Brainstem mechanisms of amylin-induced anorexia

Physiology and Behavior

Volumn 100, Issue 5, 2010, Pages 511-518

  Potes, Catarina Soares ^a   Lutz, Thomas Alexander ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Amylin; Anorexia; Area postrema; Body weight; Brainstem; C Fos; CGMP; Cholecystokinin; Food intake; Noradrenergic neurons; Pathway; Phosphorylated ERK

Indexed keywords

AMYLIN; CHOLECYSTOKININ; CYCLIC GMP; GLUCAGON LIKE PEPTIDE 1; LEPTIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROTRANSMITTER; PEPTIDE YY; PROTEIN FOS;

ANOREXIA; ARTICLE; BODY WEIGHT; BRAIN FUNCTION; BRAIN STEM; CELL ACTIVATION; ELECTROENCEPHALOGRAM; FOOD INTAKE; HUMAN; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PARABRACHIAL NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

AMYLOID; ANIMALS; ANOREXIA; APPETITE DEPRESSANTS; BRAIN STEM; EATING; HUMANS; NEURONS; SIGNAL TRANSDUCTION;

EID: 77953707385     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2010.03.001     Document Type: Article

References (109)

1. Cooper G.J., Willis A.C., Clark A., Turner R.C., Sim R.B., Reid K.B. Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc Natl Acad Sci U S A 1987, 84:8628-8632.
2. Butler P.C., Chou J., Carter W.B., Wang Y.N., Bu B.H., Chang D., et al. Effects of meal ingestion on plasma amylin concentration in NIDDM and nondiabetic humans. Diabetes 1990, 39:752-756.
3. Ogawa A., Harris V., McCorkle S.K., Unger R.H., Luskey K.L. Amylin secretion from the rat pancreas and its selective loss after streptozotocin treatment. J Clin Invest 1990, 85:973-976.
4. Young A.A., Rink T.J., Wang M.W. Dose response characteristics for the hyperglycemic, hyperlactemic, hypotensive and hypocalcemic actions of amylin and calcitonin gene-related peptide-I (CGRP alpha) in the fasted, anaesthetized rat. Life Sci 1993, 52:1717-1726.
5. Lutz T.A., Pieber T.R., Scharrer E. Amylin reduces food intake in rats at doses that cause only slightly supraphysiological plasma amylin levels. Proceedings Annual Meeting of the Society for the Study of Ingestive Behavior 1996, Banff, Canada 22-25 August:46.
6. Lutz T.A., Geary N., Szabady M.M., Del Prete E., Scharrer E. Amylin decreases meal size in rats. Physiol Behav 1995, 58:1197-1202.
7. Mack C., Wilson J., Athanacio J., Reynolds J., Laugero K., Guss S., et al. Pharmacological actions of the peptide hormone amylin in the long-term regulation of food intake, food preference, and body weight. Am J Physiol Regul Integr Comp Physiol 2007, 293:R1855-R1863.
8. Lutz T.A., Del Prete E., Scharrer E. Reduction of food intake in rats by intraperitoneal injection of low doses of amylin. Physiol Behav 1994, 55:891-895.
9. Reidelberger R.D., Haver A.C., Arnelo U., Smith D.D., Schaffert C.S., Permert J. Amylin receptor blockade stimulates food intake in rats. Am J Physiol Regul Integr Comp Physiol 2004, 287:R568-R574.
10. Mollet A., Gilg S., Riediger T., Lutz T.A. Infusion of the amylin antagonist AC 187 into the area postrema increases food intake in rats. Physiol Behav 2004, 81:149-155.
11. Arnelo U., Reidelberger R., Adrian T.E., Larsson J., Permert J. Sufficiency of postprandial plasma levels of islet amyloid polypeptide for suppression of feeding in rats. Am J Physiol 1998, 275:R1537-R1542.
12. Young A., Denaro M. Roles of amylin in diabetes and in regulation of nutrient load. Nutrition 1998, 14:524-527.
13. Lutz T.A. Amylinergic control of food intake. Physiol Behav 2006, 89:465-471.
14. Lutz T.A., Mollet A., Rushing P.A., Riediger T., Scharrer E. The anorectic effect of a chronic peripheral infusion of amylin is abolished in area postrema/nucleus of the solitary tract (AP/NTS) lesioned rats. Int J Obes Relat Metab Disord 2001, 25:1005-1011.
