Parabrachial nucleus contributions to glucagon-like peptide-1 receptor agonist-induced hypophagia

Neuropsychopharmacology

Volumn 40, Issue 8, 2015, Pages 2001-2014

  Swick, Jennifer C ^a   Alhadeff, Amber L ^b   Grill, Harvey J ^b   Urrea, Paula ^a   Lee, Stephanie M ^a   Roh, Hyunsun ^a   Baird, John Paul ^a  

^a AMHERST COLLEGE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXENDIN 4; AMINO ACID RECEPTOR STIMULATING AGENT; ANTIDIABETIC AGENT; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; IBOTENIC ACID; LITHIUM CHLORIDE; PEPTIDE; SUCROSE; TRANQUILIZER; VENOM;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; APPETITE; ARTICLE; BRAIN STEM INJURY; CONTROLLED STUDY; COORDINATION; FEEDBACK SYSTEM; FEEDING BEHAVIOR; FOOD INTAKE; HYPOPHAGIA; LICKING; MALE; NONHUMAN; PARABRACHIAL NUCLEUS; PRIORITY JOURNAL; RAT; RHOMBENCEPHALON; SUGAR INTAKE; TASTE; AGONISTS; ANALYSIS OF VARIANCE; ANIMAL; BRAIN INJURY; CHEMICALLY INDUCED; DRUG EFFECTS; EATING; EATING DISORDER; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT; WATER DEPRIVATION;

ANALYSIS OF VARIANCE; ANIMALS; ANTIMANIC AGENTS; APPETITIVE BEHAVIOR; BRAIN INJURIES; EATING; EXCITATORY AMINO ACID AGONISTS; FEEDING AND EATING DISORDERS; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; HYPOGLYCEMIC AGENTS; IBOTENIC ACID; LITHIUM CHLORIDE; MALE; PARABRACHIAL NUCLEUS; PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; SUCROSE; TASTE; VENOMS; WATER DEPRIVATION;

EID: 84930821993     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2015.50     Document Type: Article

References (76)

