Regulatory mechanisms in endoluminal release of serotonin and substance P from feline jejunum

Grönstad, K.O.; Dahlström, Annica; Florence, Lisa S.; Zinner, Michael J.; Ahlman, J. R.; Jaffe, Bernard M.

doi:10.1007/bf01296293

Cited by 24 publications

(8 citation statements)

References 17 publications

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“…EC cells have been considered to release 5-HT mainly into the blood vessels and/or intrinsic nerve terminal via a basolateral border (21). In contrast, others showed that 5-HT is also released into the intestinal lumen (1,15,28,35). We have recently demonstrated that 5-HT is released into the lumen, but not into the portal circulation in response to luminal pressure increase of the rat proximal colon (55).…”

Section: -Ht3 Receptors; 5-ht4 Receptors; Enterochromaffin Cellsmentioning

confidence: 96%

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Endogenous ghrelin and 5-HT regulate interdigestive gastrointestinal contractions in conscious rats

Taniguchi

Ariga²,

Zheng³

et al. 2008

American Journal of Physiology-Gastrointestinal and Liver Physi

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Endogenous ghrelin causes interdigestive contractions of the stomach in rats. In contrast, previous studies showed that 5-HT3 and 5-HT4 receptors were involved in regulating intestinal interdigestive contractions. We studied the possible role of endogenous ghrelin and 5-HT regulating interdigestive gastrointestinal (GI) contractions in rats. Four strain gauge transducers were implanted on the antrum, duodenum, and proximal and distal jejunum. After an overnight fast, GI contractions were recorded in freely moving conscious rats and ghrelin receptor antagonists [(D-lys3)GHRP6; 1 mol/kg], 5-HT3 antagonists (Ondansetron; 0.5 mg/kg) and 5-HT 4 antagonists (GR 125,487; 1 mg/kg) were administered (bolus iv). To evaluate the relationship between the luminal concentrations of 5-HT and phase III-like contractions of the duodenum, duodenal juice was collected via the intraduodenal catheter. 5-HT content of the duodenal juice was measured by HPLC. (D-lys3)GHRP6 significantly attenuated the occurrence and amplitude of phase III-like contractions of the antrum, but not the duodenum and jejunum. 5-HT 4 antagonists significantly reduced spontaneous phase III-like contractions of the jejunum, without affecting those of the antrum and duodenum. In contrast, 5-HT 3 antagonists did not affect phase III-like contractions in GI tract. Luminal concentration of 5-HT at the phase III-like contraction (36.0 Ϯ 13.3 ng/ml, n ϭ 9) was significantly higher than that at the phase I-like contractions of the duodenum (4.9 Ϯ 1.6 ng/ml, n ϭ 9, P Ͻ 0.05). It is suggested that released ghrelin from the gastric mucosa mediates gastric phase III-like contractions, whereas 5-HT released from enterochromaffin cells of the duodenal mucosa mediates intestinal phase III-like contractions via 5-HT 4 receptors. 5-HT3 receptors; 5-HT4 receptors; enterochromaffin cells DURING THE INTERDIGESTIVE state, the stomach and small intestine show a remarkable motor pattern, known as the migrating motor complex (MMC) in dogs (51) and humans (56). MMC consists of three phases: phase I (period of motor quiescence), phase II (period of irregular low-amplitude contractions), and phase III (period of regular high-amplitude contractions). Phase III contractions of MMC have physiological importance for clearance of secretions, debris, and microbes during fasting and let the stomach be ready to receive a next meal (56). Plasma motilin levels are highly associated with the appearance of gastric phase III in dogs (34). Motilin administration caused phase III contractions in human and dogs (33, 60).The characteristic feature of gastric MMC is different among species. In humans and dogs, MMC is usually observed every 90 -120 min the interdigestive state. In contrast, MMC cycle is short (less than 20 min) in rats and not so regular as that of humans and dogs (2, 18, 53). Since it is rather difficult to distinguish three phases in rats, these phases are called as phase I-like contractions and phase III-like contractions in rats (3,18,53).Ghrelin, a 28-amino acid peptide, was discov...

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Section: -Ht3 Receptors; 5-ht4 Receptors; Enterochromaffin Cellsmentioning

confidence: 96%

“…EC cells release 5-HT into the blood vessels and intrinsic nerve terminal via a basolateral border (21). 5-HT is also released into the intestinal lumen from EC cells (1,15,28,35).…”

Section: Discussionmentioning

confidence: 99%

Endogenous ghrelin and 5-HT regulate interdigestive gastrointestinal contractions in conscious rats

Taniguchi

Ariga²,

Zheng³

et al. 2008

American Journal of Physiology-Gastrointestinal and Liver Physi

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“…However, a number of in vivo studies have shown a measurable amount of serotonin (5HT) in the intestinal lumen of various species. Known stimulants for such luminal release of 5HT include vagal nerve stimulation (Ahlman et al 1981;Grönstad et al 1987;Zinner et al 1982), luminal acidification (Kellum et al 1983;Resnick and Gray 1962), food intake (Ferrara et al 1987) or an increase in luminal pressure (Bülbring and Crema 1959). Luminal release of 5HT has also been examined in vitro using isolated mucosa/submucosal sheets, and known stimulants include mucosal acidification and cholinergic and β-adrenergic mechanisms Miller 1982, 1983;Kellum et al 1983Kellum et al , 1984a.…”

