5-HT7 receptors modulate peristalsis and accommodation in the guinea pig ileum

Marcello Tonini, Riccardo Vicini, Elisabetta Cervio, Fabrizio De Ponti, Roberto De Giorgio, Giovanni Barbara, Vincenzo Stanghellini, Antonio Dellabianca, Catia Sternini

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Abstract

Background & Aims: The 5-hydroxytryptamine 7 (5-HT7) receptors mediate intestinal smooth muscle relaxation. In this study, we evaluated the expression of 5-HT7 receptors in the guinea pig ileum and their role in peristalsis and accommodation of the circular muscle. Methods: We used immunohistochemistry and confocal microscopy with whole tissue and cultured myenteric neurons. Peristalsis was induced by delivering a solution into the oral end of an isolated ileal segment. The effect of the selective 5-HT7 receptor antagonist SB-269970 (100 nmol/L) on peristaltic activity was evaluated at 30, 60, and 90 minutes and compared with control. Results: 5-HT7 receptor immunoreactivity was localized to numerous myenteric neurons, a few submucosal neurons, and a few smooth muscle cells of the ileum. In enteric cultured neurons, 5-HT7 receptor immunoreactivity was observed in subpopulations of after hyperpolarizing neurons and descending neurons as identified by neuron-specific nuclear protein or calbindin and neuronal nitric oxide synthase or vasoactive intestinal peptide antibodies, respectively. SB-269970 significantly increased the threshold pressure by 33.3% ± 2.2% (P <.001) and by 27.2% ± 1.6% (P <.05) at 60 and 90 minutes, respectively, without modifying the threshold volume. The accommodation significantly decreased by 27.5% both at 60 and 90 minutes (P <.05). Conclusions: Our results indicate that endogenous 5-HT is involved in the modulation of circular muscle accommodation during the preparatory phase of peristalsis via the activation of 5-HT7 receptors expressed by neurons in addition to smooth muscle cells. Overstimulation of these receptors leading to an exaggerated accommodation of circular muscle might contribute to abdominal symptoms in functional bowel disorders.

Original languageEnglish
Pages (from-to)1557-1566
Number of pages10
JournalGastroenterology
Volume129
Issue number5
DOIs
Publication statusPublished - Nov 2005

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Peristalsis
Ileum
Guinea Pigs
Neurons
Muscles
Smooth Muscle Myocytes
Calbindins
Nitric Oxide Synthase Type I
Muscle Relaxation
serotonin 7 receptor
Vasoactive Intestinal Peptide
Nuclear Proteins
Confocal Microscopy
Smooth Muscle
Serotonin
Immunohistochemistry
Pressure
Antibodies

ASJC Scopus subject areas

  • Gastroenterology

Cite this

Tonini, M., Vicini, R., Cervio, E., De Ponti, F., De Giorgio, R., Barbara, G., ... Sternini, C. (2005). 5-HT7 receptors modulate peristalsis and accommodation in the guinea pig ileum. Gastroenterology, 129(5), 1557-1566. https://doi.org/10.1053/j.gastro.2005.08.005

5-HT7 receptors modulate peristalsis and accommodation in the guinea pig ileum. / Tonini, Marcello; Vicini, Riccardo; Cervio, Elisabetta; De Ponti, Fabrizio; De Giorgio, Roberto; Barbara, Giovanni; Stanghellini, Vincenzo; Dellabianca, Antonio; Sternini, Catia.

In: Gastroenterology, Vol. 129, No. 5, 11.2005, p. 1557-1566.

Research output: Contribution to journalArticle

Tonini, M, Vicini, R, Cervio, E, De Ponti, F, De Giorgio, R, Barbara, G, Stanghellini, V, Dellabianca, A & Sternini, C 2005, '5-HT7 receptors modulate peristalsis and accommodation in the guinea pig ileum', Gastroenterology, vol. 129, no. 5, pp. 1557-1566. https://doi.org/10.1053/j.gastro.2005.08.005
Tonini M, Vicini R, Cervio E, De Ponti F, De Giorgio R, Barbara G et al. 5-HT7 receptors modulate peristalsis and accommodation in the guinea pig ileum. Gastroenterology. 2005 Nov;129(5):1557-1566. https://doi.org/10.1053/j.gastro.2005.08.005
Tonini, Marcello ; Vicini, Riccardo ; Cervio, Elisabetta ; De Ponti, Fabrizio ; De Giorgio, Roberto ; Barbara, Giovanni ; Stanghellini, Vincenzo ; Dellabianca, Antonio ; Sternini, Catia. / 5-HT7 receptors modulate peristalsis and accommodation in the guinea pig ileum. In: Gastroenterology. 2005 ; Vol. 129, No. 5. pp. 1557-1566.
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abstract = "Background & Aims: The 5-hydroxytryptamine 7 (5-HT7) receptors mediate intestinal smooth muscle relaxation. In this study, we evaluated the expression of 5-HT7 receptors in the guinea pig ileum and their role in peristalsis and accommodation of the circular muscle. Methods: We used immunohistochemistry and confocal microscopy with whole tissue and cultured myenteric neurons. Peristalsis was induced by delivering a solution into the oral end of an isolated ileal segment. The effect of the selective 5-HT7 receptor antagonist SB-269970 (100 nmol/L) on peristaltic activity was evaluated at 30, 60, and 90 minutes and compared with control. Results: 5-HT7 receptor immunoreactivity was localized to numerous myenteric neurons, a few submucosal neurons, and a few smooth muscle cells of the ileum. In enteric cultured neurons, 5-HT7 receptor immunoreactivity was observed in subpopulations of after hyperpolarizing neurons and descending neurons as identified by neuron-specific nuclear protein or calbindin and neuronal nitric oxide synthase or vasoactive intestinal peptide antibodies, respectively. SB-269970 significantly increased the threshold pressure by 33.3{\%} ± 2.2{\%} (P <.001) and by 27.2{\%} ± 1.6{\%} (P <.05) at 60 and 90 minutes, respectively, without modifying the threshold volume. The accommodation significantly decreased by 27.5{\%} both at 60 and 90 minutes (P <.05). Conclusions: Our results indicate that endogenous 5-HT is involved in the modulation of circular muscle accommodation during the preparatory phase of peristalsis via the activation of 5-HT7 receptors expressed by neurons in addition to smooth muscle cells. Overstimulation of these receptors leading to an exaggerated accommodation of circular muscle might contribute to abdominal symptoms in functional bowel disorders.",
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AU - Stanghellini, Vincenzo

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