Bidirectional GPR119 Agonism Requires Peptide YY and Glucose for Activity in Mouse and Human Colon Mucosa

Endocrinology

Volumn 159, Issue 4, 2018, Pages 1704-1717

  Tough, Iain R ^a   Forbes, Sarah ^a   Herzog, Herbert ^b   Jones, Robert M ^c   Schwartz, Thue W ^d   Cox, Helen M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c ARENA PHARMACEUTICALS   (United States)

^d University of Copenhagen   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

2 MONOACYLGLYCEROL; AR 231453; AR 440006; FREE FATTY ACID 3; FREE FATTY ACID RECEPTOR 4; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 119; G PROTEIN COUPLED RECEPTOR 119 AGONIST; G PROTEIN COUPLED RECEPTOR 40; GLUCOSE; MELANOCORTIN 4 RECEPTOR; N OLEOYLDOPAMINE; N OLEOYLETHANOLAMINE; NEUROPEPTIDE Y1 RECEPTOR; PARTIAL AGONIST; PEPTIDE YY; RECEPTOR; UNCLASSIFIED DRUG; DOPAMINE; ENDOCANNABINOID; GPR119 PROTEIN, HUMAN; MONOACYLGLYCEROL; N-OLEOYLDOPAMINE; OLEIC ACID; OXADIAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELLULAR DISTRIBUTION; COLON MOTILITY; COLON MUCOSA; COMPARATIVE EFFECTIVENESS; CONTROLLED STUDY; DRUG POTENCY; DRUG RECEPTOR BINDING; EC50; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; ION TRANSPORT; MALE; MOUSE; NCTC CLONE 929 CELL LINE; NONHUMAN; PRIORITY JOURNAL; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; COLON; DRUG EFFECT; GASTROINTESTINAL MOTILITY; GENETICS; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; COLON; DOPAMINE; ENDOCANNABINOIDS; GASTROINTESTINAL MOTILITY; GLUCOSE; HUMANS; INTESTINAL MUCOSA; ION TRANSPORT; MICE; MICE, KNOCKOUT; MONOGLYCERIDES; OLEIC ACIDS; OXADIAZOLES; PEPTIDE YY; PYRIMIDINES; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 85044578940     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2017-03172     Document Type: Article

References (47)