15. Aronne L., Fujioka K., Aroda V., Chen K., Halseth A., Kesty N.C., et al. Progressive reduction in body weight after treatment with the amylin analog pramlintide in obese subjects: a phase 2, randomized, placebo-controlled, dose-escalation study. J Clin Endocrinol Metab 2007, 92:2977-2983.
16. Smith S.R., Blundell J.E., Burns C., Ellero C., Schroeder B.E., Kesty N.C., et al. Pramlintide treatment reduces 24-h caloric intake and meal sizes and improves control of eating in obese subjects: a 6-wk translational research study. Am J Physiol Endocrinol Metab 2007, 293:E620-E627.
17. Dacquin R., Davey R.A., Laplace C., Levasseur R., Morris H.A., Goldring S.R., et al. Amylin inhibits bone resorption while the calcitonin receptor controls bone formation in vivo. J Cell Biol 2004, 164:509-514.
18. Muff R., Born W., Lutz T.A., Fischer J.A. Biological importance of the peptides of the calcitonin family as revealed by disruption and transfer of corresponding genes. Peptides 2004, 25:2027-2038.
19. Mollet A., Meier S., Grabler V., Gilg S., Scharrer E., Lutz T.A. Endogenous amylin contributes to the anorectic effects of cholecystokinin and bombesin. Peptides 2003, 24:91-98.
20. Gebre-Medhin S., Mulder H., Pekny M., Westermark G., Tornell J., Westermark P., et al. Increased insulin secretion and glucose tolerance in mice lacking islet amyloid polypeptide (amylin). Biochem Biophys Res Commun 1998, 250:271-277.
21. Lutz T.A. Pancreatic amylin as a centrally acting satiating hormone. Curr Drug Targets 2005, 6:181-189.
22. Butler A.E., Jang J., Gurlo T., Carty M.D., Soeller W.C., Butler P.C. Diabetes due to a progressive defect in beta-cell mass in rats transgenic for human islet amyloid polypeptide (HIP rat): a new model for type 2 diabetes. Diabetes 2004, 53:1509-1516.
23. Weyer C., Maggs D.G., Young A.A., Kolterman O.G. Amylin replacement with pramlintide as an adjunct to insulin therapy in type 1 and type 2 diabetes mellitus: a physiological approach toward improved metabolic control. Curr Pharm Des 2001, 7:1353-1373.
24. Hollander P., Maggs D.G., Ruggles J.A., Fineman M., Shen L., Kolterman O.G., et al. Effect of pramlintide on weight in overweight and obese insulin-treated type 2 diabetes patients. Obes Res 2004, 12:661-668.
25. Young A.A., Gedulin B., Vine W., Percy A., Rink T.J. Gastric emptying is accelerated in diabetic BB rats and is slowed by subcutaneous injections of amylin. Diabetologia 1995, 38:642-648.
26. Edwards G.L., Gedulin B., Jodka C., Dilts R.P., Miller C.C., Young A. Area postrema (AP)-lesions block the regulation of gastric emptying by amylin. Neurogastroenterol Motil 1998, 10:26.
27. Isaksson B., Wang F., Permert J., Olsson M., Fruin B., Herrington M.K., et al. Chronically administered islet amyloid polypeptide in rats serves as an adiposity inhibitor and regulates energy homeostasis. Pancreatology 2005, 5:29-36.
28. Osaka T., Tsukamoto A., Koyama Y., Inoue S. Central and peripheral administration of amylin induces energy expenditure in anesthetized rats. Peptides 2008, 29:1028-1035.
29. Roth J.D., Hughes H., Kendall E., Baron A.D., Anderson C.M. Anti-obesity effects of the {beta}-cell hormone amylin in diet induced obese rats: effects on food intake, body weight, composition, energy expenditure and gene expression. Endocrinology 2006.
30. Wielinga P.Y., Alder B., Lutz T.A. The acute effect of amylin and salmon calcitonin on energy expenditure. Physiol Behav 2007, 91:212-217.