Section: Introductionmentioning

confidence: 99%

Immunoelectron microscopic study of the luminal release of serotonin from rat enterochromaffin cells induced by high intraluminal pressure

Fujimiya

Okumiya²,

Kuwahara

1997

Histochemistry and Cell Biology

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Since definitive morphological studies showing the luminal release of serotonin have not been reported, we used a perfused system which allows physiological monitoring and biochemical as well as morphological evidence indicating release of serotonin from enterochromaffin cells. Isolated vascularly and luminally perfused rat duodenums exposed to 5-35 cmH2O of luminal pressure were measured for release of serotonin into the blood vessels and intestinal lumen. Immediately after raising the luminal pressure, the duodenum was fixed for immunoelectron microscopic localization of serotonin. Peristaltic contraction and serotonin content of the perfusates were continuously measured. The luminal release of serotonin increased with elevated intraluminal pressure, but the vascular release of serotonin was not altered. Tetrodotoxin had no effect on the pressure-stimulated luminal serotonin release. Enterochromaffin cells in control animals without increased luminal pressure contained immunogold-labeled secretory granules in the apical and basal cytoplasm. After intraluminal pressure increased, many apical secretory granules were no longer dense and immunogold particles were localized over the cytoplasmic matrix and microvilli. These findings indicate that luminal serotonin release is increased after raising the intraluminal pressure and serotonin, normally stored in the secretory granules of enterochromaffin cells, appears to be released into the cytoplasmic matrix and then diffuses or is transported into the intestinal lumen.

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“…In contrast, others showed that 5-HT is also released into the intestinal lumen in response to vagal nerve stimulation (1,20), luminal acidification (25), and food intake (10). Immunoelectron microscopic study showed the anatomical evidence that 5-HT is released from EC cells in response to an increase of luminal pressure of the rat duodenum (12).…”

mentioning

confidence: 99%

Luminally released serotonin stimulates colonic motility and accelerates colonic transit in rats

Tsukamoto

Ariga²,

Mantyh³

et al. 2007

American Journal of Physiology-Regulatory, Integrative and Comp

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(EC) cells of the epithelial cells release 5-HT into the lumen, as well as basolateral border. However, the physiological role of released 5-HT into the lumen is poorly understood. Concentrations of 5-HT in the colonic mucosa, colonic lumen, and feces were measured by HPLC in rats. To investigate whether intraluminal 5-HT accelerates colonic transit, 5-HT and 51 Cr were administered into the lumen of the proximal colon, and colonic transit was measured. To investigate whether 5-HT is released into the lumen, we used an ex vivo model of isolated vascularly and luminally perfused rat proximal colon. To investigate whether luminal 5-HT is involved in regulating stressinduced colonic motility, the distal colonic motility was recorded under the stress loading, and a 5-HT3 receptor antagonist (ondansetron, 10 Ϫ6 M, 0.5 ml) was administered intraluminally of the distal colon. Tissue content of 5-HT in the proximal colon (15.2 Ϯ 4.3 ng/mg wet tissue) was significantly higher than that in the distal colon (3.3 Ϯ 0.7 ng/mg wet tissue), while fecal content and luminal concentration of 5-HT was almost the same between the proximal and distal colon. Luminal administration of 5-HT (10 Ϫ6 -10 Ϫ5 M) significantly accelerated colonic transit. Elevation of intraluminal pressure by 10 cmH2O significantly increased the luminal concentration of 5-HT but not the vascular concentration of 5-HT. Stress-induced stimulation of the distal colonic motility was significantly attenuated by the luminal administration of ondansetron. These results suggest that luminally released 5-HT from EC cells plays an important role in regulating colonic motility in rats. enterochromaffin cells; distal colon; luminal pressure; restraint stress SEROTONIN (5-HT) IN THE GASTROINTESTINAL (GI) tract is involved in regulating GI motility. While 5-HT acts as a neurotransmitter of the enteric nervous system (15), the majority of 5-HT is stored in enterochromaffin (EC) cells of epithelial cells.EC cells have been considered to release 5-HT mainly into the blood vessels and/or intrinsic nerve terminal via a basolateral border (14). In contrast, others showed that 5-HT is also released into the intestinal lumen in response to vagal nerve stimulation (1,20), luminal acidification (25), and food intake (10). Immunoelectron microscopic study showed the anatomical evidence that 5-HT is released from EC cells in response to an increase of luminal pressure of the rat duodenum (12). However, the physiological role of released 5-HT into the GI lumen is poorly understood.In this study, we hypothesize that luminally released 5-HT from EC cells of the proximal colon is transferred distally with feces and stimulates motility of the distal colon, resulting in acceleration of colonic transit in rats. We also investigated the mechanism of luminal release of 5-HT of the rat proximal colon.There is accumulated evidence that a variety of stress stimulates colonic motility, colonic transit, and fecal pellet output (9,21,35,38,47). Stress-induced acceleration of colonic motor function...

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Regulatory mechanisms in endoluminal release of serotonin and substance P from feline jejunum

Cited by 24 publications

References 17 publications

Endogenous ghrelin and 5-HT regulate interdigestive gastrointestinal contractions in conscious rats

Endogenous ghrelin and 5-HT regulate interdigestive gastrointestinal contractions in conscious rats

Immunoelectron microscopic study of the luminal release of serotonin from rat enterochromaffin cells induced by high intraluminal pressure

Luminally released serotonin stimulates colonic motility and accelerates colonic transit in rats

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