Glucagon-like peptide-1 receptor signaling in the lateral parabrachial nucleus contributes to the control of food intake and motivation to feed

Neuropsychopharmacology

Volumn 39, Issue 9, 2014, Pages 2233-2243

  Alhadeff, Amber L ^a   Baird, John Paul ^b   Swick, Jennifer C ^b   Hayes, Matthew R ^a   Grill, Harvey J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b AMHERST COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXENDIN 4; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCAGON RECEPTOR; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANOREXIA; ARTICLE; BODY WEIGHT; BRAIN AQUEDUCT; FLUID INTAKE; FOOD INTAKE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOTIVATION; NERVE CELL; NEUROANATOMICAL TRACT TRACING; NONHUMAN; PARABRACHIAL NUCLEUS; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SOLITARY TRACT NUCLEUS; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CYTOLOGY; DRUG EFFECTS; EATING; INSTRUMENTAL CONDITIONING; LIPID DIET; METABOLISM; MOTOR ACTIVITY; NERVE TRACT; PHYSIOLOGY; PICA; REINFORCEMENT; SPRAGUE DAWLEY RAT; SYNAPSE;

ANIMALS; APPETITE REGULATION; CONDITIONING, OPERANT; DIET, HIGH-FAT; EATING; GLUCAGON-LIKE PEPTIDE 1; MALE; MOTIVATION; MOTOR ACTIVITY; NEURAL PATHWAYS; NEURONS; PARABRACHIAL NUCLEUS; PICA; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCAGON; REINFORCEMENT SCHEDULE; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84904468017     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2014.74     Document Type: Article

References (53)