1. Alhadeff AL, Baird J-P, Swick JC, Hayes MR, Grill HJ (2014). Glucagon-like peptide-1 receptor signaling in the lateral parabrachial nucleus contributes to the control of food intake and motivation to feed. Neuropsychopharmacology 39: 2233-2243.
2. Alhadeff AL, Grill HJ (2014). Hindbrain nucleus tractus solitarius glucagon-like peptide-1 receptor signaling reduces appetitive and motivational aspects of feeding. Am J Physiol Regul Integr Comp Physiol 307: R465-R470.
3. Antin J, Gibbs J, Holt J, Young RC, Smith GP (1975). Cholecystokinin elicits the complete behavioral sequence of satiety in rats. J Comp Physiol Psychol 89: 784-790.
4. Asarian L, Corp ES, Hrupka B, Geary N (1998). Intracerebroventricular glucagon-like peptide-1 (7-36) amide inhibits sham feeding in rats without eliciting satiety. Physiol Behav 64: 367-372.
5. Baird J-P, Choe A, Loveland JL, Beck J, Mahoney CE, Lord JS et al (2009). Orexin-A hyperphagia: hindbrain participation in consummatory feeding responses. Endocrinology 150: 1202-1216.
6. Baird J-P, Gray NE, Fischer SG (2006). Effects of neuropeptide Y on feeding microstructure: dissociation of appetitive and consummatory actions. Behav Neurosci 120: 937-951.
7. Baird J-P, St John SJ, Nguyen EA-N (2005). Temporal and qualitative dynamics of conditioned taste aversion processing: combined generalization testing and licking microstructure analysis. Behav Neurosci 119: 983-1003.
8. Baird JP, Grill HJ, Kaplan JM (1999). Effect of hepatic glucose infusion on glucose intake and licking microstructure in deprived and nondeprived rats. Am J Physiol 277: R1136-R1143.
9. Baird JP, Travers JB, Travers SP (2001a). Parametric analysis of gastric distension responses in the parabrachial nucleus. Am J Physiol Regul Integr Comp Physiol 281: R1568-R1580.
10. Baird JP, Travers SP, Travers JB (2001b). Integration of gastric distension and gustatory responses in the parabrachial nucleus. Am J Physiol Regul Integr Comp Physiol 281: R1581-R1593.
11. Baraboi E-D, St-Pierre DH, Shooner J, Timofeeva E, Richard D (2011). Brain activation following peripheral administration of the GLP-1 receptor agonist exendin-4. Am J Physiol Regul Integr Comp Physiol 301: R1011-R1024.
12. Barrera JG, Jones KR, Herman JP, D'Alessio DA, Woods SC, Seeley RJ (2011). Hyperphagia and increased fat accumulation in two models of chronic CNS glucagon-like peptide-1 loss of function. J Neurosci 31: 3904-3913.
13. Becskei C, Grabler V, Edwards GL, Riediger T, Lutz TA (2007). Lesion of the lateral parabrachial nucleus attenuates the anorectic effect of peripheral amylin and CCK. Brain Res 1162: 76-84.
14. Berthoud H-R, Sutton GM, Townsend RL, Patterson LM, Zheng H (2006). Brainstem mechanisms integrating gut-derived satiety signals and descending forebrain information in the control of meal size. Physiol Behav 89: 517-524.
15. Blevins T (2011). Control of postprandial glucose levels with insulin in type 2 diabetes. Postgrad Med 123: 135-147.
16. Bond A (2006). Exenatide (Byetta) as a novel treatment option for type 2 diabetes mellitus. Proc (Bayl Univ Med Cent) 19: 281-284.
17. Bullock BP, Heller RS, Habener JF (1996). Tissue distribution of messenger ribonucleic acid encoding the rat glucagon-like peptide-1 receptor. Endocrinology 137: 2968-2978.
18. Buse JB, Bergenstal RM, Glass LC, Heilmann CR, Lewis MS, Kwan AYM et al (2011). Use of twice-daily exenatide in Basal insulin-treated patients with type 2 diabetes: a randomized, controlled trial. Ann Intern Med 154: 103-112.
19. Calingasan NY, Ritter S (1993). Lateral parabrachial subnucleus lesions abolish feeding induced by mercaptoacetate but not by 2-deoxy-D-glucose. Am J Physiol 265: R1168-R1178.
20. Davis JD (1996). Deterministic and probabilistic control of the behavior of rats ingesting liquid diets. Am J Physiol 270: R793-R800.
21. Davis JD, Smith GP (1992). Analysis of the microstructure of the rhythmic tongue movements of rats ingesting maltose and sucrose solutions. Behav Neurosci 106: 217-228.
22. Davis JD, Smith GP, Kung TM (1995). Cholecystokinin changes the duration but not the rate of licking in vagotomized rats. Behav Neurosci 109: 991-996.
23. Davis JD, Smith GP, Singh B, McCann DP (2000). The impact of milk-derived unconditioned and conditioned negative feedback on the microstructure of ingestive behavior. Physiol Behav 70: 279-285.
24. Dossat AM, Diaz R, Gallo L, Panagos A, Kay K, Williams DL (2013). Nucleus accumbens GLP-1 receptors influence meal size and palatability. Am J Physiol Endocrinol Metab 304: E1314-E1320.
25. Dossat AM, Lilly N, Kay K, Williams DL (2011). Glucagon-like peptide 1 receptors in nucleus accumbens affect food intake. J Neurosci 31: 14453-14457.
