Double Incretin Receptor Knockout (DIRKO) Mice Reveal an Essential Role for the Enteroinsular Axis in Transducing the Glucoregulatory Actions of DPP-IV Inhibitors

Diabetes

Volumn 53, Issue 5, 2004, Pages 1326-1335

  Hansotia, Tanya ^a   Baggio, Laurie L ^a   Delmeire, Dominique ^b   Hinke, Simon A ^b   Yamada, Yuichiro ^c   Tsukiyama, Katsushi ^c   Seino, Yutaka ^c   Holst, Jens J ^d   Schuit, Frans ^b,f   Drucker, Daniel J ^a,e  

^a UNIVERSITY OF TORONTO   (Canada)

^b FREE UNIVERSITY OF BRUSSELS   (Belgium)

^c KYOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e TORONTO GENERAL HOSPITAL   (Canada)

^f UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DIPEPTIDYL PEPTIDASE IV; ENZYME INHIBITOR; EXENDIN 4; GASTRIC INHIBITORY POLYPEPTIDE; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; HORMONE RECEPTOR; INCRETIN RECEPTOR; INSULIN; SYR 106124; UNCLASSIFIED DRUG; VALINE PYRROLIDIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GENE FUNCTION; GENETIC TRANSDUCTION; GLUCAGON BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; HYPOGLYCEMIA; INSULIN BLOOD LEVEL; INSULIN RELEASE; KNOCKOUT GENE; KNOCKOUT MOUSE; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PANCREAS PERFUSION; PRIORITY JOURNAL; UPREGULATION; WILD TYPE;

ANIMALS; ANTIGENS, CD26; ENZYME INHIBITORS; GLUCOSE; HOMEOSTASIS; INSULIN; INTESTINES; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGANIC CHEMICALS; PEPTIDES; PYRROLES; RECEPTORS, GASTROINTESTINAL HORMONE; RECEPTORS, GLUCAGON; VALINE; VENOMS;

EID: 20244385394     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.53.5.1326     Document Type: Article

References (51)

