Central and peripheral administration of secretin inhibits food intake in mice through the activation of the melanocortin system

Neuropsychopharmacology

Volumn 36, Issue 2, 2011, Pages 459-471

  Cheng, Carrie Yuen Yee ^a   Chu, Jessica Yan Shuen ^a   Chow, Billy Kwok Chong ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

arcuate nucleus; feeding; melanocortin system; proopiomelanocortin; secretin; secretin receptor

Indexed keywords

MELANOCORTIN; MELANOCORTIN 4 RECEPTOR; MESSENGER RNA; N ACETYL ALPHA INTERMEDIN[4-10]CYCLO[4 NORLEUCINE 5 ASPARTIC ACID 7 [3 (2 NAPHTHYL)ALANINE] 10 LYSINAMIDE]; PROOPIOMELANOCORTIN; PROTEIN FOS; SECRETIN; THYROTROPIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME IMMUNOASSAY; FEEDING BEHAVIOR; FOOD INTAKE; GENE EXPRESSION; HYPOTHALAMUS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LASER CAPTURE MICRODISSECTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; TASTE AVERSION; THALAMUS MIDLINE NUCLEUS; THYROTROPIN RELEASE;

ANIMALS; APPETITE DEPRESSANTS; APPETITE REGULATION; ARCUATE NUCLEUS; DOWN-REGULATION; FEEDING BEHAVIOR; HYPOTHALAMUS; INJECTIONS, INTRAPERITONEAL; INJECTIONS, INTRAVENTRICULAR; MALE; MICE; MICE, KNOCKOUT; NEURONS; PRO-OPIOMELANOCORTIN; RANDOM ALLOCATION; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, GASTROINTESTINAL HORMONE; SECRETIN;

EID: 78650180262     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2010.178     Document Type: Article

References (85)

