Hindbrain oxytocin receptors contribute to the effects of circulating oxytocin on food intake in male rats

Endocrinology

Volumn 155, Issue 8, 2014, Pages 2845-2857

  Ho, Jacqueline M ^a,b   Anekonda, Vishwanath T ^a   Thompson, Benjamin W ^a   Zhu, Mingyan ^d   Curry, Robert W ^a   Hwang, Bang H ^a   Morton, Gregory J ^b,c   Schwartz, Michael W ^b,c   Baskin, Denis G ^a,b   Appleyard, Suzanne M ^d   Blevins, James E ^a,b  

^a VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CATECHOLAMINES; EATING; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GLUCAGON-LIKE PEPTIDE 1; INJECTIONS, INTRAPERITONEAL; INJECTIONS, INTRAVENTRICULAR; MALE; MICE; MICE, INBRED C57BL; OXYTOCIN; PEPTIDE FRAGMENTS; PRAZOSIN; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OXYTOCIN; SOLITARY NUCLEUS; WEIGHT GAIN;

EID: 84905031782     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1148     Document Type: Article

References (74)

1. Swaab DF, Purba JS, Hofman MA. Alterations in the hypothalamic paraventricular nucleus and its oxytocin neurons (putative satiety cells) in Prader-Willi syndrome: a study of five cases. J Clin Endo-crinol Metab. 1995; 80:573-579.
2. Ramachandrappa S, Raimondo A, Cali AM, et al. Rare variants in single-minded 1 (SIM1) are associated with severe obesity. J Clin Invest. 2013; 123:3042-3050.
3. Sawchenko PE, Swanson LW. Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that projecttothe medullaortothe spinal cordinthe rat. J Comp Neurol. 1982; 205:260-272.
4. Olson BR, Freilino M, Hoffman G.E., Stricker EM, Sved AF, Verbalis JG. c-Fos expression in rat brain and brainstem nuclei in response to treatments that alter food intake and gastric motility. Mol Cell Neu-rosci. 1993; 4:93-106.
5. Blouet C, Jo YH, Li X, Schwartz GJ. Mediobasal hypothalamic leucine sensing regulates food intake through activation of a hypo-thalamus-brainstem circuit. J Neurosci. 2009; 29:8302-8311.
6. Yamashita M, Takayanagi Y, Yoshida M., Nishimori K, Kusama M, Onaka T. Involvement of prolactin-releasing peptide in the activation of oxytocin neurones in response to food intake. J Neuroendo-crinol. 2013; 25:455-465.
7. Peters JH, McDougall SJ, Kellett DO, Jordan D, Llewellyn-Smith IJ, Andresen MC. Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus. J Neurosci. 2008; 28: 11731-11740.
8. Baskin DG, Kim F, Gelling RW, et al. A new oxytocin-saporin cy-totoxin for lesioning oxytocin-receptive neurons in the rat hind-brain. Endocrinology. 2010; 151:4207-4213.
9. Blevins JE, Eakin TJ, Murphy JA, Schwartz M.W., Baskin DG. Oxy-tocin innervation of caudal brainstem nuclei activated by chole-cystokinin. Brain Res. 2003; 993:30-41.
10. Olson BR, Drutarosky MD, Stricker EM, Verbalis JG. Brain oxy-tocin receptor antagonism blunts the effects of anorexigenic treat-mentsinrats: evidence for centraloxytocin inhibitionoffoodintake. Endocrinology. 1991; 129:785-791.
11. Gimpl G, Fahrenholz F. The oxytocin receptor system: structure, function, and regulation. Physiol Rev. 2001; 81:629-683.
12. Tsuda T, Ueno Y, Yoshikawa T, Kojo H., Osawa T. Microarray profiling of gene expression in human adipocytes in response to anthocyanins. Biochemical Pharmacology. 2006; 71:1184-1197.
13. Ohlsson B, Truedsson M, Djerf P, Sundler F. Oxytocin is expressed throughout the human gastrointestinal tract. Regul Pept. 2006; 135: 7-11.
14. Welch MG, Tamir H, Gross KJ, Chen J, Anwar M., Gershon MD. Expression and developmental regulation of oxytocin (OT) and oxytocin receptors (OTR) in the enteric nervous system (ENS) and intestinal epithelium. J Comp Neurol. 2009; 512:256-270.
