Vagal control of satiety and hormonal regulation of appetite

Journal of Neurogastroenterology and Motility

Volumn 17, Issue 4, 2011, Pages 338-348

  Owyang, Chung ^a   Heldsinger, Andrea ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Cholecystokinin; Leptin; Nodose ganglion; Signal transduction

Indexed keywords

EID: 80054887760     PISSN: 20930879     EISSN: 20930887     Source Type: Journal    
DOI: 10.5056/jnm.2011.17.4.338     Document Type: Review

References (112)

1. Thorens B. Glucose sensing and the pathogenesis of obesity and type 2 diabetes. Int J Obes 2008;32(suppl 6):S62-S71.
2. Savage LM, Ramos RL. Reward expectation alters learning and memory: the impact of the amygdala on appetite-driven behaviors. Behav Brain Res 2009;198:1-12.
3. German J, Kim F, Schwartz GJ, et al. Hypothalamic leptin signaling regulates hepatic insulin sensitivity via a neurocircuit involving the vagus nerve. Endocrinology 2009;150:4502-4511.
4. Cone RD. Anatomy and regulation of the central melanocortin system. Nat Neurosci 2005;8:571-578.
5. Blouet C, Jo YH, Li X, Schwartz GJ. Mediobasal hypothalamic leucine sensing regulates food intake through activation of a hypothalamus-brainstem circuit. J Neurosci 2009;29:8302-8311.
6. Maclagan NF. The role of appetite in the control of body weight. J Physiol 1937;90:385-394.
7. Gibbs J, Young RC, Smith GP. Cholecystokinin decreases food intake in rats. J Comp Physiol Psychol 1973;84:488-495.
8. Ritter RC, Covasa M, Matson CA. Cholecystokinin: proofs and prospects for involvement in control of food intake and body weight. Neuropeptides 1999;33:387-399.
9. Rogers RC, Hermann GE. Mechanisms of action of CCK to activate central vagal afferent terminals. Peptides 2008;29:1716-1725.
10. Villanueva EC, Myers MG Jr. Leptin receptor signaling and the regulation of mammalian physiology. Int J Obes (Lond) 2008;32(suppl 7):S8-S12.
11. Peter JH, Karpiel AB, Ritter RC, Simasko SM. Cooperative activation of cultured vagal afferent neurons by leptin and cholecystokinin. Endocrinology 2004;145:3652-3657.
12. Peters JH, Ritter RC, Simasko SM. Leptin and CCK modulate complementary background conductances to depolarize cultured nodose neurons. Am J Physiol Cell Physiol 2006;290:C427-C432.
13. Barrachina MD, Martínez V, Wang L, Wei JY, Taché Y. Synergistic interaction between leptin and cholecystokinin to reduce short-term food intake in lean mice. Proc Natl Acad Sci USA 1997;94:10455-10460.
14. Heldsinger A, Grabauskas G, Song I, Owyang C. Synergistic interaction between leptin and CCK in the rat nodose ganglia is mediated by PI3 kinase and STAT3 signaling pathways: implications for leptin as a regulator of short-term satiety. J Biol Chem 2011;286: 11707-11715.
15. Buchan AM, Polak JM, Solcia E, Capella C, Hudson D, Pearse AG. Electron immunohistochemical evidence for the human intestinal I cell as the source of CCK. Gut 1978;19:403-407.
16. Polak JM, Bloom SR, Rayford PL, Pearse AG, Buchan AM, Thompson JC. Identification of cholecystokinin-secreting cells. Lancet 1975;2:1016-1018.
17. Lee MC, Schiffman SS, Pappas TN. Role of neuropeptides in the regulation of feeding behavior: a review of cholecystokinin, bombesin, neuropeptide Y, and galanin. Neurosci Biobehav Rev 1994;18:313-323.
18. Crawley JN, Corwin RL. Biological actions of cholecystokinin. Peptides 1994;15:731-755.
19. Weller A, Smith GP, Gibbs J. Endogenous cholecystokinin reduces feeding in young rats. Science 1990;247:1589-1591.
20. Lewis LD, Williams JA. Regulation of cholecystokinin secretion by food, hormones, and neural pathways in the rat. Am J Physiol 1990;258(4 Pt 1):G512-G518.
21. Maclagan NF. The role of appetite in the control of body weight. J Physiol 1937;90:385-394.
22. Gibbs J, Young RC, Smith GP. Cholecystokinin decreases food intake in rats. J Comp Physiol Psychol 1973;84:488-495.
23. Baldwin BA, Parrott RF, Ebenezer IS. Food for thought: a critique on the hypothesis that endogenous CCK acts as a physiological satiety factor. Prog Neurobiol 1998;55:477-507.