1. Creutzfeldt W: The incretin concept today. Diabetologia 16:75-85, 1979
2. Dupre J, Beck JC: Stimulation of release of insulin by an extract of intestinal mucosa. Diabetes 15:555-559, 1966
3. Dupre J, Ross SA, Watson D, Brown JC: Stimulation of insulin secretion by gastric inhibitory polypeptide in man. J Clin Endocrinol Metab 37:826-828, 1973
4. Kreymann B, Ghatei MA, Williams G, Bloom SR: Glucagon-like peptide-1 7-36: a physiological incretin in man. Lancet 2:1300-1304, 1987
5. Holst JJ, Orskov C, Nielsen OV, Schwartz TW: Truncated glucagon-like peptide I, an insulin-releasing hormone from the distal gut. FEBS Lett 211:169-174, 1987
6. Mojsov S, Weir GC, Habener JF: Insulinotropin: glucagon-like peptide I (7-37) co-encoded in the glucagon gene is a potent stimulator of insulin release in the perfused rat pancreas. J Clin Invest 79:616-619, 1987
7. Nauck M, Stockmann F, Ebert R, Creutzfeldt W: Reduced incretin effect in type 2 (non-insulin-dependent) diabetes. Diabetologia 29:46-52, 1986
8. Nauck MA, Heimesaat MM, Orskov C, Holst JJ, Ebert R, Creutzfeldt W: Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J Clin Invest 91:301-307, 1993
9. Vilsboll T, Krarup T, Deacon CF, Madsbad S, Holst JJ: Reduced postprandial concentrations of intact biologically active glucagon-like peptide 1 in type 2 diabetic patients. Diabetes 50:609-613, 2001
10. Tseng CC, Zhang XY, Wolfe MM: Effect of GIP and GLP-1 antagonists on insulin release in the rat. Am J Physiol 276:E1049-E1054, 1999
11. Baggio L, Kieffer TJ, Drucker DJ: GLP-1 but not GIP regulates fasting and non-enteral glucose clearance in mice. Endocrinology 141:3703-3709, 2000
12. Lewis JT, Dayanandan B, Habener JF, Kieffer TJ: Glucose-dependent insulinotropic polypeptide confers early phase insulin release to oral glucose in rats: demonstration by a receptor antagonist. Endocrinology 141:3710-3716, 2000
13. Miyawaki K, Yamada Y, Yano H, Niwa H, Ban N, Ihara Y, Kubota A, Fujimoto S, Kajikawa M, Kuroe A, Tsuda K, Hashimoto H, Yamashita T, Jomori T, Tashiro F, Miyazaki J, Seino Y: Glucose intolerance caused by a defect in the entero-insular axis: a study in gastric inhibitory polypeptide receptor knockout mice. Proc Natl Acad Sci USA 96:14843-14847, 1999
14. Pamir N, Lynn FC, Buchan AM, Ehses J, Hinke SA, Pospisilik JA, Miyawaki K, Yamada Y, Seino Y, McIntosh CH, Pederson RA: Glucose-dependent insulinotropic polypeptide receptor null mice exhibit compensatory changes in the enteroinsular axis. Am J Physiol Endocrinol Metab 284:E931-E939, 2003
15. Scrocchi LA, Brown TJ, MacLusky N, Brubaker PL, Auerbach AB, Joyner AL, Drucker DJ: Glucose intolerance but normal satiety in mice with a null mutation in the glucagon-like peptide receptor gene. Nat Med 2:1254-1258, 1996
16. Flamez D, Van Breuseghem A, Scrocchi LA, Quartier E, Pipeleers D, Drucker DJ, Schuit F: Mouse pancreatic β-cells exhibit preserved glucose competence after disruption of the glucagon-like peptide 1 receptor gene. Diabetes 47:646-652, 1998
17. Pederson RA, Satkunarajah M, McIntosh CH, Scrocchi LA, Flamez D, Schuit F, Drucker DJ, Wheeler MB: Enhanced glucose-dependent insulinotropic polypeptide secretion and insulinotropic action in glucagon-like peptide 1 receptor -/- mice. Diabetes 47:1046-1052, 1998
18. 2+ signaling in mouse pancreatic islets with GLP-1 receptor null phenotype. Diabetes 48:1979-1986, 1999
19. Kim JG, Baggio LL, Bridon DP, Castaigne JP, Robitaille MF, Jette L, Benquet C, Drucker DJ: Development and characterization of a glucagon-like peptide 1-albumin conjugate: the ability to activate the glucagon-like peptide 1 receptor in vivo. Diabetes 52:751-759, 2003
20. Krarup T, Madsbad S, Moody AJ, Regeur L, Faber OK, Holst JJ, Sestoft L: Diminished immunoreactive gastric inhibitory polypeptide response to a meal in newly diagnosed type I (insulin-dependent) diabetics. J Clin Endocrinol Metab 56:1306-1312, 1983
21. Deacon CF, Nauck MA, Meier J, Hucking K, Holst JJ: Degradation of endogenous and exogenous gastric inhibitory polypeptide in healthy and in type 2 diabetic subjects as revealed using a new assay for the intact peptide. J Clin Endocrinol Metab 85:3575-3581, 2000
22. Orskov C, Rabenhoj L, Wettergren A, Kofod H, Holst JJ: Tissue and plasma concentrations of amidated and glycine-extended glucagon-like peptide I in humans. Diabetes 43:535-539, 1994
23. Li Y, Hansotia T, Yusta B, Ris F, Halban PA, Drucker DJ: Glucagon-like peptide-1 receptor signaling modulates beta cell apoptosis. J Biol Chem 278:471-478, 2003
24. Scrocchi LA, Brown TJ, Drucker DJ: Leptin sensitivity in non-obese GLP-1 receptor-/- mice. Diabetes 46:2029-2034, 1997
25. -/- mice. Endocrinology 139:3127-3132, 1998
26. Orskov C, Holst JJ, Nielsen OV: Effect of truncated glucagon-like peptide-1 [proglucagon-(78-107) amide] on endocrine secretion from pig pancreas, antrum, and nonantral stomach. Endocrinology 123:2009-2013, 1988
27. Meier JJ, Gallwitz B, Siepmann N, Holst JJ, Deacon CF, Schmidt WE, Nauck MA: Gastric inhibitory polypeptide (GIP) dose-dependently stimulates glucagon secretion in healthy human subjects at euglycaemia. Diabetologia 46:798-801, 2003