1. Hansen HS, RosenkildeMM, Holst JJ, Schwartz TW. GPR119 as a fat sensor. Trends Pharmacol Sci. 2012;33(7):374-381.
2. Chu ZL, Jones RM, He H, Carroll C, Gutierrez V, Lucman A, Moloney M, Gao H, Mondala H, Bagnol D, Unett D, Liang Y, Demarest K, Semple G, Behan DP, Leonard J. A role for b-cellexpressed G protein-coupled receptor 119 in glycemic control by enhancing glucose-dependent insulin release. Endocrinology. 2007; 148(6):2601-2609.
3. Chu ZL, Carroll C, Alfonso J, Gutierrez V, He H, Lucman A, Pedraza M, Mondala H, Gao H, Bagnol D, Chen R, Jones RM, Behan DP, Leonard J. A role for intestinal endocrine cell-expressed GPR119 in glycemic control by enhancing GLP-1 and GIP release. Endocrinology. 2008;149(5):2038-2047.
4. Parker HE, Habib AM, Rogers GJ, Gribble FM, Reimann F. Nutrient-dependent secretion of glucose-dependent insulinotropic polypeptide from primary murine K cells. Diabetologia. 2009; 52(2):289-298.
5. Odori S, Hosoda K, Tomita T, Fujikura J, Kusakabe T, Kawaguchi Y, Doi R, Takaori K, Ebihara K, Sakai Y, Uemoto S, Nakao K. GPR119 expression in normal human tissues and islet cell tumors: evidence for its islet-gastrointestinal distribution, expression in pancreatic beta and alpha cells, and involvement in islet function. Metabolism. 2013;62(1):70-78.
6. Reimann F, Gribble FM. Mechanisms underlying glucosedependent insulinotropic polypeptide and glucagon-like peptide-1 secretion. J Diabetes Investig. 2016;7(S1):13-19.
7. Cornall LM, Mathai ML, Hryciw DH, McAinch AJ. Is GPR119 agonism an appropriate treatment modality for the safe amelioration of metabolic diseases? Expert Opin Investig Drugs. 2013; 22(4):487-498.
8. Cox HM, Tough IR, Woolston A-M, Zhang L, Nguyen AD, Sainsbury A, Herzog H. Peptide YY is critical for acylethanolamine receptor Gpr119-induced activation of gastrointestinal mucosal responses. Cell Metab. 2010;11(6):532-542.
9. Mace OJ, Schindler M, Patel S. The regulation of K-and L-cell activity by GLUT2 and the calcium-sensing receptor CasR in rat small intestine. J Physiol. 2012;590(12):2917-2936.
10. Patel S, Mace OJ, Tough IR, White J, Cock TA, Warpman Berglund U, Schindler M, Cox HM. Gastrointestinal hormonal responses on GPR119 activation in lean and diseased rodent models of type 2 diabetes. Int J Obes. 2014;38(10):1365-1373.
11. Ritter K, Buning C, Halland N, Pöverlein C, Schwink L. G Proteincoupled receptor 119 (GPR119) agonists for the treatment of diabetes: recent progress and prevailing challenges. J Med Chem. 2016;59(8):3579-3592.
12. Ekberg JH, Hauge M, Kristensen LV, Madsen AN, Engelstoft MS, Husted AS, Sichlau R, Egerod KL, Timshel P, Kowalski TJ, Gribble FM, Reiman F, Hansen HS, Howard AD, Holst B, Schwartz TW. GPR119, a major enteroendocrine sensor of dietary triglyceride metabolites co-acting in synergy with FFA1 (GPR40). Endocrinology. 2016;157(12):4561-4569.
13. Buzard DJ, Lehmann J, Han S, Jones RM. GPR119 agonists 2009-2011. Pharm Pat Anal. 2012;1(3):285-299.
14. Huan Y, Jiang Q, Li G, Bai G, Zhou T, Liu S, Li C, Liu Q, Sun S, Yang M, Guo N, Wang X, Wang S, Liu Y, Wang G, Huang H, Shen Z. The dual DPP4 inhibitor and GPR119 agonist HBK001 regulates glycemic control and beta cell function ex and in vivo. Sci Rep. 2017;7(1):4351-4362.
15. Joshi S, Tough IR, Cox HM. Endogenous PYY and GLP-1 mediate l-glutamine responses in intestinal mucosa. Br J Pharmacol. 2013; 170(5):1092-1101.
16. Moodaley R, Smith DM, Tough IR, Schindler M, Cox HM. Agonism of free fatty acid receptors 1 and 4 generates peptide YYmediated inhibitory responses in mouse colon. Br J Pharmacol. 2017;174(23):4508-4522.
