Endogenous glucagon-like peptide-1 reduces drinking behavior and is differentially engaged by water and food intakes in rats

Journal of Neuroscience

Volumn 34, Issue 49, 2014, Pages 16417-16423

  McKay, Naomi J ^a   Galante, Daniela L ^a   Daniels, Derek ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Fluid homeostasis; Food intake; Glucagon like peptide 1; Thirst; Water intake

Indexed keywords

COMPLEMENTARY DNA; EXENDIN 9; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; MESSENGER RNA; PEPTIDE HORMONE ANTAGONIST; PROGLUCAGON; SODIUM CHLORIDE; UNCLASSIFIED DRUG; EXENDIN (9-39); PEPTIDE FRAGMENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRINKING BEHAVIOR; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL BEHAVIORAL TEST; FLUID INTAKE; FOOD DEPRIVATION; FOOD INTAKE; GENE EXPRESSION; ILEUM; IMPLANTATION; LICKING; MALE; NEUROPSYCHOLOGY; NONHUMAN; RAT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; REHYDRATION; SOLITARY TRACT NUCLEUS; STIMULATION; THIRST; TREATMENT RESPONSE; VENTRICULAR CANNULA (BRAIN); WATER DEPRIVATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; DRINKING; DRUG EFFECTS; EATING; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; PHYSIOLOGY;

ANIMALS; DRINKING; DRINKING BEHAVIOR; EATING; GENE EXPRESSION; GLUCAGON-LIKE PEPTIDE 1; ILEUM; INJECTIONS, INTRAVENTRICULAR; MALE; PEPTIDE FRAGMENTS; PROGLUCAGON; RATS; SALINE SOLUTION, HYPERTONIC; SOLITARY NUCLEUS; WATER DEPRIVATION;

EID: 84914689055     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3267-14.2014     Document Type: Article

References (40)