31. Lutz T.A. Control of food intake and energy expenditure by amylin-therapeutic implications. Int J Obes (Lond) 2009, 33(Suppl 1):S24-S27.
32. Lutz T.A. Roles of amylin in satiation, adiposity and brain development. Forum Nutr 2010, 63:64-74.
33. Sexton P.M., Paxinos G., Kenney M.A., Wookey P.J., Beaumont K. In vitro autoradiographic localization of amylin binding sites in rat brain. Neuroscience 1994, 62:553-567.
34. Lutz T.A., Senn M., Althaus J., Del Prete E., Ehrensperger F., Scharrer E. Lesion of the area postrema/nucleus of the solitary tract (AP/NTS) attenuates the anorectic effects of amylin and calcitonin gene-related peptide (CGRP) in rats. Peptides 1998, 19:309-317.
35. Fry M., Hoyda T.D., Ferguson A.V. Making sense of it: roles of the sensory circumventricular organs in feeding and regulation of energy homeostasis. Exp Biol Med 2007, 232:14-26. (Maywood).
36. Christopoulos G., Perry K.J., Morfis M., Tilakaratne N., Gao Y., Fraser N.J., et al. Multiple amylin receptors arise from receptor activity-modifying protein interaction with the calcitonin receptor gene product. Mol Pharmacol 1999, 56:235-242.
37. Muff R., Buhlmann N., Fischer J.A., Born W. An amylin receptor is revealed following co-transfection of a calcitonin receptor with receptor activity modifying proteins-1 or -3. Endocrinology 1999, 140:2924-2927.
38. Fischer J.A., Muff R., Born W. Functional relevance of G-protein-coupled-receptor-associated proteins, exemplified by receptor-activity-modifying proteins (RAMPs). Biochem Soc Trans 2002, 30:455-460.
39. McLatchie L.M., Fraser N.J., Main M.J., Wise A., Brown J., Thompson N., et al. RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 1998, 393:333-339.
40. Becskei C., Riediger T., Zund D., Wookey P., Lutz T.A. Immunohistochemical mapping of calcitonin receptors in the adult rat brain. Brain Res 2004, 1030:221-233.
41. Ueda T., Ugawa S., Saishin Y., Shimada S. Expression of receptor-activity modifying protein (RAMP) mRNAs in the mouse brain. Brain Res Mol Brain Res 2001, 93:36-45.
42. Barth S.W., Riediger T., Lutz T.A., Rechkemmer G. Peripheral amylin activates circumventricular organs expressing calcitonin receptor a/b subtypes and receptor-activity modifying proteins in the rat. Brain Res 2004, 997:97-102.
43. Riediger T., Schmid H.A., Lutz T., Simon E. Amylin potently activates AP neurons possibly via formation of the excitatory second messenger cGMP. Am J Physiol Regul Integr Comp Physiol 2001, 281:R1833-R1843.
44. Lutz T.A., Althaus J., Rossi R., Scharrer E. Anorectic effect of amylin is not transmitted by capsaicin-sensitive nerve fibers. Am J Physiol 1998, 274:R1777-R1782.
45. Lutz T.A., Del Prete E., Scharrer E. Subdiaphragmatic vagotomy does not influence the anorectic effect of amylin. Peptides 1995, 16:457-462.
46. Riediger T., Zuend D., Becskei C., Lutz T.A. The anorectic hormone amylin contributes to feeding-related changes of neuronal activity in key structures of the gut-brain axis. Am J Physiol Regul Integr Comp Physiol 2004, 286:R114-R122.
47. Gedulin B.R., Rink T.J., Young A.A. Dose-response for glucagonostatic effect of amylin in rats. Metabolism 1997, 46:67-70.
48. Riediger T., Schmid H.A., Lutz T.A., Simon E. Amylin and glucose co-activate area postrema neurons of the rat. Neurosci Lett 2002, 328:121-124.
49. Gedulin B.R., Young A.A. Hypoglycemia overrides amylin-mediated regulation of gastric emptying in rats. Diabetes 1998, 47:93-97.
50. Michel S., Becskei C., Erguven E., Lutz T.A., Riediger T. Diet-derived nutrients modulate the effects of amylin on c-fos expression in the area postrema and on food intake. Neuroendocrinology 2007.
