Brain glucagon-like peptide-1 increases insulin secretion and muscle insulin resistance to favor hepatic glycogen storage

Journal of Clinical Investigation

Volumn 115, Issue 12, 2005, Pages 3554-3563

  Knauf, Claude ^a   Cani, Patrice D ^a,b   Perrin, Christophe ^a   Iglesias, Miguel A ^a   Maury, Jean François ^a   Bernard, Elodie ^a   Benhamed, Fadilha ^c   Grémeaux, Thierry ^d   Drucker, Daniel J ^e   Kahn, C Ronald ^f   Girard, Jean ^c   Tanti, Jean François ^d   Delzenne, Nathalie M ^b   Postic, Catherine ^c   Burcelin, Rémy ^a,g  

^a CNRS   (France)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c INSTITUT COCHIN   (France)

^d INSERM   (France)

^e UNIVERSITY OF TORONTO   (Canada)

^f Joslin Institute   (United States)

^g CHU RANGUEIL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EXENDIN 4; EXENDIN[9-39]; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 DERIVATIVE; GLUCAGON LIKE PEPTIDE 1 RECEPTOR AGONIST; GLUCAGON LIKE PEPTIDE 1 RECEPTOR ANTAGONIST; GLUCOSE; GLYCOGEN; INSULIN; INSULIN RECEPTOR; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; GLUCOSE UTILIZATION; GLYCOGEN ANALYSIS; GLYCOGEN LIVER LEVEL; GLYCOGEN SYNTHESIS; HORMONE ACTION; HYPERGLYCEMIA; INSULIN RELEASE; INSULIN RESISTANCE; KNOCKOUT MOUSE; LIVER; MOUSE; MUSCLE METABOLISM; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

EID: 31044456099     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI25764     Document Type: Article

References (62)

