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Peptone Stimulates CCK-Releasing Peptide Secretion by Activating Intestinal Submucosal Cholinergic Neurons

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Peptone Stimulates CCK-Releasing Peptide Secretion by Activating Intestinal Submucosal Cholinergic Neurons Peptone stimulates CCK-releasing peptide secretion by activating intestinal submucosal cholinergic neurons. Y Li, C Owyang J Clin Invest. 1996;97(6):1463-1470. https://doi.org/10.1172/JCI118568. Research Article In this study we tested the hypothesis that peptone in the intestine stimulates the secretion of the CCK-releasing peptide (CCK-RP) which mediates CCK secretion, and examined the enteric neural circuitry responsible for CCK-RP secretion. We used a "donor-recipient" rat intestinal perfusion model to quantify the CCK-RP secreted in response to nutrient stimulation. Infusion of concentrated intestinal perfusate collected from donor rat perfused with 5% peptone caused a 62 +/- 10% increase in protein secretion and an elevation of plasma CCK levels to 6.9 +/- 1.8 pM in the recipient rat. The stimulatory effect of the intestinal washings was abolished when the donor rats were pretreated with atropine or hexamethonium but not with guanethidine or vagotomy. Mucosal application of lidocaine but not serosal application of benzalkonium chloride which ablates the myenteric neurons in the donor rats also abolished the stimulatory action of the intestinal washings. Furthermore, treatment of the donor rats with a 5HT3 antagonist and a substance P antagonist also prevented the secretion of CCK-RP. These observations suggest that peptone in the duodenum stimulates serotonin release which activates the sensory substance P neurons in the submucous plexus. Signals are then transmitted to cholinergic interneurons and to epithelial CCK-RP containing cells via cholinergic secretomotor neurons. This enteric neural circuitry which is responsible for the secretion of CCK-RP may in turn play […] Find the latest version: https://jci.me/118568/pdf Peptone Stimulates CCK-releasing Peptide Secretion by Activating Intestinal Submucosal Cholinergic Neurons Ying Li and Chung Owyang The University of Michigan Medical Center, Department of Internal Medicine, Ann Arbor, Michigan 48109 Abstract Recently it was reported that the release of CCK into the circulation is mediated by a “CCK-releasing peptide” (CCK- In this study we tested the hypothesis that peptone in the in- RP) secreted into the intestine of the rat (2, 3). When trypsin is testine stimulates the secretion of the CCK-releasing pep- present, this peptide is cleaved and inactivated. It has been tide (CCK-RP) which mediates CCK secretion, and exam- proposed that this newly discovered CCK-RP may also act as a ined the enteric neural circuitry responsible for CCK-RP mediator of pancreatic enzyme secretion in response to dietary secretion. We used a “donor-recipient” rat intestinal perfu- protein (4). Dietary protein in the intestine competes for sion model to quantify the CCK-RP secreted in response to trypsin (1), which would otherwise inactivate the CCK-RP. nutrient stimulation. Infusion of concentrated intestinal The resulting increase of active CCK-RP in the intestine re- perfusate collected from donor rat perfused with 5% pep- leases CCK and stimulates pancreatic enzyme secretion. On tone caused a 62Ϯ10% increase in protein secretion and an the other hand, if a dietary protein such as bovine serum albu- elevation of plasma CCK levels to 6.9Ϯ1.8 pM in the recipi- min or lactalbumin is a poor substrate for pancreatic proteases, ent rat. The stimulatory effect of the intestinal washings it will not prevent proteolytic inactivation of the CCK-RP and was abolished when the donor rats were pretreated with at- therefore will not evoke an increase in CCK secretion (1). ropine or hexamethonium but not with guanethidine or vag- Hence the ability of intact protein to stimulate CCK release otomy. Mucosal application of lidocaine but not serosal and pancreatic secretion has been attributed to its ability to application of benzalkonium chloride which ablates the my- bind with pancreatic proteases and reverse protease-induced enteric neurons in the donor rats also abolished the stimula- feedback inhibition of CCK release. In a recent study, how- tory action of the intestinal washings. Furthermore, treat- ever (5) it was reported that peptic digests of lactalbumin not ment of the donor rats with a 5HT3 antagonist and a native lactalbumin were potent stimuli of pancreatic secretion. substance P antagonist also prevented the secretion of It is conceivable that digests of protein in the intestine may CCK-RP. These observations suggest that peptone in the stimulate the secretion of CCK-RP. To test this hypothesis we duodenum stimulates serotonin release which activates the used a “donor-recipient” rat intestinal perfusion model that sensory substance P neurons in the submucous plexus. Sig- has been previously used to identify the CCK-RP (2) and ex- nals are then transmitted to cholinergic interneurons and to amined the ability of peptone, a pancreatic protease digest of epithelial CCK-RP containing cells via cholinergic secreto- protein in the intestine, to stimulate the secretion of CCK-RP. motor neurons. This enteric neural circuitry which is re- Furthermore, we examined the enteric neural circuitry mediat- sponsible for the secretion of CCK-RP may in turn play an ing CCK-RP secretion. The relative importance of extrinsic important role in the postprandial release of CCK. (J. Clin. versus intrinsic neural pathways were studied and the location Invest. 