15. Johnstone LE, Fong TM, Leng G. Neuronal activation in the hypothalamus and brainstem during feeding in rats. Cell Metab. 2006; 4:313-321.
16. Lucio-Oliveira F, Franci CR. Effect of the interaction between food state and the action of estrogen on oxytocinergic system activity. J Endocrinol. 2012; 212:129-138.
17. Renaud LP, Tang M, McCann MJ, Stricker E.M., Verbalis JG. Cho-lecystokinin and gastric distension activate oxytocinergic cells in rat hypothalamus. Am J Physiol. 1987; 253:R661-R665.
18. Ueta Y, Kannan H, Higuchi T, Negoro H., Yamashita H. CCK-8 excites oxytocin-secreting neurons in the paraventricular nucleus in rats-possible involvement of noradrenergic pathway. Brain Res Bull. 1993; 32:453-459.
19. Yamashita M, Takayanagi Y, Yoshida M., Nishimori K, Kusama M, Onaka T. Involvement of prolactin releasing peptide in activation of oxytocin neurones in response to food intake. J Neuroendocrinol. 2013; 25(5):455-465.
20. Olszewski PK, Klockars A, Olszewska AM, Fredriksson R, Schioth H.B., Levine AS. Molecular, immunohistochemical, and pharmacological evidence of oxytocin's role as inhibitor of carbohydrate but not fat intake. Endocrinology. 2010; 151:4736-4744.
21. Zhang G, Cai D. Circadian intervention of obesity development via resting-stage feeding manipulation or oxytocin treatment. Am J Physiol Endocrinol Metab. 2011; 301:E1004-E1012.
22. Carson DS, Hunt GE, Guastella AJ, et al. Systemically administered oxytocin decreases methamphetamine activation of the subthalamic nucleus and accumbens core and stimulates oxytocinergic neurons in the hypothalamus. Addict Biol. 2010; 15:448-463.
23. Hicks C, Jorgensen W, Brown C, et al. The nonpeptide oxytocin receptor agonist WAY 267, 464: receptor-binding profile, prosocial effects and distribution of c-Fos expressionin adolescent rats. J Neu-roendocrinol. 2012; 24:1012-1029.
24. Olson BR, Hoffman GE, Sved AF, Stricker E.M., Verbalis JG. Cho-lecystokinin induces c-fos expressioninhypothalamic oxytocinergic neurons projecting to the dorsal vagal complex. Brain Res. 1992; 569:238-248.
25. Verbalis JG, McCann MJ, McHale CM, Stricker EM. Oxytocin secretion in response to cholecystokinin and food: differentiation of nausea from satiety. Science. 1986; 232:1417-1419.
26. Arletti R, Benelli A, Bertolini A. Influence of oxytocin on feeding behavior in the rat. Peptides. 1989; 10:89-93.
27. Deblon N, Veyrat-Durebex C, Bourgoin L, et al. Mechanisms of the anti-obesity effects of oxytocin indiet-induced obese rats. PloS One. 2011; 6:e25565.
28. Maejima Y, Iwasaki Y, Yamahara Y., Kodaira M, Sedbazar U, Yada T. Peripheral oxytocin treatment ameliorates obesity by reducing food intake and visceral fat mass. Aging. 2011; 3:1169-1177.
29. Morton GJ, Thatcher BS, Reidelberger RD, et al. Peripheral oxy-tocin suppresses food intake and causes weight loss in diet-induced obese rats. Am J Physiol Endocrinol Metab. 2012; 302:E134-E144.
30. Zhang G, Bai H, Zhang H, et al. Neuropeptide exocytosis involving synaptotagmin-4 and oxytocin in hypothalamic programming of body weight and energy balance. Neuron. 2011; 69:523-535.
31. Neumann ID, Maloumby R, Beiderbeck DI, Lukas M, Landgraf R. Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice. Psychoneuroendocrinology. 2013; 38:1985-1993.
32. Maolood N, Meister B. Protein components of the blood-brain barrier (BBB) in the brainstem area postrema-nucleus tractus solitarius region. J Chem Neuroanat. 2009; 37:182-195.
33. Banks WA. Blood-brain barrier and energy balance. Obesity. 2006; 14(SUPPL. 5):234S-237S.
34. Banks WA. The blood-brain barrier as a regulatory interface in the gut-brain axes. Physiol Behav. 2006; 89:472-476.