24. Passaro E Jr, Debas H, Oldendorf W, Yamada T. Rapid appearance of intraventricularly administered neuropeptides in the peripheral circulation. Brain Res 1982;241:355-340.
25. Smith GP, Jerome C, Norgren R. Afferent axons in abdominal vagus mediated satiety effect of CCK in rats. Am J Physiol 1985; 249(5 Pt 2):R638-R641.
26. Ritter RC, Ladenheim EE. Capsaicin pretreatment attenuates suppression of food intake by CCK. Am J Physiol 1985;248(4 Pt 2):R501-R504.
27. Dourish CT, Rucket AC, Tattersall FD, Iversen SD. Evidence that decreased feeding induced by systemic injection of CCK is mediated by CCK-A receptors. Eur J Pharmacol 1989;173:233-234.
28. Smith GP, Jerome C, Cushin BJ, Eterno R, Simansky KJ. Abdominal vagotomy blocks the satiety effects of cholecystokinin in the rat. Science 1981;213:1036-1037.
29. Melville LD, Smith GP, Gibbs J. Devazepide antagonized the inhibitory effect of cholocystokinin in sham-feeding rats. Pharmacol Biochem Behav 1992;43:975-977.
30. Ebenezer IS. The effects of a peripherally acting cholecystokinin1 receptor antagonist on food intake in rats: implications for the cholecystokinin-satiety hypothesis. Eur J Pharmacol 2003;461:113-118.
31. Covasa M, Marcuson JK, Ritter RC. Diminished satiation in rats exposed to elevated levels of endogenous or exogenous cholecystokinin. Am J Physiol Regul Integr Comp Physiol 2001;280:R331-R337.
32. Hewson G, Leighton GE, Hill RG, Hughes J. The cholecystokinin receptor antagonist L364,718 increases food intake in the rat by attenuating the action of endogenous cholecystokinin. Br J Pharmacol 1988;93:79-84.
33. Ebenezer IS, de la Riva C, Baldwin BA. Effects of the CCK receptor antagonist MK-329 on food intake in pigs. Phsyiol Behav 1990;47:145-148.
34. Silver AJ, Flood JF, Song AM, Morley JE. Evidence for a physiological role for CCK in the regulation of food intake in mice. Am J Physiol 1989;256(3 Pt 2):R646-R652.
35. Weatherford SC, Chiruzzo FY, Laughton WB. Satiety induced by endogenous and exogenous cholecystokinin is mediated by CCK-A receptors in mice. Am J Physiol 1993;262(4 Pt 2):R574-R578.
36. Covasa M, Forbes JM. Effects of the CCK receptor antagonist MK-329 on food intake in broiler chickens. Pharmacol Biochem Behav 1994;48:479-486.
37. Cheng CA, Geoghegan JG, Lawson DC, Berlangieri SU, Akwari O, Pappas TN. Central and peripheral effects of CCK receptor antagonists on satiety in dogs. Am J Physiol 1993;265(2 Pt 1):G219-G223.
38. Bado A, Duriex C, Moizo L, Rogues BP, Lewn MJ. Cholecystokinin-A receptor mediation of food intake in cats. Am J Physiol 1991;256(4 Pt 2):R693-R697.
39. Zarbin MA, Wamsley JK, Innis RB, Kuhar MJ. Cholecystokinin receptors: presence and axonal flow in the rat vagus nerve. Life Sci 1981;29:697-705.
40. Moran TH, Smith GP, Hostetler AM, McHugh PR. Transport of cholecystokinin (CCK) binding sites in subdiaphragmatic vagal branches. Brain Res 1987;415:149-152.
41. Li Y, Zhang XC, Wang LM, Renenan EW, Fogel R, Owyang C. Vagal afferent pathway mediates physiological action of CCK on pancreatic enzyme secretion: pancreatic secretion, neurophysiological and receptor autoradiographic studies. Gastroenterology 1993;104:A837.
42. Blackshaw LA, Grundy D. Effect of cholecystokinin on two classes of gastroduodenal vagal afferent fibers. J Auton Nerv Syst 1990;31:191-201.
43. Sankaran H, Goldfine ID, Bailey A, Licko V, Williams JA. Relationship of cholecystokinin receptor binding to regulation of biological functions in pancreatic acini. Am J Physiol 1982;242:G250-G257.
44. Villanueva ML, Collins SM, Jensen RT, Gardner JD. Structural requirements for action of cholecystokinin on enzyme secretion from pancreatic acini. Am J Physiol 1982;242:G416-G422.