1. Szekely, M., and Szelenyi, Z. 2005. Regulation of energy balance by peptides: a review. Curr. Protein Pept. Sci. 6:327-353.
2. Kalra, S. 1997. Appetite and body weight regulation: is it all in the brain? Neuron. 19:220-230.
3. Kalra, S., et al. 1999. Interacting appetite-regulating pathways in the hypothalamic regulation of body weight. Endocr. Rev. 20:68-100.
4. Gyires, K. 2004. Neuropeptides and gastric mucosal homeostasis. Curr. Top Med. Chem. 4:63-73.
5. Lustig, R. 2003. Autonomic dysfunction of the beta-cell and the pathogenesis of obesity. Rev. Endocr. Metab. Disord. 4:23-32.
6. Oomura, Y., and Yoshimatsu, H. 1984. Neural network of glucose monitoring system. J. Auton. Nerv. Syst. 10:359-372.
7. Shimazu, T. 1987. Neuronal regulation of hepatic glucose metabolism in mammals. Diabetes Metab. Rev. 3:185-206.
8. Creutzfeldt, W. 1979. The incretin concept today. Diabetologia. 16:75-85.
9. Holst, J. 1994. Glucagon like peptide 1: a newly discovered gastrointestinal hormone. Gastroenterology. 107:1848-1855.
10. Holst, J.J., and Gromada, J. 2004. Role of incretin hormones in the regulation of insulin secretion in diabetic and nondiabetic humans. Am. J. Physiol. Endocrinol. Metab. 287:E199-E206.
11. Jin, S.L., et al. 1988. Distribution of glucagonlike peptide I (GLP-I), glucagon, and glicentin in the rat brain: an immunocytochemical study. J. Comp. Neurol. 271:519-532.
12. Yamamoto, H., et al. 2002. Glucagon-like peptide-1 receptor stimulation increases blood pressure and heart rate and activates autonomic regulatory neurons. J. Clin. Invest. 110:43-52. doi:10.1172/JCI200215595.
13. Turton, M.D., et al. 1996. A role for glucagon-like peptide-1 in the central regulation of feeding. Nature. 379:69-72.
14. Tang-Christensen, M., et al. 1996. Central administration of GLP-1-(7-36) amide inhibits food and water intake in rats. Am. J. Physiol. 271:R848-R856.
15. Liu, M., Seino, S., and Kirchgessner, A.L. 1999. Identification and characterization of glucoresponsive neurons in the enteric nervous system. J. Neurosci. 19:10305-10317.
16. Dyer, J., Vayro, S., and Shirazi-Beechey, S.P. 2003. Mechanism of glucose sensing in the small intestine. Biochem. Soc. Trans. 31:1140-1142.
17. Oomura, Y., Ono, T., Ooyama, H., and Wayner, M.J. 1969. Glucose and osmosensitive neurones of the rat hypothalamus. Nature. 222:282-284.
18. Orsini, J.C., Himmi, T., Wiser, A.K., and Perin, J. 1990. Local versus indirect action of glucose on the lateral hypothalamic neurons sensitive to glycemic level. Brain Res. Bull. 25:49-53.
19. Himmi, T., Boyer, A., and Orsini, J.C. 1998. Changes in lateral hypothalamic neuronal activity accompanying hyper and hypoglycemias. Physiol. Behav. 44:347-354.
20. Koyama, Y., et al. 2000. Evidence that carotid bodies play an important role in glucoregulation in vivo. Diabetes. 49:1434-1442.
21. Shimazu, T., and Amakawa, A. 1975. Regulation of glycogen metabolism in liver by the autonomic nervous system. Biochim. Biophys. Acta. 385:242-256.
22. Hevener, A., Bergman, R., and Donovan, C. 2000. Portal vein afferents are critical for the sympathoadrenal response to hypoglycemia. Diabetes. 49:8-12.
23. Hevener, A.L., Bergman, R.N., and Donovan, C.M. 1997. Novel glucosensor for hypoglycemic detection localized to the portal vein. Diabetes. 46:1521-1525.
24. Nishizawa, M., et al. 2000. The hepatic vagal reception of intraportal GLP-1 is via receptor different from the pancreatic GLP-1 receptor. J. Auton. Nerv. Syst. 80:14-21.
25. Burcelin, R., Da Costa, A., Drucker, D., and Thorens, B. 2001. Glucose competence of the hepatoportal vein sensor requires the presence of an activated glucagon-like peptide-1 receptor. Diabetes. 50:1720-1728.
26. Nishizawa, M., et al. 2003. Effect of intraportal glucagon-like peptide-1 on glucose metabolism in conscious dogs. Am. J. Physiol. Endocrinol. Metab. 284:E1027-E1036.
27. Dardevet, D., et al. 2004. Insulin-independent effects of GLP-1 on canine liver glucose metabolism: duration of infusion and involvement of hepatoportal region. Am. J. Physiol. Endocrinol. Metab. 287:E75-E81.
28. Obici, S., et al. 2001. Central melanocortin receptors regulate insulin action. J. Clin. Invest. 108:1079-1085. doi:10.1172/JCI200112954.
29. Deacon, C.F., et al. 1998. Dipeptidyl peptidase IV resistant analogues of glucagon-like peptide-1 which have extended metabolic stability and improved biological activity. Diabetologia. 41:271-278.
30. Burcelin, R., et al. 2003. GLUT4, AMP kinase, but not the insulin receptor, are required for hepatoportal glucose sensor-stimulated muscle glucose utilization. J. Clin. Invest. 111:1555-1562. doi:10.1172/JCI200316888.
31. Yamashita, H., et al. 2001. A glucose-responsive transcription factor that regulates carbohydrate metabolism in the liver. Proc. Natl. Acad. Sci. U. S. A. 98:9116-9121.
32. Dentin, R., et al. 2004. Hepatic glucokinase is required for the synergistic action of ChREBP and SREBP-1c on glycolytic and lipogenic gene expression. J. Biol. Chem. 279:20314-20326.