26. Edwards CM, Stanley SA, Davis R, Brynes AE, Frost GS, Seal LJ et al (2001). Exendin-4 reduces fasting and postprandial glucose and decreases energy intake in healthy volunteers. Am J Physiol Endocrinol Metab 281: E155-E161.
27. Flynn FW, Grill HJ, Schulkin J, Norgren R (1991). Central gustatory lesions: II. Effects on sodium appetite, taste aversion learning, and feeding behaviors. Behav Neurosci 105: 944-954.
28. Fulwiler CE, Saper CB (1984). Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res 319: 229-259.
29. Giza BK, Scott TR, Vanderweele DA (1992). Administration of satiety factors and gustatory responsiveness in the nucleus tractus solitarius of the rat. Brain Res Bull 28: 637-639.
30. Göke R, Fehmann HC, Linn T, Schmidt H, Krause M, Eng J et al (1993). Exendin-4 is a high potency agonist and truncated exendin-(9-39)-amide an antagonist at the glucagon-like peptide 1-(7-36)-amide receptor of insulin-secreting beta-cells. J Biol Chem 268: 19650-19655.
31. Grill HJ (2010). Leptin and the systems neuroscience of meal size control. Front Neuroendocrinol 31: 61-78.
32. Hayes MR, Bradley L, Grill HJ (2009). Endogenous hindbrain glucagon-like peptide-1 receptor activation contributes to the control of food intake by mediating gastric satiation signaling. Endocrinology 150: 2654-2659.
33. Hayes MR, Skibicka KP, Grill HJ (2008). Caudal brainstem processing is sufficient for behavioral, sympathetic, and parasympathetic responses driven by peripheral and hindbrain glucagon-like-peptide-1 receptor stimulation. Endocrinology 149: 4059-4068.
34. Hernandez-Mesa N, Mamedov Z, Bures J (1985). Operant control of the pattern of licking in rats. Exp Brain Res 58: 117-124.
35. Jessen L, Aulinger BA, Hassel JL, Roy KJ, Smith EP, Greer TM et al (2012). Suppression of food intake by glucagon-like peptide-1 receptor agonists: relative potencies and role of dipeptidyl peptidase-4. Endocrinology 153: 5735-5745.
36. Kanoski SE, Fortin SM, Arnold M, Grill HJ, Hayes MR (2011). Peripheral and central GLP-1 receptor populations mediate the anorectic effects of peripherally administered GLP-1 receptor agonists, liraglutide and exendin-4. Endocrinology 152: 3103-3112.
37. Kanoski SE, Rupprecht LE, Fortin SM, De Jonghe BC, Hayes MR (2012). The role of nausea in food intake and body weight suppression by peripheral GLP-1 receptor agonists, exendin-4 and liraglutide. Neuropharmacology 62: 1916-1927.
38. Karimnamazi H, Travers JB (1998). Differential projections from gustatory responsive regions of the parabrachial nucleus to the medulla and forebrain. Brain Res 813: 283-302.
39. Karimnamazi H, Travers SP, Travers JB (2002). Oral and gastric input to the parabrachial nucleus of the rat. Brain Res 957: 193-206.
40. Kastin AJ, Akerstrom V (2003). Entry of exendin-4 into brain is rapid but may be limited at high doses. Int J Obes Relat Metab Disord 27: 313-318.
41. Kinzig KP, D'Alessio DA, Seeley RJ (2002). The diverse roles of specific GLP-1 receptors in the control of food intake and the response to visceral illness. J Neurosci 22: 10470-10476.
42. Lundy RF, Norgren R (2004). Activity in the hypothalamus, amygdala, and cortex generates bilateral and convergent modulation of pontine gustatory neurons. J Neurophysiol 91: 1143-1157.
43. Maersk M, Belza A, Holst JJ, Fenger-Grøn M, Pedersen SB, Astrup A et al (2012). Satiety scores and satiety hormone response after sucrose-sweetened soft drink compared with isocaloric semi-skimmed milk and with non-caloric soft drink: a controlled trial. Eur J Clin Nutr 66: 523-529.
44. Mamedov Z, Bures J (1984). Sensory feedback modulates the central pacemaker of licking in rats. Neurosci Lett 45: 1-6.
45. Mathes CM, Bueter M, Smith KR, Lutz TA, Roux CW, le, Spector AC (2012). Roux-en-Y gastric bypass in rats increases sucrose taste-related motivated behavior independent of pharmacological GLP-1-receptor modulation. Am J Physiol Regul Integr Comp Physiol 302: R751-R767.
46. McMahon LR, Wellman PJ (1998). PVN infusion of GLP-1-(7-36) amide suppresses feeding but does not induce aversion or alter locomotion in rats. Am J Physiol 274: R23-R29.
47. Merchenthaler I, Lane M, Shughrue P (1999). Distribution of prepro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. J Comp Neurol 403: 261-280.
48. Nakagawa A, Satake H, Nakabayashi H, Nishizawa M, Furuya K, Nakano S et al (2004). Receptor gene expression of glucagon-like peptide-1, but not glucose-dependent insulinotropic polypeptide, in rat nodose ganglion cells. Auton Neurosci 110: 36-43.
49. Nishijo H, Norgren R (1990). Responses from parabrachial gustatory neurons in behaving rats. J Neurophysiol 63: 707-724.
50. Norgren R, Hajnal A, Mungarndee SS (2006). Gustatory reward and the nucleus accumbens. Physiol Behav 89: 531-535.