1. Asakawa A, Inui A, Yuzuriha H, Ueno N, Katsuura G, Fujimiya M et al (2003). Characterization of the effects of pancreatic polypeptide in the regulation of energy balance. Gastroenterology 124: 1325-1336.
2. Batterham RL, Cohen MA, Ellis SM, Le Roux CW, Roux CW, Withers DJ et al (2003a). Inhibition of food intake in obese subjects by peptide YY3-36. N Engl J Med 349: 941-948.
3. Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL et al (2002). Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 418: 650-654.
4. Batterham RL, Le Roux CW, Cohen MA, Park AJ, Ellis SM, Patterson M et al (2003b). Pancreatic polypeptide reduces appetite and food intake in humans. J Clin Endocrinol Metab 88: 3989-3992. (Pubitemid 37034556)
5. Bayliss WM, Starling EH (1902). The mechanism of pancreatic secretion. J Physiol 28: 325-353.
6. 0Amato M, Drewe J (2001). Loxiglumide, a CCK-A receptor antagonist, stimulates calorie intake and hunger feelings in humans. Am J Physiol Regul Integr Comp Physiol 280: R1149-R1154.
7. Benoit SC, Air EL, Coolen LM, Strauss R, Jackman A, Clegg DJ et al (2002). The catabolic action of insulin in the brain is mediated by melanocortins. J Neurosci 20: 9048-9052.
8. Boden G, Essa N, Owen OE, Reichle FA (1974). Effects of intraduodenal administration of HCl and glucose on circulating immunoreactive secretin and insulin concentrations. J Clin Invest 53: 1185-1193.
9. Broadwell RD, Brightman MW (1976). Entry of peroxidase into neurons of the central and peripheral nervous systems from extracerebral and cerebral blood. J Comp Neurol 166: 257-283.
10. Broberger C, Johansen J, Johansson C, Schalling M, Hokfelt T (1998). The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium gluta-mate-treated mice. Proc Natl Acad Sci USA 95: 15043-15048.
11. Challis BG, Pinnock SB, Coll AP, Carter RN, Dickson SL, O'Rahilly S (2003). Acute effects of PYY3-36 on food intake and hypothalamic neuropeptide expression in the mouse. Biochem Biophys Res Commun 311: 915-919.
12. Charlton CG, O'Donohue TL, Miller RL, Jacobowitz DM (1981). Secretin immunoreactivity in rat and pig brain. Peptides 2(Suppl 1): 45-49.
13. Chisholm DJ, Young JD, Lazarus L (1969). The gastrointestinal stimulus to insulin release. I. Secretin. J Clin Invest 48: 1453-1460.
14. Chu JY, Lee LT, Lai CH, Vaudry H, Chan YS, Yung WH et al (2009). Secretin as a neurohypophysial factor regulating body water homeostasis. Proc Natl Acad Sci USA 106: 15961-15966.
15. Chu JY, Yung WH, Chow BK (2006). Endogenous release of secretin from the hypothalamus. Ann N Y Acad Sci 1070: 196-200.
16. Cohen MA, Ellis SM, Le Roux CW, Batterham RL, Park A, Patterson M et al (2003). Oxyntomodulin suppresses appetite and reduces food intake in humans. J Clin Endocrinol Metab 88: 4696-4701. (Pubitemid 37357514)
17. Cone RD, Cowley MA, Butler AA, Fan W, Marks DL, Low MJ (2001). The arcuate nucleus as a conduit for diverse signals relevant to energy homeostasis. Int J Obes Relat Metab Disord 5: S63-S67.
18. Cowley MA, Smart JL, Rubinstein M, Cerdán MG, Diano S, Horvath TL et al (2001). Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411: 480-484.
19. Dakin CL, Small CJ, Park AJ, Seth A, Ghatei MA, Bloom SR (2002). Repeated ICV administration of oxyntomodulin causes a greater reduction in body weight gain than in pair-fed rats. Am J Physiol Endocrinol Metab 283: E1173-E1177.
20. Dakin CL, Gunn I, Small CJ, Edwards CM, Hay DL, Smit h DM et al (2001). Oxyntomodulin inhibits food intake in the rat. Endocrinology 142: 4244-4250.
21. Dakin CL, Small CJ, Batterham RL, Neary NM, Cohen MA, Patterson M et al (2004). Peripheral oxyntomodulin reduces food intake and body weight gain in rats. Endocrinology 145: 2687-2695.