35. Blevins JE, Schwartz MW, Baskin DG. Evidence that paraventricu-lar nucleus oxytocin neurons link hypothalamic leptin action to caudal brain stem nuclei controlling meal size. Am J Physiol Regul Integr Comp Physiol. 2004; 287:R87-R96.
36. Williams DL, Schwartz MW, Bastian LS, Blevins J.E., Baskin DG. Immunocytochemistry and laser capture microdissection for realtime quantitative PCR identify hindbrain neurons activated by interaction between leptin and cholecystokinin. J Histochem Cy-tochem. 2008; 56:285-293.
37. Paxinos G, Watson C eds. The Rat Brain in Stereotaxic Coordinates. 6th ed. Burlington, MA: Academic Press; 2007.
38. Paxinos G, Franklin KBJ. The Mouse Brain in Sterotaxic Coordinates. 2nd ed. San Diego, CA: Academic Press; 2001.
39. Ring RH, Malberg JE, Potestio L, et al. Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacology. 2006; 185:218-225.
40. Ring RH, Schechter LE, Leonard SK, et al. Receptor and behavioral pharmacology of WAY-267464, a non-peptide oxytocin receptor agonist. Neuropharmacology. 2010; 58:69-77.
41. Morton GJ, Thatcher BS, Reidelberger RD, et al. Peripheral oxy-tocin suppresses food intake and causes weight loss in diet-induced obese rats. Am J Physiol Endocrinol Metab. 2012; 302:E134-E144.
42. Wellman PJ, Davies BT, Morien A, McMahon L. Modulation of feeding by hypothalamic paraventricular nucleus a1- and α2-adrenergic receptors. Life Sci. 1993; 53:669-679.
43. Guo TZ, Tinklenberg J, Oliker R, Maze M. Central α1-adrenocep-tor stimulation functionally antagonizes the hypnotic response to dexmedetomidine, an a2-adrenoceptor agonist. Anesthesiology. 1991; 75:252-256.
44. Davies BT, Wellman PJ. Effects on ingestive behavior in rats of the a1-adrenoceptor agonist cirazoline. Eur J Pharmacol. 1992; 210: 11-16.
45. Rinaman L, Rothe EE. GLP-1 receptor signaling contributes to an-orexigenic effect of centrally administered oxytocin in rats. Am J Physiol Regul Integr Comp Physiol. 2002; 283:R99-R106.
46. Banks WA, During MJ, Niehoff ML. Brain uptake of the glucagon-like peptide-1 antagonist exendin(9-39) after intranasal administration. J Pharmacol Exp Ther. 2004; 309:469-475.
47. Kastin AJ, Akerstrom V. Entry of exendin-4 into brain is rapid but may be limited at high doses. IntJ Obes Relat Metab Disord. 2003; 27:313-318.
48. Williams DL, Baskin DG, Schwartz MW. Evidence that intestinal glucagon-like peptide-1 plays a physiological role in satiety. Endocrinology. 2009; 150:1680-1687.
49. Uvnas-Moberg K, Stock S, Eriksson M, Linden A., Einarsson S, Kunavongkrit A. Plasma levels of oxytocin increase in response to suckling and feeding in dogs and sows. Acta Physiol Scand. 1985; 124: 391-398.
50. Ohlsson B, Forsling ML, Rehfeld JF, Sjolund K. Cholecystokinin stimulation leads to increased oxytocin secretion in women. Eur J Surg. 2002; 168:114-118.
51. Camerino C. Low sympathetic tone and obese phenotype in oxy-tocin-deficient mice. Obesity. 2009; 17:980-984.
52. Takayanagi Y, Kasahara Y, Onaka T, Takahashi N., Kawada T, Nishimori K. Oxytocin receptor-deficient mice developed late-onset obesity. Neuroreport. 2008; 19:951-955.
53. Backman SB, Henry JL. Effects of oxytocin and vasopressin on thoracic sympathetic preganglionic neurones in the cat. Brain Res Bull. 1984; 13:679-684.
54. Armour JA, Klassen GA. Oxytocin modulation of intrathoracic sympathetic ganglionic neurons regulating the canine heart. Peptides. 1990; 11:533-537.
55. Gould BR, Zingg HH. Mapping oxytocin receptor gene expression in the mouse brain and mammary gland using an oxytocin receptor-LacZ reporter mouse. NeuroScience. 2003; 122:155-167.
56. Muchmore DB, Little SA, de Haen C. A dual mechanism of action of ocytocin in rat epididymal fat cells. J Biol Chem. 1981; 256:365-372.