17. Engelstoft MS, Norn C, Hauge M, Holliday ND, Elster L, Lehmann J, Jones RM, Frimurer TM, Schwartz TW. Structural basis for constitutive activity and agonist-induced activation of the enteroendocrine fat sensor GPR119. Br J Pharmacol. 2014;171(24): 5774-5789.
18. Hassing HA, Fares S, Larsen O, Pad H, Hauge M, Jones RM, Schwartz TW, Hansen HS, Rosenkilde MM. Biased signaling of lipids and allosteric actions of synthetic molecules for GPR119. Biochem Pharmacol. 2016;119:66-75.
19. Habib AM, Richards P, Rogers GJ. Reimann F, Gribble FM. Colocalisation and secretion of GLP-1 and PYY from primary cultured human L cells. Diabetologia. 2013;56(6):1413-1416.
20. Cox HM, Tough IR. Neuropeptide Y, Y1, Y2 and Y4 receptors mediate Y agonist responses in isolated human colon mucosa. Br J Pharmacol. 2002;135(6):1505-1512.
21. Hyland NP, Sjöberg F, Tough IR, Herzog H, Cox HM. Functional consequences of neuropeptide Y Y 2 receptor knockout and Y2 antagonism in mouse and human colonic tissues. Br J Pharmacol. 2003;139(4):863-871.
22. Tough IR, Holliday ND, Cox HM. Y(4) receptors mediate the inhibitory responses of pancreatic polypeptide in human and mouse colon mucosa. J Pharmacol Exp Ther. 2006;319(1):20-30.
23. Cox HM. Neuroendocrine peptide mechanisms controlling intestinal epithelial function. Curr Opin Pharmacol. 2016;31: 50-56.
24. Overton HA, Babbs AJ, Doel SM, Fyfe MC, Gardner LS, Griffin G, Jackson HC, Procter MJ, Rasamison CM, Tang-Christensen M, Widdowson PS, Williams GM, Reynet C. Deorphanization of a G protein-coupled receptor for oleoylethanolamide and its use in the discovery of small-molecule hypophagic agents. Cell Metab. 2006; 3(3):167-175.
25. Lauffer LM, Iakoubov R, Brubaker PL. GPR119 is essential for oleoylethanolamide-induced glucagon-like peptide-1 secretion from the intestinal enteroendocrine L-cell. Diabetes. 2009;58(5): 1058-1066.
26. Lan H, Vassileva G, Corona A, Liu L, Baker H, Golovkov A, Abbondanzo SJ, Hu W, Yang S, Ning Y, Del Vecchio RA, Poulet F, Laverty M, Gustafson EL, Hedrick JA, Kowalski TJ. GPR119 is required for physiological regulation of glucagon-like peptide-1 secretion but not for metabolic homeostasis. J Endocrinol. 2009; 201(2):219-230.
27. Moss CE, Glass LL, Diakogiannaki E, Pais R, Lenaghan C, Smith DM, Wedin M, Bohlooly-Y M, Gribble FM, Reimann F. Lipid derivatives activate GPR119 and trigger GLP-1 secretion in primary murine L-cells. Peptides. 2016;77:16-20.
28. Flock G, Holland D, Seino Y, Drucker DJ. GPR119 regulates murine glucose homeostasis through incretin receptordependent and independent mechanisms. Endocrinology. 2011; 152(2):374-383.
29. Panaro BL, Flock GB, Campbell JE, Beaudry JL, Cao X, Drucker DJ. b-Cell inactivation of GPR119 unmasks incretin dependence of GPR119-mediated glucoregulation. Diabetes. 2017;66(6): 1626-1635.
30. Panaro BL, Tough IR, Engelstoft MS, Matthews RT, Digby GJ, Møller CL, Svendsen B, Gribble F, Reimann F, Holst JJ, Holst B, Schwartz TW, Cox HM, Cone RD. The melanocortin-4 receptor is expressed in enteroendocrine L cells and regulates the release of peptide YY and glucagon-like peptide 1 in vivo. Cell Metab. 2014; 20(6):1018-1029.
31. Tough IR, Forbes S, Tolhurst R, Ellis M, Herzog H, Bornstein JC, Cox HM. Endogenous peptide YY and neuropeptide Y inhibit colonic ion transport, contractility and transit differentially via Y1 and Y2 receptors. Br J Pharmacol. 2011;164(2b):471-484.
32. Hauge M, Ekberg JP, Engelstoft MS, Timshel P, Madsen AN, Schwartz TW. Gq and Gs signaling acting in synergy to control GLP-1 secretion. Mol Cell Endocrinol. 2017;449:64-73.