22. Diaco JF, Miller LD, Kuo PT, Feng LY, Sugerman HJ (1971). Effects of secretin on serum immunoreactive insulin and insulin-like activity. Ann Surg 173: 578-582.
23. Dogrukol-Ak D, Tore F, Tuncel N (2004). Passage of VIP/PACAP/ secretin family across the blood-brain barrier: therapeutic effects. Curr Pharm Des 10: 1325-1340.
24. Domschke W, Greenberg GR, Domschke S, Bloom SR, Mitznegg P, Sprugel W et al (1977). Endogenous acid releases secretin in man. Acta Hepatogastroenterol (Stuttg) 24: 262-263.
25. Elias CF, Lee C, Kelly J, Aschkenasi C, Ahima RS, Couceyro PR et al (1998). Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron 21: 1375-1385.
26. Elmquist JK, Ahima RS, Maratos-Flier E, Flier JS, Saper CB (1997). Leptin activates neurons in ventrobasal hypothalamus and brainstem. Endocrinology 138: 839-842.
27. Fekete C, Légrádi G, Mihály E, Huang QH, Tatro JB, Rand WM et al (2000). alpha-Melanocyte-stimulating hormone is contained in nerve terminals innervating thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventri-cular nucleus and prevents fasting-induced suppression of prothyrotropin-releasing hormone gene expression. J Neurosci 20: 1550-1558.
28. Fekete C, Sarkar S, Rand WM, Harney JW, Emerson CH, Bianco AC et al (2002). Agouti-related protein (AGRP) has a central inhibitory action on the hypothalamic-pituitary-thyroid (HPT) axis; comparisons between the effect of AGRP and neuropeptide Y on energy homeostasis and the HPT axis. Endocrinology 143: 3846-3853.
29. Gerber JG, Payne NA (1996). Secretin inhibits canine gastric acid secretion in response to pentagastrin by modulating gastric histamine release. J Pharmacol Exp Ther 279: 718-723.
30. Gibbs J, Young RC, Smith GP (1973). Cholecystokinin decreases food intake in rats. J Comp Physiol Psychol 84: 488-495.
31. Glick Z, Thomas DW, Mayer J (1971). Absence of effect of injections of the intestinal hormones secretin and choecystoki-nin-pancreozymin upon feeding behavior. Physiol Behav 6: 5-8.
32. Gray MA, Greenwell JR, Argent BE (1988). Secretin-regulated chloride channel on the apical plasma membrane of pancreatic duct cells. J Membr Biol 105: 131-142.
33. Greenberg GR, McCloy RF, Baron JH, Bryant MG, Bloom SR (1982). Gastric acid regulates the release of plasma secretin in man. Eur J Clin Invest 12: 361-372.
34. Grovum WL (1981). Factors affecting the voluntary intake of food by sheep. 3. The effect of intravenous infusions of gastrin, cholecystokinin and secretin on motility of the reticulo-rumen and intake. Br J Nutr 45: 183-201.
35. Hakansson ML, Hulting AL, Meister B (1996). Expression of leptin receptor mRNA in the hypothalamic arcuate nucleus-relationship with NPY neurones. Neuroreport 7: 3087-3092.
36. Hahn TM, Breininger JF, Baskin DG, Schwartz MW (1998). Coexpression of Agrp and NPY in fasting-activated hypotha-lamic neurons. Nat Neurosci 1: 271-272.
37. Hewson AK, Dickson SL (2000). Systemic administration of ghrelin induces Fos and Egr-1 proteins in the hypothalamic arcuate nucleus of fasted and fed rats. J Neuroendocrinol 12: 1047-1049.
38. Hewson G, Leighton GE, Hill RG, Hughes J (1988). The cholecystokinin receptor antagonist L364,718 increases food intake in the rat by attenuation of the action of endogenous cholecystokinin. Br J Pharmacol 93: 79-84.
39. Jin HO, Lee KY, Chang TM, Chey WY, Dubois A (1994). Secretin: a physiological regulator of gastric emptying and acid output in dogs. Am J Physiol 267(4 Pt 1): G702-G708.
40. Köves K, Kausz M, Reser D, Illyés G, Takács J, Heinzlmann A et al (2004). Secretin and autism: a basic morphological study about the distribution of secretin in the nervous system. Regul Pept 123: 209-216.