1. Beak SA, Heath MM, Small CJ, Morgan DG, Ghatei MA, Taylor AD, Buckingham JC, Bloom SR, Smith DM (1998) Glucagon-like peptide-1 stimulates luteinizing hormone-releasing hormone secretion in a rodent hypothalamic neuronal cell line. J Clin Invest 101:1334-1341. CrossRef Medline
2. Bourjeili N, Turner M, Stinner J, Ely D (1995) Sympathetic nervous system influences salt appetite in four strains of rats. Physiol Behav 58:437-443. CrossRef Medline
3. Cani PD, Hoste S, Guiot Y, Delzenne NM (2007) Dietary non-digestible carbohydrates promote L-cell differentiation in the proximal colon of rats. Br J Nutr 98:32-37. CrossRef Medline
4. Chelikani PK, Haver AC, Reidelberger RD (2005) Intravenous infusion of glucagon-like peptide-1 potently inhibits food intake, sham feeding, and gastric emptying in rats. Am J Physiol Regul Integr Comp Physiol 288: R1695-R1706. CrossRef Medline
5. Deaux E, Kakolewski JW (1970) Emotionally induced increases in effective osmotic pressure and subsequent thirst. Science 169:1226-1228. CrossRef Medline
6. Egecioglu E, Engel JA, Jerlhag E (2013a) The glucagon-like peptide 1 analogue Exendin-4 attenuates the nicotine-induced locomotor stimulation, accumbal dopamine release, conditioned place preference as well as the expression of locomotor sensitization in mice. PLoS One 8:e77284. CrossRef Medline
7. Egecioglu E, Steensland P, Fredriksson I, Feltmann K, Engel JA, Jerlhag E (2013b) The glucagon-like peptide 1 analogue Exendin-4 attenuates alcohol mediated behaviors in rodents. Psychoneuroendocrinology 38: 1259-1270. CrossRef Medline
8. Elliott RM, Morgan LM, Tredger JA, Deacon S, Wright J, Marks V (1993) Glucagon-like peptide-1 (7-36)amide and glucose-dependent insulinotropic polypeptide secretion in response to nutrient ingestion in man: acute post-prandial and 24-h secretion patterns. J Endocrinol 138:159-166. CrossRef Medline
9. Gardiner SM, March JE, Kemp PA, Bennett T (2006) Mesenteric vasoconstriction and hindquarters vasodilatation accompany the pressor actions of exendin-4 in conscious rats. J Pharmacol Exp Ther 316:852-859. CrossRef Medline
10. Goldstone AP, Morgan I, Mercer JG, Morgan DG, Moar KM, Ghatei MA, Bloom SR (2000) Effect of leptin on hypothalamic GLP-1 peptide and brain-stem pre-proglucagon mRNA. Biochem Biophys Res Commun 269:331-335. CrossRef Medline
11. Gutzwiller JP, Hruz P, Huber AR, Hamel C, Zehnder C, Drewe J, Gutmann H, Stanga Z, Vogel D, Beglinger C (2006) Glucagon-like peptide-1 is involved in sodium and water homeostasis in humans. Digestion 73:142-150. CrossRef Medline
12. Hayes MR, Kanoski SE, Alhadeff AL, Grill HJ (2011) Comparative effects of the long-acting glp-1 receptor ligands, liraglutide and exendin-4, on food intake and body weight suppression in rats. Obesity 19:1342-1349. CrossRef Medline
13. Holst JJ (2007) The physiology of glucagon-like peptide 1. Physiol Rev 87: 1409-1439. CrossRef Medline
14. Holst JJ, Deacon CF (2005) Glucagon-like peptide-1 mediates the therapeutic actions of DPP-IV inhibitors. Diabetologia 48:612-615. CrossRef Medline
15. Jin SL, Han VK, Simmons JG, Towle AC, Lauder JM, Lund PK (1988) Distribution of glucagonlike peptide I (GLP-I), glucagon, and glicentin in the rat brain: an immunocytochemical study. J Comp Neurol 271:519-532. CrossRef Medline
16. Kreisler AD, Davis EA, Rinaman L (2014) Differential activation of chemically identified neurons in the caudal nucleus of the solitary tract in nonentrained rats after intake of satiating vs. non-satiating meals. Physiol Behav S0031-9384(14)00032-8. CrossRef Medline
17. Larsen PJ, Tang-Christensen M, Holst JJ, Orskov C (1997) Distribution of glucagon-like peptide-1 and other preproglucagon-derived peptides in the rat hypothalamus and brainstem. Neuroscience 77:257-270. CrossRef Medline
18. Larsen PJ, Fledelius C, Knudsen LB, Tang-Christensen M (2001) Systemic administration of the long-acting GLP-1 derivative NN2211 induces lasting and reversible weight loss in both normal and obese rats. Diabetes 50:2530-2539. CrossRef Medline
19. Lu SS, Yu YL, Zhu HJ, Liu XD, Liu L, Liu YW, Wang P, Xie L, Wang GJ (2009) Berberine promotes glucagon-like peptide-1 (7-36) amide secretion in streptozotocin-induced diabetic rats. J Endocrinol 200:159-165. CrossRef Medline
20. Maniscalco JW, Kreisler AD, Rinaman L (2012) Satiation and stressinduced hypophagia: examining the role of hindbrain neurons expressing prolactin-releasing Peptide or glucagon-like peptide 1. Front Neurosci 6:199. CrossRef Medline
