Gastroenterology
Volume 137, Issue 2 , Pages 598-606.e2 , August 2009

Release of Endogenous Opioids From Duodenal Enteroendocrine Cells Requires Trpm5

Received 24 September 2008 ,Accepted 23 February 2009.

References 

  1. Rindi G, Leiter AB, Kopin AS, et al. The “normal” endocrine cell of the gut: changing concepts and new evidences. Ann N Y Acad Sci. 2004;1014:1–12
  2. Strader AD, Woods SC. Gastrointestinal hormones and food intake. Gastroenterology. 2005;128:175–191
  3. Cummings DE, Overduin J. Gastrointestinal regulation of food intake. J Clin Invest. 2007;117:13–23
  4. Zhang Y, Hoon MA, Chandrashekar J, et al. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell. 2003;112:293–301
  5. Damak S, Rong M, Yasumatsu K, et al. Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses. 2006;31:253–264
  6. Kaske S, Krasteva G, Konig P, et al. TRPM5, a taste-signaling transient receptor potential ion-channel, is a ubiquitous signaling component in chemosensory cells. BMC Neurosci. 2007;8:49
  7. Bezençon C, le Coutre J, Damak S. Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses. 2007;32:41–49
  8. Lin W, Ogura T, Margolskee RF, et al. TRPM5-expressing solitary chemosensory cells respond to odorous irritants. J Neurophysiol. 2008;99:1451–1460
  9. Bodnar RJ, Klein GE. Endogenous opiates and behavior: 2005. Peptides. 2006;27:3391–3478
  10. Parton LE, Ye CP, Coppari R, et al. Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity. Nature. 2007;449:228–232
  11. Appleyard SM, Hayward M, Young JI, et al. A role for the endogenous opioid beta-endorphin in energy homeostasis. Endocrinology. 2003;144:1753–1760
  12. Coll AP, Farooqi S, Challis BG, et al. Proopiomelanocortin and energy balance: insights from human and murine genetics. J Clin Endocrinol Metab. 2004;89:2557–2562
  13. Vaccarino AL, Kastin AJ. Endogenous opiates: 2000. Peptides. 2001;22:2257–2328
  14. Smith TW, Hughes J, Kosterlitz HW, et al. Enkephalins: isolation, distribution and function. In:  Kosterlitz HW editors. Opiates and endogenous opiate peptides. Amsterdam, The Netherlands: Elsevier/North-Holland Biomedical Press; 1986;p. 57–62
  15. Tari A, Miyachi Y, Sumii K, et al. Beta-endorphin-like immunoreactivity in normal mucosa, muscle layer, adenocarcinoma, and polyp of the colon. Dig Dis Sci. 1988;33:429–434
  16. Lolova IS, Davidoff MS, Itzev DE. Histological and immunocytochemical data on the differentiation of intestinal endocrine cells in human fetus. Acta Physiol Pharmacol Bulg. 1998;23:61–71
  17. Holzer P. Opioids and opioid receptors in the enteric nervous system: from a problem in opioid analgesia to a possible new prokinetic therapy in humans. Neurosci Lett. 2004;361:192–195
  18. Sandhu BK, Phillips AD, Milla PJ. Opiate agonists and enterotoxin. Biochem Soc Trans. 1984;12:205–208
  19. Matsumura M, Saito S, Fujino M. Effects of solution of low pH and taurocholate on release of beta-endorphin-like immunoreactivity from human duodenal mucosa in vitro. Regul Pept. 1982;3:173–181
  20. Matsumura M, Wada H, Saito S. Effect of solution of low pH on release of beta-endorphin-like immunoreactivity and ACTH-like reactivity from human gastric antral mucosa in vitro. Gastroenterol Jpn. 1983;18:210–215
  21. Money SR, Petroianu A, Gintzler AR, et al. Meal-stimulated release of Methionie-enkephalin into the canine jejunal lumen. J Clin Invest. 1988;81:822–825
  22. Shimizu I, Matsumura M, Hirota M, et al. Beta-endorphin in the human gallbladder. Regul Pept. 1986;16:331–338