45. Li Y, Zhu J, Owyang C. Electrical physiological evidence for high and low-affinity vagal CCK-A receptors. Am J Physiol 1999;277(2 Pt 1):G469-G477.
46. Weatherford SC, Laughton WB, Salabarria J, et al. CCK satiety is differentially mediated by high- and low-affinity CCK receptors in mice and rats. Am J Physiol 1993;264(2 Pt 2):R244-R249.
47. Schwartz GJ, McHugh PR, Moran TH. Pharmacological dissociation of responses to CCK and gastric loads in rat mechanosensitive vagal afferents. Am J Physiol 1994;267(1 Pt 2):R303-R308.
48. Li Y, Hao Y, Owyang C. High-affinity CCK-A receptors on the vagus nerve mediate CCK-stimulated pancreatic secretion in rats. Am J Physiol 1997;273(3 Pt 1):G679-G685.
49. Burdyga G, Spiller D, Morris R, et al. Expression of the leptin receptor in rat and human nodose ganglion neurons. Neuroscience 2002;109:339-347.
50. Burdyga G, Varro A, Dimaline R, Thompson DG, Dockray GJ. Ghrelin receptors in rat and human nodose ganglia: putative role in regulating CB-1 and MCH receptor abundance. Am J Physiol Gastrointest Liver Physiol 2006;290:G1289-G1297.
51. Burdyga G, Lal S, Varro A, Dimaline R, Thompson DG, Dockray GJ. Expression of cannabinoid CB1 receptors by vagal afferent neurons is inhibited by the cholecystokinin. J Neurosci 2004;24:2708-2715.
52. Burdyga G, Lal S, Spiller D, et al. Localization of orexin-1 receptors to vagal afferent neurons in the rat and humans. Gastroenterology 2003;124:129-139.
53. Burdyga G, Varro A, Dimaline R, Thompson DG, Dockray GJ. Feeding-dependent depression of melanin-concentrating hormone and melanin-concentrating hormone receptor-1 expression in vagal afferent neurones. Neuroscience 2006;137:1405-1415.
54. Date Y, Toshinai K, Koda S, et al. Peripheral interaction of ghrelin with cholecystokinin on feeding regulation. Endocrinology 2005;146:3518-3525.
55. De Lartigue G, Dimaline R, Varro A, Dockray GJ. Cocaine- and amphetamine-regulated transcript: stimulation of expression in rat vagal afferent neurons by cholecystokinin and suppression by ghrelin. J Neurosci 2007;27:2876-2882.
56. Moran TH, Katz LF, Plata-Salaman CR, Schwartz GJ. Disordered food intake and obesity in rats lacking cholecystokinin A receptors. Am J Physiol 1998;274(3 Pt 2):R618-R625.
57. Nakamura H, Kihara Y, Tashiro M, et al. Defects of cholecystokinin (CCK)-A receptor gene expression and CCK-A receptormediated biological functions in Otsuka Long-Evans Tokushima Fatty (OLETF) rats. J Gastroenterol 1998;33:702-709.
58. Miller LJ, Holicky EL, Ulrich CD, Wieben ED. Abnormal processing of the human cholecystokinin receptor gene in association with gallstones and obesity. Gastroenterology 1995;109:1375-1380.
59. Schneider H, Sänger P, Hanisch E. In vitro effects of cholecystokinin fragments on human gallbladders. Evidence for an altered CCK-receptor structure in a subgroup of patients with gallstones. J Hepatol 1997;26:1063-1068.
60. Campfield LA, Smith FJ, Guisez Y, Devos R, Burn P. Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 1995;269:546-549.
61. Halaas JL, Gajiwala KS, Maffei M, et al. Weight-reducing effects of the plasma protein encoded by the obese gene. Science 1995;269:543-546.
62. Loftus TM. An adipocyte-central nervous system regulatory loop in the control of adipose homeostasis. Semin Cell Biol 1999;10:11-18.
63. Considine RV, Sinha MK, Heiman ML, et al. Serum immunoreactiveleptin concentration in normal weight and obese humans. N Engl J Med 1996;334:292-295.
64. Robertson SA, Leinninger GM, Myers MG Jr. Molecular and neural mediators of leptin action. Physiol Behav 2008;94:637-642.
65. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature 1994;372:425-432.
66. Bado A, Levaseur S, Attoub S, et al. The stomach is a source of leptin. Nature 1998;394:790-793.
67. Sobhani I, Bado A, Vissuzaine C, et al. Leptin secretion and leptin receptor in the human stomach. Gut 2000;47:178-183.
68. Pelleymounta MA, Cullon MJ, Baker MB, et al. Effects of the obese gene product on body weight regulation in ob/ob mice. Science 1995;269:540-543.