51. Riediger T., Michel S., Forster K., Lutz T.A. The ability of amylin to reduce eating depends on the protein content of the diet. Appetite 2009, 52:854.
52. Rowland N.E., Crews E.C., Gentry R.M. Comparison of Fos induced in rat brain by GLP-1 and amylin. Regul Pept 1997, 71:171-174.
53. Becskei C., Grabler V., Edwards G.L., Riediger T., Lutz T.A. Lesion of the lateral parabrachial nucleus attenuates the anorectic effect of peripheral amylin and CCK. Brain Res 2007, 1162:76-84.
54. Morgan J.I., Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu Rev Neurosci 1991, 14:421-451.
55. Muller R., Bravo R., Burckhardt J., Curran T. Induction of c-fos gene and protein by growth factors precedes activation of c-myc. Nature 1984, 312:716-720.
56. Chang L., Karin M. Mammalian MAP kinase signalling cascades. Nature 2001, 410:37-40.
57. Torii S., Nakayama K., Yamamoto T., Nishida E. Regulatory mechanisms and function of ERK MAP kinases. J Biochem 2004, 136:557-561. (Tokyo).
58. Nishimoto S., Nishida E. MAPK signalling: ERK5 versus ERK1/2. EMBO Rep 2006, 7:782-786.
59. Yuan L.L., Adams J.P., Swank M., Sweatt J.D., Johnston D. Protein kinase modulation of dendritic K+channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 2002, 22:4860-4868.
60. Sutton G.M., Patterson L.M., Berthoud H.R. Extracellular signal-regulated kinase 1/2 signaling pathway in solitary nucleus mediates cholecystokinin-induced suppression of food intake in rats. J Neurosci 2004, 24:10240-10247.
61. Bhavsar S., Watkins J., Young A. Synergy between amylin and cholecystokinin for inhibition of food intake in mice. Physiol Behav 1998, 64:557-561.
62. Morfis M., Tilakaratne N., Furness S.G., Christopoulos G., Werry T.D., Christopoulos A., et al. Receptor activity-modifying proteins differentially modulate the G protein-coupling efficiency of amylin receptors. Endocrinology 2008, 149:5423-5431.
63. Armstrong D.M., Pickel V.M., Joh T.H., Reis D.J., Miller R.J. Immunocytochemical localization of catecholamine synthesizing enzymes and neuropeptides in area postrema and medial nucleus tractus solitarius of rat brain. J Comp Neurol 1981, 196:505-517.
64. Armstrong D.M., Pickel V.M., Joh T.H., Reis D.J. Electron microscopic immunocytochemical localization of tyrosine hydroxylase in the area postrema of rat. J Comp Neurol 1982, 206:259-272.
65. Steinbusch H.W. Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 1981, 6:557-618.
66. Lambas-Senas L., Chamba G., Dennis T., Renaud B., Scatton B. Distribution of dopamine, noradrenaline and adrenaline in coronal sections of the rat lower brainstem. Brain Res 1985, 347:306-312.
67. Milner T.A., Joh T.H., Pickel V.M. Tyrosine hydroxylase in the rat parabrachial region: ultrastructural localization and extrinsic sources of immunoreactivity. J Neurosci 1986, 6:2585-2603.
68. Lanca A.J., van der Kooy D. A serotonin-containing pathway from the area postrema to the parabrachial nucleus in the rat. Neuroscience 1985, 14:1117-1126.
69. Miceli M.O., Post C.A., van der Kooy D. Catecholamine and serotonin colocalization in projection neurons of the area postrema. Brain Res 1987, 412:381-385.
70. Lutz T.A., Riediger T., Zuend D., Wookey P. Amylin activates a dopaminergic pathway in the area postrema. Appetite 2002, 39:91.
71. Turek V.F., Cole R.L., Vu C., Roland B., Roth J.D. The characterization of neurons in the rat brainstem that are activated by amylin. Neuroscience Meeting Planner San Diego, CA: Society for Neuroscience 2007, online:Program No. 524.527.