  23. Nakazato M. Guanylin family: new intestinal peptides regulating electrolyte and water homeostasis. J Gastroenterol. 2001;36:219–225
  24. Forte LR. Uroguanylin and guanylin peptides: pharmacology and experimental therapeutics. Pharmacol Ther. 2004;104:137–162
  25. Sindić A, Schlatter E. Cellular effects of guanylin and uroguanylin. J Am Soc Nephrol. 2006;17:607–616
  26. Clapp TR, Medler KF, Damak S, et al. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol. 2006;4:7
  27. Sbarbati A, Osculati F. A new fate for old cells: brush cells and related elements. J Anat. 2005;206:349–358
  28. Sbarbati A, Osculati F. The taste cell-related diffuse chemosensory system. Prog Neurobiol. 2005;75:295–307
  29. Morroni M, Cangiotti AM, Cinti S. Brush cells in the human duodenojejunal junction: an ultrastructural study. J Anat. 2007;211:125–131
  30. Orwoll ES, Kendall JW. Beta-endorphin and adrenocorticotropin in extrapituitary sites: gastrointestinal tract. Endocrinology. 1980;107:438–442
  31. O'Donohue TL, Dorsa DM. The opiomelanotropinergic neuronal and endocrine systems. Peptides. 1982;3:353–395
  32. Liu D, Zhang Z, Liman ER. Extracellular acid block and acid-enhanced inactivation of the Ca2+-activated cation channel TRPM5 involve residues in the S3-S4 and S5-S6 extracellular domains. J Biol Chem. 2005;280:20691–20699
  33. Sato A, Miyoshi S. Fine structure of tuft cells of the main excretory duct epithelium in the rat submandibular gland. Anat Rec. 1997;248:325–331
  34. Bezençon C, Fürholz A, Raymond F, et al. Murine intestinal cells expressing Trpm5 are mostly brush cells and express markers of neuronal and inflammatory cells. Comp Neurol. 2008;509:514–525
  35. Lin H, Elashoff JD, Kwok GM, et al. Stimulation of duodenal motility by hyperosmolar mannitol depends on local osmoreceptor control. Am J Physiol. 1994;266:G940–G943
  36. Bubenik GA. Thirty four years since the discovery of gastrointestinal melatonin. J Physiol Pharmacol. 2008;59(Suppl 2):33–51
  37. Shimizu M, Son DO. Food-derived peptides and intestinal functions. Curr Pharm Des. 2007;13:885–895
  38. Iwan M, Jarmołowska B, Bielikowicz K, et al. Transport of micro-opioid receptor agonists and antagonist peptides across Caco-2 monolayer. Peptides. 2008;29:1042–1047
  39. Lee HJ, Amidon GL. The effect of enzyme inhibitor and absorption site following [D-ala2, D-leu5]enkephalin oral administration in rats. Biopharm Drug Dispos. 2002;23:131–141
  40. Roberts PR, Burney JD, Black KW, et al. Effect of chain length on absorption of biologically active peptides from the gastrointestinal tract. Digestion. 1999;60:332–337
  41. Karsdal MA, Byrjalsen I, Riis BJ, et al. Optimizing bioavailability of oral administration of small peptides through pharmacokinetic and pharmacodynamic parameters: the effect of water and timing of meal intake on oral delivery of salmon calcitonin. BMC Clin Pharmacol. 2008;8:5
  42. Builders PF, Kunle OO, Okpaku LC, et al. Preparation and evaluation of mucinated sodium alginate microparticles for oral delivery of insulin. Eur J Pharm Biopharm. 2008;70:777–783
  43. Kamei N, Morishita M, Chiba H, et al. Complexation hydrogels for intestinal delivery of interferon beta and calcitonin. J Control Release. 2009;134:98–102
  44. Pezalla PD, Lis M, Seidah NG, et al. Lipotropin, melanotropin and endorphin: in vivo catabolism and entry into cerebrospinal fluid. Can J Neurol Sci. 1978;5:183–188