33. Brighton CA, Rievaj J, Kuhre RE, Glass LL, Schoonjans K, Holst JJ, Gribble FM, Reimann F. Bile acids trigger GLP-1 release predominantly by accessing basolaterally located G-protein coupled bile acid receptors. Endocrinology. 2015;156(11): 3961-3970.
34. Forbes S, Stafford S, Coope G, Heffron H, Real K, Newman R, Davenport R, Barnes M, Grosse J, Cox H. Selective FFA2 agonism appears to act via intestinal PYY to reduce transit and food intake, but does not improve glucose tolerance in mouse models. Diabetes. 2015;64(11):3763-3771.
35. Chu ZL, Carroll C, Chen R, Alfonso J, Gutierrez V, He H, Lucman A, Xing C, Sebring K, Zhou J, Wagner B, Unett D, Jones RM, Behan DP, Leonard J. N-Oleoyldopamine enhances glucose homeostasis through the activation of GPR119. Mol Endocrinol. 2010;24(1): 161-170.
36. Hassing HA, EngelstoftMS, Sichlau RM, Madsen AN, Rehfeld JF, Pedersen J, Jones RM, Holst JJ, Schwartz TW, Rosenkilde MM, Hansen HS. Oral 2-oleyl glyceryl ether improves glucose tolerance in mice through the GPR119 receptor. Biofactors. 2016;42(6): 665-673.
37. Husted AS, Trauelsen M, Rudenko O, Hjorth SA, Schwartz TW. GPCR-mediated signaling of metabolites. Cell Metab. 2017;25(4): 777-796.
38. Norn C, Hauge M, Engelstoft MS, Kim SH, Lehmann J, Jones RM, Schwartz TW, Frimurer TM. Mutation-guided unbiased modeling of the fat sensor GPR119 for high-yield agonist screening. Structure. 2015;23(12):2377-2386.
39. Binder HJ, Sandle GI. Electrolyte transport in the mammalian colon. In: Johnson LR, ed. Physiology of the Gastrointestinal Tract. 2nd ed. New York, NY: Raven; 1994:2133-2171.
40. Cox HM, Pollock EL, Tough IR, Herzog H. Multiple Y receptors mediate pancreatic polypeptide responses in mouse colon mucosa. Peptides. 2001;22(3):445-452.
41. Tough IR, Moodaley R, Cox HM. Mucosal glucagon-like peptide 1 (GLP-1) responses are mediated by calcitonin gene-related peptide (CGRP) in the mouse colon and both peptide responses are areaspecific. Neurogastroenterol Motil. 2018;30(1):e13149.
42. Cho HJ, Kosari S, Hunne B, Callaghan B, Rivera LR, Bravo DM, Furness JB. Differences in hormone localisation patterns of K and L type enteroendocrine cells in the mouse and pig small intestine and colon. Cell Tissue Res. 2015;359(2):693-698.
43. Cvijanovic N, Isaacs NJ, Rayner CK, Feinle-Bisset C, Young RL, Little TJ. Duodenal fatty acid sensor and transporter expression following acute fat exposure in healthy lean humans. Clin Nutr. 2017;36(2):564-569.
44. Hansen KB, Rosenkilde MM, Knop FK, Wellner N, Diep TA, Rehfeld JF, Andersen UB, Holst JJ, Hansen HS. 2-Oleoyl glycerol is a GPR119 agonist and signals GLP-1 release in humans. J Clin Endocrinol Metab. 2011;96(9):E1409-E1417.
45. Nøhr MK, Pedersen MH, Gille A, Egerod KL, Engelstoft MS, Husted AS, Sichlau RM, Grunddal KV, Poulsen SS, Han S, Jones RM, Offermanns S, Schwartz TW. GPR41/FFAR3 and GPR43/ FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes. Endocrinology. 2013;154(10):3552-3564.
46. Cohen LJ, Esterhazy D, Kim SH, Lemetre C, Aguilar RR, Gordon EA, Pickard AJ, Cross JR, Emiliano AB, Han SM, Chu J, Vila-Farres X, Kaplitt J, Rogoz A, Calle PY,HunterC, Bitok JK, Brady SF. Commensal bacteria make GPCR ligands that mimic human signalling molecules. Nature. 2017;549(7670):48-53.
47. Ullmer C, Alvarez Sanchez R, Sprecher U, Raab S, Mattei P, Dehmlow H, Sewing S, Iglesias A, Beauchamp J, Conde-Knape K. Systemic bile acid sensing by G protein-coupled bile acid receptor 1 (GPBAR1) promotes PYY and GLP-1 release. Br J Pharmacol. 2013;169(3):671-684.