72. Torack R.M., Stranahan P., Hartman B.K. The role of norepinephrine in the function of the area postrema. I. Immunofluorescent localization of dopamine-beta-hydroxylase and electron microscopy. Brain Res 1973, 61:235-252.
73. Potes C.S., Riediger T., Lutz T.A. Noradrenergic neurons of the area postrema mediate amylin's anorectic action. Appetite 2009, 52:853.
74. Potes CS, Turek VF, Cole R, Vu C, Roland BL, Roth JD, et al. Noradrenergic neurons of the area postrema mediate amylin's anorexigenic action. Am J Physiol Regul Integr Comp Physiol 2010 submitted.
75. Lutz T.A., Tschudy S., Mollet A., Geary N., Scharrer E. Dopamine D(2) receptors mediate amylin's acute satiety effect. Am J Physiol Regul Integr Comp Physiol 2001, 280:R1697-R1703.
76. Stafanini E., Clement-Cormier Y. Detection of dopamine receptors in the area postrema. Eur J Pharmacol 1981, 74:257-260.
77. Qian M., Johnson A.E., Kallstrom L., Carrer H., Sodersten P. Cholecystokinin, dopamine D2 and N-methyl-d-aspartate binding sites in the nucleus of the solitary tract of the rat: possible relationship to ingestive behavior. Neuroscience 1997, 77:1077-1089.
78. Torack R.M., LaValle M. The role of norepinephrine in the function of the area postrema. II. In vitro incubation and stimulated release of tritiated norepinephrine. Brain Res 1973, 61:253-265.
79. Devoto P., Flore G., Pani L., Gessa G.L. Evidence for co-release of noradrenaline and dopamine from noradrenergic neurons in the cerebral cortex. Mol Psychiatry 2001, 6:657-664.
80. Devoto P., Flore G., Pira L., Longu G., Gessa G.L. Alpha2-adrenoceptor mediated co-release of dopamine and noradrenaline from noradrenergic neurons in the cerebral cortex. J Neurochem 2004, 88:1003-1009.
81. Devoto P., Flore G., Vacca G., Pira L., Arca A., Casu M.A., et al. Co-release of noradrenaline and dopamine from noradrenergic neurons in the cerebral cortex induced by clozapine, the prototype atypical antipsychotic. Psychopharmacology (Berl) 2003, 167:79-84.
82. Bednar I., Forsberg G., Linden A., Qureshi G.A., Sodersten P. Involvement of dopamine in inhibition of food intake by cholecystokinin octapeptide in male rats. J Neuroendocrinol 1991, 3:491-496.
83. Bednar I., Qian M., Qureshi G.A., Kallstrom L., Johnson A.E., Carrer H., et al. Glutamate inhibits ingestive behaviour. J Neuroendocrinol 1994, 6:403-408.
84. Lutz T.A., Del Prete E., Walzer B., Scharrer E. The histaminergic, but not the serotoninergic, system mediates amylin's anorectic effect. Peptides 1996, 17:1317-1322.
85. Mollet A., Lutz T.A., Meier S., Riediger T., Rushing P.A., Scharrer E. Histamine H1 receptors mediate the anorectic action of the pancreatic hormone amylin. Am J Physiol Regul Integr Comp Physiol 2001, 281:R1442-R1448.
86. Mollet A., Meier S., Riediger T., Lutz T.A. Histamine H1 receptors in the ventromedial hypothalamus mediate the anorectic action of the pancreatic hormone amylin. Peptides 2003, 24:155-158.
87. Saper C.B. The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. Annu Rev Neurosci 2002, 25:433-469.
88. Rowland N.E., Richmond R.M. Area postrema and the anorectic actions of dexfenfluramine and amylin. Brain Res 1999, 820:86-91.
89. Potes C.S., Lutz T.A., Riediger T. The central signaling pathways of amylin: a neuroanatomical study. Appetite 2008, 51:391.
90. Potes CS, Lutz TA, Riediger T. Identification of central projections from amylin-activated neurons to the lateral hypothalamus. Brain Res 2010 submitted.
91. Beaumont K., Kenney M.A., Young A.A., Rink T.J. High affinity amylin binding sites in rat brain. Mol Pharmacol 1993, 44:493-497.