41. Kamegai J, Tamura H, Shimizu T, Ishii S, Sugihara H, Wakabayashi I (2000). Central effect of ghrelin, an endogenous growth hormone secretagogue, on hypothalamic peptide gene expression. Endocrinology 141: 4797-4800.
42. Kanno N, LeSage G, Glaser S, Alpini G (2001). Regulation of cholangiocyte bicarbonate secretion. Am J Physiol Gastrointest Liver Physiol 281: G612-G625.
43. Kissileff HR, Pi-Sunyer FX, Thornton J, Smith GP (1981). C-terminal octapeptide of cholecystokinin decreases food intake in man. Am J Clin Nutr 34: 154-160.
44. Kofod H (1986). Secretin N-terminal hexapeptide potentiates insulin release in mouse islets. Regul Pept 15: 229-237. (Pubitemid 16027766)
45. Konturek SJ, Zabielski R, Konturek JW, Czarnecki J (2003). Neuroendocrinology of the pancreas; role of brain-gut axis in pancreatic secretion. Eur J Pharmacol 481: 1-14.
46. Kraegen EW, Chisholm DJ, Young JD, Lazarus L (1970). The gastrointestinal stimulus to insulin release. II. A dual action of secretin. J Clin Invest 49: 524-529.
47. Kristensen P, Judge ME, Thim L, Ribel U, Christjansen KN, Wulff BS et al (1998). Hypothalamic CART is a new anorectic peptide regulated by leptin. Nature 393: 72-76.
48. Lee SM, Chen L, Chow BK, Yung WH (2005). Endogenous release and multiple actions of secretin in the rat cerebellum. Neuroscience 134: 377-386.
49. Lerner RL, Porte Jr D (1970). Uniphasic insulin responses to secretin stimulation in man. J Clin Invest 49: 2276-2280.
50. Lerner RL, Porte Jr D (1972). Studies of secretin-stimulated insulin responses in man. J Clin Invest 51: 2205-2210.
51. Malaisse-Lagae F, Carpentier JL, Patel YC, Malaisse WJ, Orci L (1977). Pancreatic polypeptide: a possible role in the regulation of food intake in the mouse. Hypothesis. Experientia 33: 915-917.
52. 0 Shea D, Edwards CM, Turton MD, Heath MM, Gunn I et al (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.
53. Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K et al (2001). A role for ghrelin in the central regulation of feeding. Nature 409: 194-198.
54. Ng SS, Yung WH, Chow BK (2002). Secretin as a neuropeptide. Mol Neurobiol 26: 97-107.
55. Nussdorfer GG, Bahcelioglu M, Neri G, Malendowicz LK (2000). Secretin, glucagon, gastric inhibitory polypeptide, parathyroid hormone, and related peptides in the regulation of the hypothalamus- pituitary-adrenal axis. Peptides 21: 309-324.
56. O'Donohue TL, Charlton CG, Miller RL, Boden G, Jacobowitz DM (1981). Identification, characterization, and distribution of secretin immunoreactivity in rat and pig brain. Proc Natl Acad Sci USA 78: 5221-5224.
57. Paxinos G, Franklin KB (2001). The Mouse Brain in Stereotaxic Coordinates. Academic Press: San Diego.
58. Peruzzo B, Pastor FE, Blázquez JL, Schöbitz K, Peláez B, Amat P et al (2000). A second look at the barriers of the medial basal hypothalamus. Exp Brain Res 132: 10-26.
59. Rhodes RA, Skerven G, Chey WY, Chang TM (1988). Acid-independent release of secretin and cholecystokinin by intra-duodenal infusion of fat in humans. Pancreas 3: 391-398.
60. Rodbell M, Birnbaumer L, Pohl SL (1970). Adenyl cyclase in fat cells. 3. Stimulation by secretin and the effects of trypsin on the receptors for lipolytic hormones. J Biol Chem 245: 718-722.
61. Rudman D, Del Rio AE (1969). Lipolytic activity of synthetic porcine secretin. Endocrinology 85: 214-217.
62. Schaffalitzky de Muckadell OB, Fahrenkrug J (1978). Secretion pattern of secretin in man: regulation by gastric acid. Gut 19: 812-818.
63. Shiratori K, Watanabe S, Takeuchi T (1992). Role of endogenous secretin and cholecystokinin in intraduodenal oleic acid-induced inhibition of gastric acid secretion in rats. Dig Dis Sci 37: 397-402.