33. Postic, C., et al. 1993. The effects of hyperinsulinemia and hyperglycemia on GLUT4 and hexokinase II mRNA and protein in rat skeletal muscle and adipose tissue. Diabetes. 42:922-929.
34. Printz, R.L., Magnuson, M.A., and Granner, D.K. 1993. Mammalian glucokinase. Annu. Rev. Nutr. 13:463-496.
35. Kamohara, S., Burcelin, R., Halaas, J.L., Friedman, J.M., and Charron, M.J. 1997. Acute stimulation of glucose metabolism in mice by leptin treatment. Nature. 389:374-377.
36. Minokoshi, Y., et al. 2002. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature. 415:339-343.
37. Blazquez, E., et al. 1998. Glucagon-like peptide-1 (7-36) amide as a novel neuropeptide. Mol. Neurobiol. 18:157-173.
38. Wojtaszewski, J.F., Nielsen, J.N., and Richter, E.A. 2002. Invited review: effect of acute exercise on insulin signaling and action in humans. J. Appl. Physiol. 93:384-392.
39. Dominguez, J.E., et al. 2003. The anti-diabetic agent sodium tungstate activates glycogen synthesis through an insulin receptor-independent pathway. J. Biol. Chem. 278:42785-42794.
40. Kinzig, K.P., et al. 2003. CNS glucagon-like peptide-1 receptors mediate endocrine and anxiety responses to interoceptive and psychogenic stressors. J. Neurosci. 23:6163-6170.
41. Alvarez, E., Roncero, I., Chowen, J.A., Thorens, B., and Blazquez, E. 1996. Expression of the glucagon-like peptide-1 receptor gene in rat brain. J. Neurochem. 66:920-927.
42. Goke, R., Larsen, P.J., Mikkelsen, J.D., and Sheikh, S.P. 1995. Distribution of GLP-1 binding sites in the rat brain: evidence that exendin-4 is a ligand of brain GLP-1 binding sites. Eur. J. Neurosci. 7:2294-2300.
43. Shimizu, I., Hirota, M., Ohboshi, C., and Shima, K. 1987. Identification and localization of glucagon-like peptide-1 and its receptor in rat brain. Endocrinology. 121:1076-1082.
44. Goke, R., Larsen, P.J., Mikkelsen, J.D., and Sheikh, S.P. 1995. Identification of specific binding sites for glucagon-like peptide-1 on the posterior lobe of the rat pituitary. Neuroendocrinology. 62:130-134.
45. Mercer, J.G., Moar, K.M., Findlay, P.A., Hoggard, N., and Adam, C.L. 1998. Association of leptin receptor (OB-Rb), NPY and GLP-1 gene expression in the ovine and murine brainstem. Regul. Pept. 75-76:271-278.
46. Goldstone, A.P., et al. 2000. Effect of leptin on hypothalamic GLP-1 peptide and brain-stem preproglucagon mRNA. Biochem. Biophys. Res. Commun. 269:331-335.
47. Tang-Christensen, M., Vrang, N., and Larsen, P.J. 2001. Glucagon-like peptide containing pathways in the regulation of feeding behaviour. Int. J. Obes. Relat. Metab. Disord. 25(Suppl. 5):S42-S47.
48. Alvarez, E., et al. 2005. The expression of GLP-1 receptor mRNA and protein allows the effect of GLP-1 on glucose metabolism in the human hypothalamus and brainstem. J. Neurochem. 92:798-806.
49. Matschinsky, F.M. 1996. A lesson in metabolic regulation inspired by the glucokinase paradigm. Diabetes. 45:223-241.
50. Thorens, B. 1992. Expression cloning of the pancreatic beta cell receptor for the gluco-incretin hormone glucagon-like peptide 1. Proc. Natl. Acad. Sci. U. S. A. 89:8641-8645.
51. Hill, C.E., Phillips, J.K., and Sandow, S.L. 2001. Heterogeneous control of blood flow amongst different vascular beds. Med. Res. Rev. 21:1-60.
52. Perrin, C., Knauf, C., and Burcelin, R. 2004. Intracerebroventricular infusion of glucose, insulin, and the adenosine monophosphate-activated kinase activator, 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside, controls muscle glycogen synthesis. Endocrinology. 145:4025-4033.
53. Fisher, S.J., Bruning, J.C., Lannon, S., and Kahn, C.R. 2005. Insulin signaling in the central nervous system is critical for the normal sympathoadrenal response to hypoglycemia. Diabetes. 54:1447-1451.
54. Obici, S., Zhang, B.B., Karkanias, G., and Rossetti, L. 2002. Hypothalamic insulin signaling is required for inhibition of glucose production. Nat. Med. 8:1376-1382.
55. Burcelin, R., Crivelli, V., Dacosta, A., Roy-Tirelli, A., and Thorens, B. 2002. Heterogeneous metabolic adaptation of C57BL/6J mice to high-fat diet. Am. J. Physiol. Endocrinol. Metab. 282:E834-E842.
56. Preitner, F., et al. 2004. Gluco-incretins control insulin secretion at multiple levels as revealed in mice lacking GLP-1 and GIP receptors. J. Clin. Invest. 113:635-645. doi:10.1172/JCI200420518.
57. Bruning, J., et al. 1998. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol. Cell. 2:559-569.
58. Burcelin, R., and Thorens, B. 2001. Glucagon secretion is predominantly controlled by extrapancreatic GLUT2-dependent glucose sensors. Diabetes. 50:1282-1289.
59. Burcelin, R., Dolci, W., and Thorens, B. 2000. Portal glucose infusion in the mouse induces hypoglycemia. Evidence that the hepatoportal glucose sensor stimulates glucose utilization. Diabetes. 49:1635-1642.
60. Somogyi, M. 1945. Determination of blood sugar. J. Biol. Chem. 160:69-73.
61. Burcelin, R., et al. 2004. Impaired glucose homeostasis in mice lacking the alpha1b-adrenergic receptor subtype. J. Biol. Chem. 279:1108-1115.
62. Heydrick, S.J., et al. 1993. Defect in skeletal muscle phosphatidylinositol-3-kinase in obese insulin-resistant mice. J. Clin. Invest. 91:1358-1366.