51. Olivos DR, McGrath LE, Turner CA, Montaubin O, Mietlicki-Baase EG, Hayes MR (2014). Intraduodenal milk protein concentrate augments the glycemic and food intake suppressive effects of DPP-IV inhibition. Am J Physiol Regul Integr Comp Physiol 306: R157-R163.
52. Paues J, Mackerlova L, Blomqvist A (2006). Expression of melanocortin-4 receptor by rat parabrachial neurons responsive to immune and aversive stimuli. Neuroscience 141: 287-297.
53. Pelchat ML, Grill HJ, Rozin P, Jacobs J (1983). Quality of acquired responses to tastes by Rattus norvegicus depends on type of associated discomfort. J Comp Psychol 97: 140-153.
54. Punjabi M, Arnold M, Rüttimann E, Graber M, Geary N, Pacheco-López G et al (2014). Circulating glucagon-like peptide-1 (GLP-1) inhibits eating in male rats by acting in the hindbrain and without inducing avoidance. Endocrinology 155: 1690-1699.
55. Reilly S (1999). The parabrachial nucleus and conditioned taste aversion. Brain Res Bull 48: 239-254.
56. Renner E, Puskás N, Dobolyi A, Palkovits M (2012). Glucagon-like peptide-1 of brainstem origin activates dorsomedial hypothalamic neurons in satiated rats. Peptides 35: 14-22.
57. Rinaman L (2010). Ascending projections from the caudal visceral nucleus of the solitary tract to brain regions involved in food intake and energy expenditure. Brain Res 1350: 18-34.
58. Rüttimann EB, Arnold M, Geary N, Langhans W (2010). GLP-1 antagonism with exendin (9-39) fails to increase spontaneous meal size in rats. Physiol Behav 100: 291-296.
59. Sakai N, Yamamoto T (1997). Conditioned taste aversion and c-fos expression in the rat brainstem after administration of various USs. Neuroreport 8: 2215-2220.
60. Schwartz GJ, Salorio CF, Skoglund C, Moran TH (1999). Gut vagal afferent lesions increase meal size but do not block gastric preloadinduced feeding suppression. Am J Physiol 276: R1623-R1629.
61. Scott KA, Moran TH (2007). The GLP-1 agonist exendin-4 reduces food intake in nonhuman primates through changes in meal size. Am J Physiol Regul Integr Comp Physiol 293: R983-R987.
62. Shin Y-K, Martin B, Golden E, Dotson CD, Maudsley S, Kim W et al (2008). Modulation of taste sensitivity by GLP-1 signaling. J Neurochem 106: 455-463.
63. 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.
64. Spector AC, Redman R, Garcea M (1996). The consequences of gustatory nerve transection on taste-guided licking of sucrose and maltose in the rat. Behav Neurosci 110: 1096-1109.
65. Stanford JA, Vorontsova E, Surgener SP, Gerhardt GA, Fowler SC (2003). Aged Fischer 344 rats exhibit altered orolingual motor function: relationships with nigrostriatal neurochemical measures. Neurobiol Aging 24: 259-266.
66. Szayna M, Doyle ME, Betkey JA, Holloway HW, Spencer RG, Greig NH et al (2000). Exendin-4 decelerates food intake, weight gain, and fat deposition in Zucker rats. Endocrinology 141: 1936-1941.
67. Tokita K, Yamamoto T, Boughter JD (2012). Gustatory neural responses to umami stimuli in the parabrachial nucleus of C57BL/6J mice. J Neurophysiol 107: 1545-1555.
68. Travers JB, Dinardo LA, Karimnamazi H (1997). Motor and premotor mechanisms of licking. Neurosci Biobehav Rev 21: 631-647.
69. Trifunovic R, Reilly S (2001). Medial versus lateral parabrachial nucleus lesions in the rat: effects on cholecystokinin-and D-fenfluramine-induced anorexia. Brain Res 894: 288-296.
70. Vahl TP, Tauchi M, Durler TS, Elfers EE, Fernandes TM, Bitner RD et al (2007). Glucagon-like peptide-1 (GLP-1) receptors expressed on nerve terminals in the portal vein mediate the effects of endogenous GLP-1 on glucose tolerance in rats. Endocrinology 148: 4965-4973.
71. Vrang N, Larsen PJ (2010). Preproglucagon derived peptides GLP-1, GLP-2 and oxyntomodulin in the CNS: role of peripherally secreted and centrally produced peptides. Prog Neurobiol 92: 442-462.
72. Weijnen JA (1998). Licking behavior in the rat: measurement and situational control of licking frequency. Neurosci Biobehav Rev 22: 751-760.
73. Williams DL, Baskin DG, Schwartz MW (2009). Evidence that intestinal glucagon-like peptide-1 plays a physiological role in satiety. Endocrinology 150: 1680-1687.
74. Williams DL, Grill HJ, Weiss SM, Baird J-P, Kaplan JM (2002). Behavioral processes underlying the intake suppressive effects of melanocortin 3/4 receptor activation in the rat. Psychopharmacology (Berl) 161: 47-53.
75. Young RC, Gibbs J, Antin J, Holt J, Smith GP (1974). Absence of satiety during sham feeding in the rat. J Comp Physiol Psychol 87: 795-800.
76. Zheng H, Shin AC, Lenard NR, Townsend RL, Patterson LM, Sigalet DL et al (2009). Meal patterns, satiety, and food choice in a rat model of Roux-en-Y gastric bypass surgery. Am J Physiol Regul Integr Comp Physiol 297: R1273-R1282.