69. Levin N, Nelson C, Gurney A, Vandlen R, de Sanvege F. Decreased food intake does not completely account for adiposity reduction after ob protein infusion. Proc Natl Acad Sci USA 1996;93:1726-1730.
70. Chen G, Koyama K, Yuan X, et al. Disappearance of body fat in normal rats induced by adenovirus-mediated leptin gene therapy. Proc Natl Acad Sci USA 1996;93:14795-14799.
71. Barachina MD, Martínez V, Wei JY, Taché Y. Leptin-induced decrease in food intake is not associated with changes in gastric emptying in lean mice. Am J Physiol 1997;272(3 Pt 2):R1007-R1011.
72. Yuan CS, Dey L, Xie JT, Aung HH. Gastric effects of galanin and its interaction with leptin on brainstem neuronal activity. J Pharmacol Exp Ther 2002;301:488-493.
73. Moran TH, Ameglio PJ, Schwartz GJ, McHugh PR. Blockade of type A, not type B, CCK receptors attenuates satiety actions on exogenous and endogenous CCK. Am J Physiol 1992;262(Pt 2):R46-R50.
74. Ritta RC, Covasa M, Matson CA. Cholecystokinin: proofs and prospects for involvement in control of food intake and body weight. Neuropeptides 1999;33:387-399.
75. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature 2000;404: 661-671.
76. Cowley MA, Smart JL, Rubinstein M, et al. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 2001;411:480-484.
77. Kievit P, Howard JK, Badman MK, et al. Enhanced leptin sensitivity and improved glucose homeostasis in mice lacking suppressor of cytokine signaling-3 in POMC-expressing cells. Cell Metabolism 2006;4:123-132.
78. Obici S, Feng Z, Tan J, Liu L, Karkanias G, Rossetti L. Central melanocortin receptors regulate insulin action. J Clin Invest 2001;108:1079-1085.
79. Dungan HM, Clifton DK, Steiner RA. Minireview: kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion. Endocrinology 2006;147:1154-1158.
80. Rondini TA, Baddini SP, Sousa LF, Bittencourt JC, Elias CF. Hypothalamic cocaine- and amphetamine-regulated transcript neurons project to areas expressing gonadotropin releasing hormone immunoreactivity and to the anteroventral periventricular nucleus in male and female rats. Neuroscience 2004;125:735-748.
81. Harris M, Aschkenasi C, Elias CF, et al. Transcriptional regulation of the thyrotropin-releasing hormone gene by leptin and melanocortin signaling. J Clin Invest 2001;107:111-120.
82. Elmquist JK, Coppari R, Balthasar N, Ichinose M, Lowell BB. Identifying hypothalamic pathways controlling food intake, body weight, and glucose homeostasis. J Comp Neurol 2005;493:63-71.
83. Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz MW. Central nervous system control of food intake and body weight. Nature 2006;443:289-295.
84. Elmquist JK, Elias CF, Saper CB. From lesions to leptin: hypothalamic control of food intake and body weight. Neuron 1999;22: 221-232.
85. Elmquist JK, Bjørbaek C, Ahima RS, Flier JS, Saper CB. Distributions of leptin receptor mRNA isoforms in the rat brain. J Comp Neurol 1998;395:535-547.
86. Baskin DG, Schwartz MW, Seeley RJ, et al. Leptin receptor long-form splice-variant protein expression in neuron cell bodies of the brain and co-localization with neuropeptide Y mRNA in the arcuate nucleus. J Histochem Cytochem 1999;47:353-362.
87. Marsh DJ, Hollopeter G, Huszar D, et al. Response of melanocortin-4 receptor-deficient mice to anorectic and orexigenic peptides. Nat Genet 1999;21:119-122.
88. Ste Marie L, Miura GI, Marsh DJ, Yagaloff K, Palmiter RD. A metabolic defect promotes obesity in mice lacking melanocortin-4 receptors. Proc Natl Acad Sci USA 2000;97:12339-12344.
89. Bates SH, Stearns WH, Dundon TA, et al. STAT3 signaling is required for leptin regulation of energy balance but not reproduction. Nature 2003;421:856-859.
90. Björnholm M, Münzberg H, Leshan RL, et al. Mice lacking inhibitory leptin receptor signals are lean with normal endocrine function. J Clin Invest 2007;117:1354-1360.
91. Gao Q, Wolfgang MJ, Neschen S, et al. Disruption of neural signal transducer and activator of transcription 3 causes obesity, diabetes, infertility, and thermal dysregulation. Proc Natl Acad Sci USA 2004;101:4661-4666.