21. McKay NJ, Daniels D (2013) Glucagon-like Peptide-1 receptor agonist administration suppresses both water and saline intake in rats. J Neuroendocrinol 25:929-938. CrossRef Medline
22. McKay NJ, Kanoski SE, Hayes MR, Daniels D (2011) Glucagon-like peptide-1 receptor agonists suppress water intake independent of effects on food intake. Am J Physiol Regul Integr Comp Physiol 301:R1755-R1764. CrossRef Medline
23. Meeran K, O’Shea D, Edwards CM, Turton MD, Heath MM, Gunn I, Abusnana S, Rossi M, Small CJ, Goldstone AP, Taylor GM, Sunter D, Steere J, Choi SJ, Ghatei MA, Bloom SR (1999) Repeated intracerebroventricular administration of glucagon-like peptide-1-(7-36) amide or exendin-(9-39) alters body weight in the rat. Endocrinology 140:244-250. CrossRef Medline
24. Merchenthaler I, Lane M, Shughrue P (1999) Distribution of pre-proglucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. J Comp Neurol 403:261-280. CrossRef Medline
25. Mojsov S, Kopczynski MG, Habener JF (1990) Both amidated and nonamidated forms of glucagon-like peptide I are synthesized in the rat intestine and the pancreas. J Biol Chem 265:8001-8008.Medline
26. Navarro M, Rodriquez de Fonseca F, Alvarez E, Chowen JA, Zueco JA, Gomez R, Eng J, Blázquez E (1996) Colocalization of glucagon-like peptide-1 (GLP-1) receptors, glucose transporter GLUT-2, and glucokinase mRNAs in rat hypothalamic cells: evidence for a role of GLP-1 receptor agonists as an inhibitory signal for food and water intake. J Neurochem 67:1982-1991. CrossRef Medline
27. Orskov C, Wettergren A, Holst JJ (1996) Secretion of the incretin hormones glucagon-like peptide-1 and gastric inhibitory polypeptide correlates with insulin secretion in normal man throughout the day. Scand J Gastroenterol 31:665-670. CrossRef Medline
28. Robinson MM, Evered MD (1987) Pressor action of intravenous angiotensin II reduces drinking response in rats. Am J Physiol 252:R754-R759.Medline
29. Sato MA, Yada MM, De Luca LA Jr (1996) Antagonism of the reninangiotensin system and water deprivation-induced NaCl intake in rats. Physiol Behav 60:1099-1104. CrossRef Medline
30. Schick RR, Zimmermann JP, vorm Walde T, Schusdziarra V (2003) Peptides that regulate food intake: glucagon-like peptide 1-(7-36) amide acts at lateral and medial hypothalamic sites to suppress feeding in rats. Am J Physiol Regul Integr Comp Physiol 284:R1427-R1435.Medline
31. Serre V, Dolci W, Schaerer E, Scrocchi L, Drucker D, Efrat S, Thorens B (1998) Exendin-(9-39) is an inverse agonist of the murine glucagon-like peptide-1 receptor: implications for basal intracellular cyclic adenosine 3,5-monophosphate levels and beta-cell glucose competence. Endocrinology 139:4448-4454. CrossRef Medline
32. Smith GP (2001) John Davis and the meanings of licking. Appetite 36:84-92. CrossRef Medline
33. Spector AC, Klumpp PA, Kaplan JM (1998) Analytical issues in the evaluation of food deprivation and sucrose concentration effects on the microstructure of licking behavior in the rat. Behav Neurosci 112:678-694. CrossRef Medline
34. Tang-Christensen M, Larsen PJ, Göke R, Fink-Jensen A, Jessop DS, Møller M, Sheikh SP (1996) Central administration of GLP-1-(7-36) amide inhibits food and water intake in rats. Am J Physiol 271:R848-R856.Medline
35. Turton MD, O’Shea D, Gunn I, Beak SA, Edwards CM, Meeran K, Choi SJ, Taylor GM, Heath MM, Lambert PD, Wilding JP, Smith DM, Ghatei MA, Herbert J, Bloom SR (1996) A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 379:69-72. CrossRef Medline
36. Vaswani K, Tejwani GA, Mousa S (1983) Stress induced differential intake of various diets and water by rat: the role of the opiate system. Life Sci 32:1983-1996. CrossRef Medline
37. Wang T, Edwards GL, Baile CA (1998) Glucagon-like peptide-1 (7-36) amide administered into the third cerebroventricle inhibits water intake in rats. Proc Soc Exp Biol Med 219:85-91. CrossRef Medline
38. Williams DL, Baskin DG, Schwartz MW (2009) Evidence that intestinal glucagon-like peptide-1 plays a physiological role in satiety. Endocrinology 150:1680-1687. CrossRef Medline
39. Yamamoto H, Lee CE, Marcus JN, Williams TD, Overton JM, Lopez ME, Hollenberg AN, Baggio L, Saper CB, Drucker DJ, Elmquist JK (2002) Glucagon-like peptide-1 receptor stimulation increases blood pressure and heart rate and activates autonomic regulatory neurons. J Clin Invest 110:43-52. CrossRef Medline
40. Yu YL, Lu SS, Yu S, Liu YC, Wang P, Xie L, Wang GJ, Liu XD (2009) Huanglian-jie-du-decoction modulates glucagon-like peptide-1 secretion in diabetic rats. J Ethnopharmacol 124:444-449. CrossRef Medline