57. Schaffler A, Binart N, Scholmerich J, Buchler C. Hypothesis paper: brain talks with fat-evidence for a hypothalamic-pituitary-adipose axis? Neuropeptides. 2005; 39:363-367.
58. Llewellyn-Smith IJ, Kellett DO, Jordan D, Browning KN, Travagli RA. Oxytocin-immunoreactive innervation of identified neurons in the rat dorsal vagal complex. Neurogastroenterol Motil. 2012; 24: e136-e146.
59. Appleyard SM, Marks D, Kobayashi K, Okano H., Low MJ, Andresen MC. Visceral afferents directly activate catecholamine neurons in the solitary tract nucleus. J Neurosci. 2007; 27:13292-13302.
60. Rinaman L, Verbalis JG, Stricker EM, Hoffman GE. Distribution and neurochemical phenotypes of caudal medullary neurons activated to express cFos following peripheral administration of cholecystokinin. J Comp Neurol. 1993; 338:475-490.
61. Rinaman L, Hoffman GE, Dohanics J, Le WW, Stricker E.M., Verbalis JG. Cholecystokinin activates catecholaminergic neurons in the caudal medulla that innervate the paraventricular nucleus of the hypothalamus in rats. J Comp Neurol. 1995; 360:246-256.
62. Rinaman L. Hindbrain noradrenergic lesions attenuate anorexia and alter central cFos expression in rats after gastric viscerosensory stimulation. J Neurosci. 2003; 23:10084-10092.
63. Sands SA, Morilak DA. Expression of α1D adrenergic receptor messenger RNA in oxytocin-and corticotropin-releasing hormone-synthesizing neurons in the rat paraventricular nucleus. NeuroScience. 1999; 91:639-649.
64. Rinaman L. Interoceptive stress activates glucagon-like peptide-1 neurons that project to the hypothalamus. Am J Physiol. 1999; 277: R582-R590.
65. McMahon LR, Wellman PJ. PVN infusion of GLP-1-(7-36) amide suppresses feeding but does not induce aversion or alter locomotion in rats. Am J Physiol. 1998; 274:R23-R29.
66. Zueco JA, Esquifino AI, Chowen JA, Alvarez E, Castrillon P.O., Blazquez E. Coexpression of glucagon-like peptide-1 (GLP-1) receptor, vasopressin, and oxytocin mRNAs in neurons of the rat hypothalamic supraoptic and paraventricular nuclei: effect of GLP-1(7-36)amide on vasopressin and oxytocin release. J Neurochem. 1999; 72:10-16.
67. Alhadeff AL, Rupprecht LE, Hayes MR. 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. 2012; 153:647-658.
68. Dossat AM, Lilly N, Kay K, Williams DL. Glucagon-like peptide 1 receptors in nucleus accumbens affect food intake. J Neurosci. 2011; 31:14453-14457.
69. Maruyama M, Matsumoto H, Fujiwara K, et al. Prolactin-releasing peptide as a novel stress mediator in the central nervous system. Endocrinology. 2001; 142:2032-2038.
70. Stornetta RL, Sevigny CP, Guyenet PG. Vesicular glutamate transporter DNPI/VGLUT2 mRNA is present in C1 and several other groups of brainstem catecholaminergic neurons. J Comp Neurol. 2002; 444:191-206.
71. Monstein HJ, Grahn N, Truedsson M, Ohlsson B. Oxytocin and oxytocin-receptor mRNA expression in the human gastrointestinal tract: a polymerase chain reaction study. Regul Pept. 2004; 119:39-44.
72. Qin J, Feng M, Wang C, Ye Y., Wang PS, Liu C. Oxytocin receptor expressed on the smooth muscle mediates the excitatory effect of oxytocin on gastric motility in rats. Neurogastroenterol Motil. 2009; 21:430-438.
73. Wu CL, Doong ML, Wang PS. Involvement of cholecystokinin receptor in the inhibition of gastrointestinal motility by oxytocin in ovariectomized rats. Eur J Pharmacol. 2008; 580:407-415.
74. Wu CL, Hung CR, Chang FY, Pau K.Y., Wang PS. Pharmacological effects of oxytocin on gastric emptying and intestinal transit of a non-nutritive liquid meal in female rats. Naunyn Schmiedebergs Arch Pharmacol. 2003, 367:406-413.