92. Bjorbak C, Lavery HJ, Bates SH, et al. SOCS3 mediates feedback inhibition of the leptin receptor via Tyr985. J Biol Chem 2000;275:40649-40657.
93. Gill HJ. Distributed neural control of energy balance: contributions from hindbrain and hypothalamus. Obesity (Silver Spring) 2006; 14(suppl 5):216S-221S.
94. Buyse M, Ovesjö ML, Goïot H, et al. Expression and regulation of leptin receptor proteins in afferent and efferent neurons of the vagus nerve. Eur J Neurosci 2001;14:64-72.
95. Peiser C, Springer J, Groneberg DA, McGregor GP, Fischer A, Lang RE. Leptin receptor expression in nodose ganglion cells projecting to the rat gastric fundus. Neurosci Lett 2002;320:41-44.
96. Li Y, Wu X, Zhou S, Owyang C. Low-affinity CCK-A receptors are coexpressed with leptin receptors in rat nodose ganglia: implications for leptin as a regulator of short-term satiety. Am J Physiol Gastrointest Liver Physiol 2011;300:G217-G227.
97. Wang YH, Taché Y, Sheibel AB, Go VL, Wei JY. Two types of leptin-responsive gastric vagal afferent terminals: an in vitro single-unit study in rats. Am J Physiol 1997;273(2 Pt 2):R833-R837.
98. Emond M, Schwartz GJ, Ladenhiem EE, Moran TH. Central leptin modulates behavioral and neural responsitivity to CCK. Am J Physiol 1999;276(5 Pt 2):R1545-R1549.
99. Matson CA, Ritter RC. Long-term CCK-leptin synergy suggests a role for CCK in the regulation of body weight. Am J Physiol 1999;276(4 Pt 2):R1038-R1045.
100. Matson CA, Reid DF, Cannon TA, Ritter RC. Cholecystokinin and leptin act synergistically to reduce body weight. Am J Physiol Regul Integr Comp Physiol 2000;278:R883-R890.
101. Yuan CS, Attele AS, Dey Z, Xie JT. Gastric effects of cholecystokinin and its interaction with leptin on brainstem neuronal activity in neonatal rats. J Pharmacol Exp Ther 2000;295:177-182.
102. White DW, Wang DW, Chua SC Jr, et al. Constitutive and impaired signaling of leptin receptors containing the Gln → Pro extracellular domain fatty mutation. Proc Natl Acad Sci USA 1997; 94:10657-10662.
103. Niederau C, Meereis-Schwanke K, Klonowski-Stumpe H, Herberg L. CCK-resistance in Zucker obese vs lean rats. Regul Pept 1997; 70:97-104.
104. Phillips MS, Liu Q, Hammond HA, et al. Leptin receptor missense mutation in the fatty Zucker rat. Nat Genet 1996;13:18-19.
105. Dryden S, King P, Packavance L, Doyle P, Williams G. Divergent effects of intracerebroventricular and peripheral leptin administration on feeding and hypothalamic neuropeptide Y in lean and obese (fa/fa) Zucker rats. Clin Sci (Lond) 1999;96:307-312.
106. De Fanti BA, Backus RC, Hamilton JS, Gietzen DW, Horwitz BA. Lean (Fa/Fa) but not obese (fa/fa) Zucker rats release cholecystokinin at PVN after a gavaged meal. Am J Physiol 1998;275(1 Pt 1):E1-E5.
107. Zhang X, Wrzeszczynska MH, Horvath CM, Darnell JE Jr. Interacting regions in Stat3 and c-Jun that participate in cooperative transcriptional motivation. Mol Cell Biol 1999;19:7138-7146.
108. Covasa M, Ritter RC. Rats maintained on high-fat diets exhibit reduced satiety in response to CCK and bombesin. Peptides 1998;19: 1407-1415.
109. French SJ, Murray B, Rumsey RD, Fadzlin R, Read NW. Adaptation to high-fat diets: effects on eating behavior and plasma cholecystokinin. Br J Nutr 1995;73:179-189.
110. Cunningham KM, Daly J, Horowitz M, Read NW. Gastrointestinal adaptation to diets of differing fat composition in human volunteers. Gut 1991;32:483-486.
111. Covasa M, Ritter RC. Reduced sensitivity to the satiation effect of intestinal oleate in rats adapted to high-fat diet. Am J Physiol 1999; 277(1 Pt 2):R279-R285.
112. De Lartigue G, Barbier de la Serre C, Espero E, Lee J, Raybould HE. Diet-induced obesity leads to the development of leptin resistance in vagal afferent neurons. Am J Physiol Endocrinol Metab 2011;301:E187-E195.