1. Alhadeff AL, Rupprecht LE, Hayes MR (2012). GLP-1 neurons in the nucleus of the solitary tract project directly to the ventral tegmental area and nucleus accumbens to control for food intake. Endocrinology 153: 647-658.
2. Andrews PL, Horn CC (2006). Signals for nausea and emesis: implications for models of upper gastrointestinal diseases. Auton Neurosci 125: 100-115.
3. Astrup A, Rossner S, Van Gaal L, Rissanen A, Niskanen L, Al Hakim M et al (2009). Effects of liraglutide in the treatment of obesity: a randomised, double-blind, placebo-controlled study. Lancet 374: 1606-1616.
4. Baird JP, Travers JB, Travers SP (2001). Parametric analysis of gastric distension responses in the parabrachial nucleus. Am J Physiol Regul Integr Comp Physiol 281: R1568-R1580.
5. Blessing WW (1997). The Lower Brainstem and Bodily Homeostasis. Oxford University Press: New York, NY.
6. Brog JS, Salyapongse A, Deutch AY, Zahm DS (1993). The patterns of afferent innervation of the core and shell in the 'accumbens' part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol 338: 255-278.
7. Buse JB, Henry RR, Han J, Kim DD, Fineman MS, Baron AD (2004). Effects of exenatide (exendin-4) on glycemic control over 30 weeks in sulfonylurea-treated patients with type 2 diabetes. Diabetes Care 27: 2628-2635.
8. Buse JB, Rosenstock J, Sesti G, Schmidt WE, Montanya E, Brett JH et al (2009). Liraglutide once a day versus exenatide twice a day for type 2 diabetes: a 26-week randomised, parallel-group, multinational, open-label trial (LEAD-6). Lancet 374: 39-47.
9. Chaijale NN, Aloyo VJ, Simansky KJ (2013). The stereoisomer (+)-naloxone potentiates G-protein coupling and feeding associated with stimulation of mu opioid receptors in the parabrachial nucleus. J Psychopharmacol 27: 302-311.
10. Cho YK, Li CS, Smith DV (2002). Gustatory projections from the nucleus of the solitary tract to the parabrachial nuclei in the hamster. Chem Senses 27: 81-90.
11. De Jonghe BC, Horn CC (2009). Chemotherapy agent cisplatin induces 48-h Fos expression in the brain of a vomiting species, the house musk shrew (Suncus murinus). Am J Physiol Regul Integr Comp Physiol 296: R902-R911.
12. De Oliveira LB, Kimura EH, Callera JC, De Luca LA Jr, Colombari DS, Menani JV (2011). Baclofen into the lateral parabrachial nucleus induces hypertonic sodium chloride and sucrose intake in rats. Neuroscience 183: 160-170.
13. Dickson SL, Shirazi RH, Hansson C, Bergquist F, Nissbrandt H, Skibicka KP (2012). The glucagon-like peptide 1 (GLP-1) analogue, exendin-4, decreases the rewarding value of food: a new role for mesolimbic GLP-1 receptors. J Neurosci 32: 4812-4820.
14. DiPatrizio NV, Simansky KJ (2008). Activating parabrachial cannabinoid CB1 receptors selectively stimulates feeding of palatable foods in rats. J Neurosci 28: 9702-9709.
15. Dossat AM, Lilly N, Kay K, Williams DL (2011). Glucagonlike peptide 1 receptors in nucleus accumbens affect food intake. J Neurosci 31: 14453-14457.
16. Elmquist JK, Scammell TE, Jacobson CD, Saper CB (1996). Distribution of Fos-like immunoreactivity in the rat brain following intravenous lipopolysaccharide administration. J Comp Neurol 371: 85-103.
17. Gaykema RP, Daniels TE, Shapiro NJ, Thacker GC, Park SM, Goehler LE (2009). Immune challenge and satiety-related activation of both distinct and overlapping neuronal populations in the brainstem indicate parallel pathways for viscerosensory signaling. Brain Res 1294: 61-79.
18. Goke R, Larsen PJ, Mikkelsen JD, Sheikh SP (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.
19. Grill HJ, Hayes MR (2012). Hindbrain neurons as an essential hub in the neuroanatomically distributed control of energy balance. Cell Metab 16: 296-309.
20. Hayes MR (2012). Neuronal and intracellular signaling pathways mediating GLP-1 energy balance and glycemic effects. Physiol Behav 106: 413-416.
21. 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.
22. Hayes MR, De Jonghe BC, Kanoski SE (2010). Role of the glucagonlike- peptide-1 receptor in the control of energy balance. Physiol Behav 100: 503-510.
23. Hayes MR, Leichner TM, Zhao S, Lee GS, Chowansky A, Zimmer D et al (2011). Intracellular signals mediating the food intakesuppressive effects of hindbrain glucagon-like peptide-1 receptor activation. Cell Metab 13: 320-330.
24. Hisadome K, Reimann F, Gribble FM, Trapp S (2011). CCK stimulation of GLP-1 neurons involves alpha1-adrenoceptormediated increase in glutamatergic synaptic inputs. Diabetes 60: 2701-2709.
25. Holst JJ (2007). The physiology of glucagon-like peptide 1. Physiol Rev 87: 1409-1439.
26. Kanoski SE, Alhadeff AL, Fortin SM, Gilbert JR, Grill HJ (2013). Leptin signaling in the medial nucleus tractus solitarius reduces food seeking and willingness to work for food. Neuropsychopharmacology 39: 605-613.
27. Kanoski SE, Fortin SM, Arnold M, Grill HJ, Hayes MR (2011a). 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.
28. Kanoski SE, Fortin SM, Arnold M, Grill HJ, Hayes MR (2011b). Peripheral and central GLP-1 receptor populations mediate qthe anorectic effects of peripherally administered GLP-1 receptor agonists, liraglutide and exendin-4. Endocrinology 152: 3103-3112.
29. 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.
30. Karimnamazi H, Travers SP, Travers JB (2002). Oral and gastric input to the parabrachial nucleus of the rat. Brain Res 957: 193-206.
31. 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.
32. 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.
33. Li CS, Chung S, Lu DP, Cho YK (2012). Descending projections from the nucleus accumbens shell suppress activity of tasteresponsive neurons in the hamster parabrachial nuclei. J Neurophysiol 108: 1288-1298.
34. 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(1 Pt 2): R23-R29.
35. 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.
36. Mietlicki-Baase EG, Ortinski PI, Rupprecht LE, Olivos DR, Alhadeff AL, Pierce RC et al (2013a). The food intakesuppressive effects of glucagon-like peptide-1 receptor signaling in the ventral tegmental area are mediated by AMPA/kainate receptors. Am J Physiol Endocrinol Metab 305: E1367-E1374.
37. Mietlicki-Baase EG, Rupprecht LE, Olivos DR, Zimmer DJ, Alter MD, Pierce RC et al (2013b). Amylin receptor signaling in the ventral tegmental area is physiologically relevant for the control of food intake. Neuropsychopharmacology 38: 1685-1697.
38. Miller RL, Stein MK, Loewy AD (2011). Serotonergic inputs to FoxP2 neurons of the pre-locus coeruleus and parabrachial nuclei that project to the ventral tegmental area. Neuroscience 193: 229-240.
39. Norgren R (1976). Taste pathways to hypothalamus and amygdala. J Comp Neurol 166: 17-30.
40. Norgren R (1978). Projections from the nucleus of the solitary tract in the rat. Neuroscience 3: 207-218.
41. Overton PG, Vautrelle N, Redgrave P (2014). Sensory regulation of dopaminergic cell activity: phenomenology, circuitry and function. Neuroscience (e-pub ahead of print).
42. Paxinos G, Watson C (2005). The Rat Brain in Stereotaxic Coordinates. 5th edn Academic Press: San Diego, CA.
43. 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.
44. Ritter RC (2004). Gastrointestinal mechanisms of satiation for food. Physiol Behav 81: 249-273.
45. Ritter RC, Slusser PG, Stone S (1981). Glucoreceptors controlling feeding and blood glucose: location in the hindbrain. Science 213: 451-452.
46. 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.
47. Skibicka KP, Grill HJ (2009). Hypothalamic and hindbrain melanocortin receptors contribute to the feeding, thermogenic, and cardiovascular action of melanocortins. Endocrinology 150: 5351-5361.
48. Vrang N, Phifer CB, Corkern MM, Berthoud HR (2003). Gastric distension induces c-Fos in medullary GLP-1/2-containing neurons. Am J Physiol Regul Integr Comp Physiol 285: R470-R478.
49. Wilson JD, Nicklous DM, Aloyo VJ, Simansky KJ (2003). An orexigenic role for mu-opioid receptors in the lateral parabrachial nucleus. Am J Physiol Regul Integr Comp Physiol 285: R1055-R1065.
50. Wu Q, Boyle MP, Palmiter RD (2009). Loss of GABAergic signaling by AgRP neurons to the parabrachial nucleus leads to starvation. Cell 137: 1225-1234.
51. Wu Q, Clark MS, Palmiter RD (2012). Deciphering a neuronal circuit that mediates appetite. Nature 483: 594-597.
52. Zhang C, Kang Y, Lundy RF (2011a). Terminal field specificity of forebrain efferent axons to the pontine parabrachial nucleus and medullary reticular formation. Brain Res 1368: 108-118.
53. Zhang Y, Kerman IA, Laque A, Nguyen P, Faouzi M, Louis GW et al (2011b). Leptin-receptor-expressing neurons in the dorsomedial hypothalamus and median preoptic area regulate sympathetic brown adipose tissue circuits. J Neurosci 31: 1873-1884.