  45. Quito FL, Seybold VS, Brown DR. Opiate binding sites in mucosa of pig small intestine. Life Sci. 1991;49:PL219–PL222
  46. Nano JL, Fournel S, Rampal P. Characterization of delta-opioid receptors and effect of enkephalins on IRD 98 rat epithelial intestinal cell line. Pflugers Arch. 2000;439:547–554
  47. Nylund G, Pettersson A, Bengtsson C, et al. Functional expression of mu-opioid receptors in the human colon cancer cell line, HT-29, and their localization in human colon. Dig Dis Sci. 2008;53:461–466
  48. Flemström G, Kivilaakso E, Briden S, et al. Gastroduodenal bicarbonate secretion in mucosal protection (Possible role of vasoactive intestinal peptide and opiates). Dig Dis Sci. 1985;30:63S–68S
  49. Flemstrom G, Jedstedt G, Nylander O. Beta-endorphin and enkephalins stimulate duodenal mucosal alkaline secretion in the rat in vivo. Gastroenterology. 1986;90:368–372
  50. Forte LR. Guanylin regulatory peptides: structures, biological activities mediated by cyclic GMP and pathobiology. Regul Pept. 1999;81:25–39
  51. Anseloni VC, Ren K, Dubner R, et al. A brainstem substrate for analgesia elicited by intraoral sucrose. Neuroscience. 2005;133:231–243
  52. Anseloni VC, Weng HR, Terayama R, et al. Age-dependency of analgesia elicited by intraoral sucrose in acute and persistent pain models. Pain. 2002;97:93–103
  53. Okan F, Coban A, Ince Z, et al. Analgesia in preterm newborns: the comparative effects of sucrose and glucose. Eur J Pediatr. 2007;166:1017–1024
  54. Vukavic T. Intestinal absorption of IgA in the newborn. J Pediatr Gastroenterol Nutr. 1983;2:248–251
  55. Vukavić T. Timing of the gut closure. J Pediatr Gastroenterol Nutr. 1984;3:700–703
  56. Catassi C, Bonucci A, Coppa GV, et al. Intestinal permeability changes during the first month: effect of natural versus artificial feeding. J Pediatr Gastroenterol Nutr. 1995;21:383–386
  57. Van de Perre P. Transfer of antibody via mother's milk. Vaccine. 2003;21:3374–3376
  58. Vaarala O, Atkinson MA, Neu J. The “perfect storm” for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes. 2008;57:2555–2562
  59. Callahan MJ. Irritable bowel syndrome neuropharmacology (A review of approved and investigational compounds). J Clin Gastroenterol. 2002;35:S58–S67
  60. Philippe D, Chakass D, Thuru X, et al. Mu opioid receptor expression is increased in inflammatory bowel diseases: implications for homeostatic intestinal inflammation. Gut. 2006;55:815–823
  61. Verma-Gandhu M, Verdu EF, Bercik P, et al. Visceral pain perception is determined by the duration of colitis and associated neuropeptide expression in the mouse. Gut. 2007;56:358–364
  62. Pol O, Palacio JR, Margarita M, et al. The expression of delta- and kappa-opioid receptor is enhanced during intestinal inflammation in mice. J Pharmacol Exp Ther. 2003;306:455–462

 Conflicts of interest Dr Margolskee has a personal financial interest in the form of stock ownership in the Redpoint Bio company, receives consulting fees from the Redpoint Bio company, and is an inventor on patents and patent applications that have been licensed to the Redpoint Bio company. The remaining authors disclose no conflicts.

 Funding Supported in part by National Institutes of Health grants DC007399 and DK073248 (to B.M.) and DC03055 (to R.F.M.).

PII: S0016-5085(09)00356-4

doi: 10.1053/j.gastro.2009.02.070

Gastroenterology
Volume 137, Issue 2 , Pages 598-606.e2 , August 2009

Article Tools

* Image Usage & Resolution