92. van Rossum D., Menard D.P., Fournier A., St-Pierre S., Quirion R. Autoradiographic distribution and receptor binding profile of [125I]Bolton Hunter-rat amylin binding sites in the rat brain. J Pharmacol Exp Ther 1994, 270:779-787.
93. Roth J.D., Roland B.L., Cole R.L., Trevaskis J.L., Weyer C., Koda J.E., et al. Leptin responsiveness restored by amylin agonism in diet-induced obesity: evidence from nonclinical and clinical studies. Proc Natl Acad Sci U S A 2008, 105:7257-7262.
94. Turek V.F., Trevaskis J.L., Levin B.E., Dunn-Meynell A.A., Irani B., Gu G., et al. Mechanisms of amylin/leptin synergy in rodent models. Endocrinology 2010, 151:143-152.
95. Weyer C. Hormones in concert. The Scientist 2010, 23:34.
96. Chan J.L., Roth J.D., Weyer C. It takes two to tango: combined amylin/leptin agonism as a potential approach to obesity drug development. J Investig Med 2009, 57:777-783.
97. Rinaman L., Verbalis J.G., Stricker E.M., Hoffman G.E. Distribution and neurochemical phenotypes of caudal medullary neurons activated to express cFos following peripheral administration of cholecystokinin. J Comp Neurol 1993, 338:475-490.
98. Monnikes H., Lauer G., Arnold R. Peripheral administration of cholecystokinin activates c-fos expression in the locus coeruleus/subcoeruleus nucleus, dorsal vagal complex and paraventricular nucleus via capsaicin-sensitive vagal afferents and CCK-A receptors in the rat. Brain Res 1997, 770:277-288.
99. Asarian L. Loss of cholecystokinin and glucagon-like peptide-1-induced satiation in mice lacking serotonin 2C receptors. Am J Physiol Regul Integr Comp Physiol 2009, 296:R51-R56.
100. Baggio L.L., Huang Q., Cao X., Drucker D.J. An albumin-exendin-4 conjugate engages central and peripheral circuits regulating murine energy and glucose homeostasis. Gastroenterology 2008, 134:1137-1147.
101. Bonaz B., Taylor I., Tache Y. Peripheral peptide YY induces c-fos-like immunoreactivity in the rat brain. Neurosci Lett 1993, 163:77-80.
102. Inoue K., Hisatomi A., Umeda F., Nawata H. Effects of glucagon-like peptide 1 (7-36) amide and glucagon on amylin release from perfused rat pancreas. Horm Metab Res 1991, 23:407-409.
103. Ruttimann E.B., Arnold M., Hillebrand J.J., Geary N., Langhans W. Intrameal hepatic portal and intraperitoneal infusions of glucagon-like peptide-1 reduce spontaneous meal size in the rat via different mechanisms. Endocrinology 2009, 150:1174-1181.
104. Moran T.H. Differential effects of peptide combination on food intake. Proceedings of the First Swiss Winter Conference on Ingestive Behavior 2009, St. Moritz, Switzerland:36.
105. Riediger T., Lutz T., Schmid H.A., Scharrer E. The area postrema as a major target for peptides controlling food intake. Soc Neurosci Abstr 2000, 30. 396.10.
106. Roth J., Coffey T., Jodka C., Maier H., Athanacio J., Mack C., et al. Combination therapy with amylin and PYY[3 36] in obese rodents: anorexigenic synergy and weight loss additivity. Endocrinology 2007.
107. Riediger T., Michel S., Becskei C., Lutz T.A. Diet-derived nutrients and PYY modulate the effects of amylin on c-Fos expression in the area postrema and on food intake. Neuroscience Meeting Planner San Diego, CA: Society for Neuroscience 2007, online 2007;Program No. 299.07.
108. Osto M., Wielinga P.Y., Alder B., Walser N., Lutz T.A. Modulation of the satiating effect of amylin by central ghrelin, leptin and insulin. Physiol Behav 2007, 91:566-572.
109. Hayes M.R., Skibicka K.P., Leichner T.M., Guarnieri D.J., DiLeone R.J., Bence K.K., et al. Endogenous leptin signaling in the caudal nucleus tractus solitarius and area postrema is required for energy balance regulation. Cell Metab 2010, 11:77-83.