1996. 97:1463–1470.) Key words: substance P • sero- of the local neural plexus identified. In addition, we delineated tonin • enteric nervous system • cholecystokinin • cholecys- the individual components of the enteric neural circuitry which tokinin-releasing peptide mediates CCK-RP secretion. Introduction Methods Cholecystokinin (CCK)1 plays an important role in the media- Materials tion of postprandial pancreatic secretion and gallbladder con- traction. In the rat, protein is the major dietary intestinal stim- The following were purchased from Sigma Chemical Co. (St. Louis, l ulus for CCK release (1). Little, however, is known about the MO): Peptone, maltose, -amino acids, atropine sulfate, hexametho- nium and benzalkonium chloride. mechanisms regulating CCK secretion. Animal preparation Male Sprague-Dawley rats, weighing between 250 and 300 grams, Address correspondence to Chung Owyang, M.D., The University of were fasted overnight and anesthetized with a mixture of xylazine Michigan Medical Center, 3912 Taubman Center, Box 0362, Ann Ar- and ketamine (13 and 87 mg/kg body wt, respectively). Supplemental bor, MI 48109-0362. Phone: 313-936-4785; FAX: 313-036-7392. doses were used every 2 h as needed to maintain adequate anesthesia. Received for publication 4 August 1995 and accepted in revised Through a midline incision, a polyethylene catheter was inserted into form 12 December 1995. the common bile pancreatic duct at the ampulla. A second catheter was placed in the duodenum, slightly above the ampulla for the intes- 1. Abbreviations used in this paper: CCK, cholecystokinin; RP, releas- tinal perfusion of bile pancreatic juice. The abdominal wound was ing peptide. covered with a saline gauge and the animal body temperature was monitored by a rectal thermal probe and maintained at 37ЊC with a J. Clin. Invest. heating pad. After 60 min of stabilization, combined bile and pancre- © The American Society for Clinical Investigation, Inc. atic secretions were collected every 15 min. The volume was mea- 0021-9738/96/03/1463/08 $2.00 sured, and an aliquot was taken and diluted with distilled water for Volume 97, Number 6, March 1996, 1463–1470 protein determination. The remainder of the undiluted bile pancre- Peptone Stimulates Cholecystokinin-releasing Peptide 1463 atic juice was returned to the intestine via the duodenal cannula dur- acute bilateral subdiaphragmatic vagotomy was performed in donor ing the next collection period. Bile pancreatic juice protein was mea- rats. Through a midline incision of the abdominal wall, the stomach sured spectrophotometrically using the assay method of Bradford (6). was carefully manipulated to expose the esophagus. The subdia- Our previous study (7) has confirmed that the increase in protein out- phragmatic vagal trunks were exposed halfway between the dia- put in the bile pancreatic juice following CCK-8 stimulation mainly phragm and the gastric cardia. Both anterior and posterior trunks of reflected protein from the pancreatic source. Biliary juice protein did the vagal nerves were transected. For control experiments, the ab- not increase with CCK stimulation. dominal vagal nerves were exposed but not cut. Intraluminal peptone perfusion studies were performed following acute vagotomy. Pancre- atic amylase output and plasma CCK levels were monitored in the re- Experimental protocols cipient rats following the same protocol as described earlier. Effect of intraluminal nutrients on CCK-RP secretion after 5-h diver- Effects of mucosal anesthestic and serosal application of benzalko- sion of BPJ. To investigate the effect of intraluminal peptone on nium choloride (BAC) on peptone-stimulated CCK-RP secretion. CCK-RP secretion, we utilized the donor-recipient rat model de- The enteric nervous system is composed of the myenteric and submu- scribed previously (2). The common bile-pancreatic duct was cannu- cous plexuses. To investigate if the submucous plexus is involved in lated at the ampulla for diversion of bile pancreatic juice. Two cannu- the mediation of CCK-RP secretion, 1% lidocaine was used as a topi- las were placed into the small bowel: one in the proximal duodenum cal anesthetic (2 ml/kg bolus plus 0.2 ml/min for 5 min at hourly inter- for the infusion of saline or nutrient solutions and the other in the je- vals intraduodenally) ten minutes before the intraduodenal perfusion junum 20 cm distal to the ligament of Tretz for collection of intestinal of 5% peptone. This method has previously been shown to inhibit the perfusates. We have shown previously that diversion of bile pancre- increase in superior mesenteric artery blood flow evoked by in- atic juice from the intestine resulted in a marked increase in plasma traduodenal perfusion of 0.1N HCl (10). To investigate if myeteric CCK levels and pancreatic secretion.
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