestine 15 (J1), 25 (J2), and 35 (J3) cm distal to the pylorus.All animals were supplied with one or two jugular vein catheters for administration of drugs.The electrodes and catheters were tunneled subcutaneously to exit at the back of the animal's neck.After surgery the animals were housed singly and allowed to recover for at least 7 d before experiments were undertaken.During recovery the rats were trained to accept experimental conditions.Experiments were then carried out in conscious animals after an 8-h fasting period in wirebottomed cages with free access to water.During the experiments, the rats were placed in Bollman cages.The electrodes were connected to an EEG preamplifier (7P5B) operating a Grass Polygraph 7B (Grass Instruments, Quincy, MA).The time constant was set at 0.015 s and the low and high cut-off frequencies were set at 10 and 35 Hz, respectively.

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GLP-1 RAs decelerate gastric emptying to levels indicative of gastroparesis.
“The capacity of GLP-1 RAs to decelerate gastric emptying to levels indicative of gastroparesis raises concerns regarding potential intestinal obstruction and perioperative aspiration risk.”
From Exploring the Side Effects of GLP-1 Receptor Agonist: To Ensure Its Optimal Positioning (2025) · cites this paper as [26]
The Discussion (page not provided) describes an inhibitory effect of GLP-1 on gastric emptying, citing a finding in healthy humans. The paper’s own experiments concern small-bowel motility in rats; it does not establish that GLP-1 receptor agonists delay gastric emptying to levels indicative of gastroparesis. (LLM, conf=0.88)
Experimental — accuracy not yet measured
GLP-1 inhibits intestinal contractions through mechanisms that may involve the central nervous system via vagal pathways or direct action on central receptors, and the enteric nervous system by modulating neurotransmission through presynaptic receptors affecting nitric oxide release.
“GLP-1 inhibits intestinal contractions through mechanisms that may involve the central nervous system via vagal pathways or direct action on central receptors [24], as well as the enteric nervous system by modulating neurotransmission through presynaptic receptors affecting nitric oxide release [25,26].”
From Exploring the Side Effects of GLP-1 Receptor Agonist: To Ensure Its Optimal Positioning (2025) · cites this paper as [26]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
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Nitric oxide mediates some effects of GLP-1, including inhibition of small bowel motility in rats, protection against ethanol-induced gastric mucosal lesions, and relaxation of vascular endothelium.
“Because nitric oxide (NO) mediates some effects of GLP-1 (e.g., inhibition of small bowel motility in rats) (48)—protection against ethanol-induced gastric mucosal lesions (20) and relaxation of vascular endothelium (31)]”
From Effects of glucagon-like peptide-1, yohimbine, and nitrergic modulation on sympathetic and parasympathetic activity in humans (2008) · cites this paper as [48]

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Glucagon-like peptide 1 as a regulator of food intake and body weight: therapeutic perspectives
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The Effect of Bariatric Surgery on Intestinal Absorption and Transit Time
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Effects of glucagon-like peptide-1, yohimbine, and nitrergic modulation on sympathetic and parasympathetic activity in humans
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Somatostatin-28 regulates GLP-1 secretion via somatostatin receptor subtype 5 in rat intestinal cultures
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Incretin‐Based Drugs and Risk of Intestinal Obstruction Among Patients With Type 2 Diabetes
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Glucagon-like Peptide-1 (GLP-1) and the Control of Glucose Metabolism in Mammals and Teleost Fish1
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GLP-2: What do we know? What are we going to discover?
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Nitrergic contribution to gastric relaxation induced by glucagon-like peptide-1 (GLP-1) in healthy adults
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Effects of glucagon‐like peptide‐1 and sympathetic stimulation on gastric accommodation in humans<sup>1</sup>
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Glucagon-like peptide-1 modulates neurally evoked mucosal chloride secretion in guinea pig small intestine in vitro
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Exendin-4, an analogue of glucagon-like peptide-1, attenuates hyperalgesia through serotonergic pathways in rats with neonatal colonic sensitivity.
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Local, exendin-(9—39)-insensitive, site of action of GLP-1 in canine ileum
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The inhibitory mechanism of GLP-1, but not glucagon, on fasted gut motility is dependent on the l-arginine/nitric oxide pathway
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Influences of protein ingestion on glucagon‐like peptide ( GLP )‐1‐immunoreactive endocrine cells in the chicken ileum
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Transient, early release of glucagon-like peptide-1 during low rates of intraduodenal glucose delivery
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The Enteroendocrine System in Obesity
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Receptor-mediated inhibition of small bowel migrating complex by GLP-1 analog ROSE-010 delivered via pulmonary and systemic routes in the conscious rat
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Glucagon-like Peptide-1 (GLP-1) and the Control of Glucose Metabolism in Mammals and Teleost Fish
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Relevance of Glucagon-Like Peptide 1 (GLP-1) in Inflammatory Bowel Diseases: A Narrative Review
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Effects of Glucagon-like Peptide-1 in Diabetic Rat Small Resistance Arteries
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The inhibitory mechanism of GLP-1, but not glucagon, on fasted gut motility is dependent on the l-arginine/nitric oxide pathway
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GLP-1 and GLP-2 act in concert to inhibit fasted, but not fed, small bowel motility in the rat
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Self-citation

Authors: Tolessa, T., Gutniak, M., Holst, J. J., Efendic, S., & Hellström, P. M.
Affiliations: Karolinska University Hospital (SE)
University of Copenhagen (DK)
Corresponding author: Hellström, P M
ORCID: Tolessa, T
Holst, J J
Hellström, P M
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 1998-08-15
Volume: 102
Issue: 4
Pages: 764-774
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci942
PMC: PMC508939
OpenAlex: W1993285386
Semantic Scholar: d5e144c56460491fd3e29399f7faa9668bc1b92f
Cited by: 139
References: 50
Citations by year: 2026: 5 · 2025: 3 · 2024: 8 · 2023: 2 · 2022: 2 · 2021: 7 · 2019: 2 · 2018: 5 · 2017: 3 · 2016: 5 · 2015: 2 · 2014: 8 · 2013: 5 · 2012: 8
FWCI: 3.52
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
Funders: Magnus Bergvalls Stiftelse
Medical Research Council
Topics: Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
Keywords: glucagon-like peptide-1, small intestine motility, migrating motor complex, nitric oxide, insulin, somatostatin, exendin-9-39, GLP-1 receptor, intestinal transit, L-NNA, L-arginine, gastrointestinal hormones, rat intestine
MeSH terms: Glucagon-Like Peptide-1 Receptor, Animals, Drug Interactions, Eating, Electromyography, Fasting, Gastrointestinal Motility, Gastrointestinal Transit, Glucagon, Insulin, Intestine, Small, Male, Nitric Oxide, Peptide Fragments, Protein Precursors, Somatostatin, Myoelectric Complex, Migrating, Rats, Sprague-Dawley, Receptors, Glucagon, Nitric Oxide Synthase, Nitroarginine, Rats, Glucagon-Like Peptide 1

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Inhibitory effect of glucagon-like peptide-1 on small bowel motility. Fasting but not fed motility inhibited via nitric oxide independently of insulin and somatostatin.

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