64. Sipols AJ, Baskin DG, Schwartz MW (1995). Effect of intracer- ebroventricular insulin infusion on diabetic hyperphagia and hypothalamic neuropeptide gene expression. Diabetes 44: 147-151.
65. Stephens TW, Basinski M, Bristow PK, Bue-Valleskey JM, Burgett SG, Craft L et al (1995). The role of neuropeptide Y in the antiobesity action of the obese gene product. Nature 377: 530-532.
66. Tamura H, Kamegai J, Shimizu T, Ishii S, Sugihara H, Oikawa S (2002). Ghrelin stimulates GH but not food intake in arcuate nucleus ablated rats. Endocrinology 143: 3268-3275.
67. Tang-Christensen M, Vrang N, Larsen PJ (2001). Glucagon-like peptide containing pathways in the regulation of feeding behaviour. Int J Obes Relat Metab Disord 25(Suppl 5): S42-S47.
68. Tay J, Goulet M, Rusche J, Boismenu R (2004). Age-related and regional differences in secretin and secretin receptor mRNA levels in the rat brain. Neurosci Lett 366: 176-181.
69. Tschop M, Smiley DL, Heiman ML (2000). Ghrelin induces adiposity in rodents. Nature 407: 908-913.
70. Tschop M, Smiley DL, Heiman ML (2000). Ghrelin induces adiposity in rodents. Nature 407: 908-913.
71. Turton MD, O'Shea D, Gunn I, Beak SA, Edwards CM, Meeran K et al (1996). A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 379: 69-72. (Pubitemid 26008136)
72. Ueno N, Inui A, Iwamoto M, Kaga T, Asakawa A, Okita M et al (1999). Decreased food intake and body weight in pancreatic polypeptide-overexpressing mice. Gastroenterology 117: 1427-1432.
73. van Houten M, Posner BI, Kopriwa BM, Brawer JR (1979). Insulin-binding sites in the rat brain: in vivo localization to the circumventricular organs by quantitative radioautography. Endocrinology 105: 666-673.
74. Vaudry D, Gonzalez BJ, Basille M, Yon L, Fournier A, Vaudry H (2000). Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Rev 52: 269-324.
75. Verdich C, Flint A, Gutzwiller JP, Naslund E, Beglinger C, Hellstrom PM et al (2001). A meta-analysis of the effect of glucagon-like peptide-1 (7-36) amide on ad libitum energy intake in humans. J Clin Endocrinol Metab 86: 4382-4389.
76. Wang L, Saint-Pierre DH, Tache Y (2002). Peripheral ghrelin selectively increases Fos expression in neuropeptide YFsynthesizing neurons in mouse hypothalamic arcuate nucleus. Neurosci Lett 325: 47-51.
77. Welch MG, Keune JD, Welch-Horan TB, Anwar N, Anwar M, Ludwig RJ et al (2004a). Secretin: hypothalamic distribution and hypothesized neuroregulatory role in autism. Cell Mol Neurobiol 24: 219-241.
78. Welch MG, Keune JD, Welch-Horan TB, Anwar N, Anwar M, Ludwig RJ et al (2004b). Secretin: hypothalamic distribution and hypothesized neuroregulatory role in autism. Cell Mol Neurobiol 24: 219-241.
79. WHO (2010). Obesity and Overweight-Facts about Overweight and Obesity. WHO: Geneva.
80. Willesen MG, Kristensen P, Romer J (1999). Colocalization of growth hormone secretagogue receptor and NPY mRNA in the arcuate nucleus of the rat. Neuroendocrinology 70: 306-316.
81. Wren AM, Small CJ, Abbott CR, Dhillo WS, Seal LJ, Cohen MA et al (2001). Ghrelin causes hyperphagia and obesity in rats. Diabetes 50: 2540-2547.
82. Wren AM, Small CJ, Ward HL, Murphy KG, Dakin CL, Taheri S et al (2000). The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology 141: 4325-4328.
83. Yamamoto H, Kishi T, Lee CE, Choi BJ, Fang H, Hollenberg AN et al (2003). Glucagon-like peptide-1-responsive catecholamine neurons in the area postrema link peripheral glucagon-like peptide-1 with central autonomic control sites. J Neurosci 23: 2939-2946.
84. Yang H, Wang L, Wu SV, Tay J, Goulet M, Boismenu R et al (2004). Peripheral secretin-induced Fos expression in the rat brain is largely vagal dependent. Neuroscience 128: 131-141.
85. You CH, Chey WY (1987). Secretin is an enterogastrone in humans. Dig Dis Sci 32: 466-471.