28. Zawalich WS, Zawalich KC: Effects of protein kinase C inhibitors on insulin secretory responses from rodent pancreatic islets. Mol Cell Endocrinol 177:95-105, 2001
29. Siegel EG, Creutzfeldt W: Stimulation of insulin release in isolated rat islets by GIP in physiological concentrations and its relation to islet cyclic AMP content. Diabetologia 28:857-861, 1985
30. Holst JJ, Deacon CF: Inhibition of the activity of dipeptidyl-peptidase IV as a treatment for type 2 diabetes. Diabetes 47:1663-1670, 1998
31. Marguet D, Baggio L, Kobayashi T, Bernard AM, Pierres M, Nielsen PF, Ribel U, Watanabe T, Drucker DJ, Wagtmann N: Enhanced insulin secretion and improved glucose tolerance in mice lacking CD26. Proc Natl Acad Sci USA 97:6874-6879, 2000
32. Ahren B, Simonsson E, Larsson H, Landin-Olsson M, Torgeirsson H, Jansson PA, Sandqvist M, Bavenholm P, Efendic S, Eriksson JW, Dickinson S, Holmes D: Inhibition of dipeptidyl peptidase IV improves metabolic control over a 4-week study period in type 2 diabetes. Diabetes Care 25:869-875, 2002
33. Henriksen EJ, Jacob S, Fogt DL, Dietze GJ: Effect of chronic bradykinin administration on insulin action in an animal model of insulin resistance. Am J Physiol 275:R40-R45, 1998
34. Yang C, Chao J, Hsu WH: The effect of bradykinin on secretion of insulin, glucagon, and somatostatin from the perfused rat pancreas. Metabolism 46:1113-1115, 1997
35. Zhu L, Tamvakopoulos C, Xie D, Dragovic J, Shen X, Fenyk-Melody JE, Schmidt K, Bagchi A, Griffin PR, Thornberry NA, Sinha Roy R: The role of dipeptidyl peptidase IV in the cleavage of glucagon family peptides: in vivo metabolism of pituitary adenylate cyclase activating polypeptide-(1-38). J Biol Chem 278:22418-22423, 2003
36. Unger RH, Eisentraut AM: Entero-insular axis. Arch Int Med 123:261-266, 1969
37. Elrick H, Stimmler L, Hlad CJ, Arai Y: Plasma insulin responses to oral and intravenous glucose administration. J Clin Endocrinol Metab 24:1076-1082, 1964
38. Perley MJ, Kipnis DM: Plasma insulin responses to oral and intravenous glucose: studies in normal and diabetic subjects. J Clin Invest 46:1954-1962, 1967
39. Scrocchi LA, Marshall BA, Cook SM, Brubaker PL, Drucker DJ: Glucose homeostasis in mice with disruption of GLP-1 receptor signaling. Diabetes 47:632-639, 1998
40. Leiter EH: Mice with targeted gene disruptions or gene insertions for diabetes research: problems, pitfalls, and potential solutions. Diabetologia 45:296-308, 2002
41. Serre V, Dolci W, Scrocchi LA, Drucker DJ, Efrat S, Thorens B: Exendin-(9-39) as an inverse agonist of the murine GLP-1 receptor: implications for basal intracellular cAMP levels and b cell glucose competence. Endocrinology 139:4448-4454, 1998
42. Jamen F, Persson K, Bertrand G, Rodriguez-Henche N, Puech R, Bockaert J, Ahren B, Brabet P: PAC1 receptor-deficient mice display impaired insulinotropic response to glucose and reduced glucose tolerance. J Clin Invest 105:1307-1315, 2000
43. Moens K, Heimberg H, Flamez D, Huypens P, Quartier E, Ling Z, Pipeleers D, Gremlich S, Thorens B, Schuit F: Expression and functional activity of glucagon, glucagon-like peptide 1, and glucose-dependent insulinotropic peptide receptors in rat pancreatic islet cells. Diabetes 45:257-261, 1996
44. Huypens P, Ling Z, Pipeleers D, Schuit F. Glucagon receptors on human islet cells contribute to glucose competence of insulin release. Diabetologia 43:1012-1019, 2000
45. Deacon CF, Holst JJ: Dipeptidyl peptidase IV inhibition as an approach to the treatment and prevention of type 2 diabetes: a historical perspective. Biochem Biophys Res Commun 294:1-4, 2002
46. Drucker DJ: Therapeutic potential of dipeptidyl peptidase IV inhibitors for the treatment of type 2 diabetes. Expert Opin Investig Drugs 12:87-100, 2003
47. Mentlein R: Dipeptidyl-peptidase IV (CD26)-role in the inactivation of regulatory peptides. Regul Pept 85:9-24, 1999
48. Balkan B, Kwasnik L, Miserendino R, Holst JJ, Li X: Inhibition of dipeptidyl peptidase IV with NVP-DPP728 increases plasma GLP-1 (7-36 amide) concentrations and improves oral glucose tolerance in obese Zucker rats. Diabetologia 42:1324-1331, 1999
49. Deacon CF, Danielsen P, Klarskov L, Olesen M, Holst JJ: Dipeptidyl peptidase IV inhibition reduces the degradation and clearance of GIP and potentiates its insulinotropic and antihyperglycemic effects in anesthetized pigs. Diabetes 50:1588-1597, 2001
50. Hansotia T, Baggio L, Yamada Y, Tsukiyama S, Preitner F, Thorens B, Seino Y, Drucker DJ: Combined genetic disruption of dual incretin receptor signaling pathways reveals novel glucose lowering properties of DPP-IV inhibitors in mice (Abstract). Diabetes 52 (Suppl. 1):A77, 2003
51. Pospisilik JA, Stafford SG, Demuth HU, Brownsey R, Parkhouse W, Finegood DT, McIntosh CH, Pederson RA: Long-term treatment with the dipeptidyl peptidase IV inhibitor P32/98 causes sustained improvements in glucose tolerance, insulin sensitivity, hyperinsulinemia, and β-cell glucose responsiveness in VDF (fa/fa) Zucker rats. Diabetes 51:943-950, 2002