Salivary peptide tyrosine-tyrosine 3-36 modulates ingestive behavior without inducing taste aversion

Journal of Neuroscience

Volumn 33, Issue 47, 2013, Pages 18368-18380

  Hurtado, Maria D ^a   Sergeyev, Valeriy G ^c   Acosta, Andres ^a   Spegele, Michael ^a   La Sala, Michael ^a   Waler, Nickolas J ^a   Chiriboga Hurtado, Juan ^a   Currlin, Seth W ^a   Herzog, Herbert ^d   Dotson, Cedrick D ^b   Gorbatyuk, Oleg S ^a   Zolotukhin, Sergei ^a  

^a Neuroscience Institute   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UDMURT STATE UNIVERSITY   (Russian Federation)

^d GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERMEDIN; CORTICOTROPIN RELEASING FACTOR; GLUCAGON LIKE PEPTIDE 1; IODINE 125; MITOGEN ACTIVATED PROTEIN KINASE 7; OXYTOCIN; PEPTIDE YY; TYROSINE 3 MONOOXYGENASE; VASOPRESSIN; WATER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOREXIA; ARTICLE; AUGMENTATION INDEX; BEHAVIOR DISORDER; BRAIN STEM RESPONSE; CATECHOLAMINE NERVE CELL; CONTROLLED STUDY; FOREBRAIN; HABITUATION; HUNGER; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INGESTION; KERATINOCYTE; MALE; MOUSE; MOUTH CAVITY; NAUSEA; NONHUMAN; ONCOGENE C FOS; POST HOC ANALYSIS; PRIORITY JOURNAL; SALIVA ANALYSIS; SATIETY; TASTE AVERSION;

ALPHA-MSH; AMINOPHYLLINE; ANIMALS; CONDITIONING (PSYCHOLOGY); EATING; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GLUCAGON-LIKE PEPTIDE 1; HUMANS; IODINE ISOTOPES; MALE; MICE; MICE, INBRED C57BL; OXYTOCIN; PEPTIDE FRAGMENTS; PEPTIDE YY; PROTO-ONCOGENE PROTEINS C-FOS; SALIVA; SATIATION; TYROSINE 3-MONOOXYGENASE; VASOPRESSINS;

EID: 84887836851     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1064-13.2013     Document Type: Article

References (77)

1. Acosta A, Hurtado MD, Gorbatyuk O, La Sala M, Duncan D, Aslanidi G, Campbell-Thompson M, Zhang L, Herzog H, Voutetakis A, Baum BJ, Zolotukhin S (2011) Salivary PYY: a putative bypass to satiety. PLoS One 6:e26137. CrossRef Medline
2. Aoyagi T, Kusakawa S, Sanbe A, Hiroyama M, Fujiwara Y, Yamauchi J, Tanoue A (2009) Enhanced effect of neuropeptide Y on food intake caused by blockade of the V(1A) vasopressin receptor. Eur J Pharmacol 622:32-36. CrossRef Medline
3. Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL, Wren AM, Brynes AE, Low MJ, Ghatei MA, Cone RD, Bloom SR (2002) Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 418: 650-654. CrossRef Medline
4. Belecky TL, Smith DV (1990) Postnatal development of palatal and laryngeal taste buds in the hamster. J Comp Neurol 293:646-654. CrossRef Medline
5. Belgardt BF, Brüning JC (2010) CNS leptin and insulin action in the control of energy homeostasis. AnnN Y Acad Sci 1212:97-113. CrossRef Medline
6. Bernstein IL, Chavez M, Allen D, Taylor EM (1992) Area postrema mediation of physiological and behavioral effects of lithium chloride in the rat. Brain Res 575:132-137. CrossRef Medline
7. Blevins JE, Baskin DG (2010) Hypothalamic-brainstem circuits controlling eating. Forum Nutr 63:133-140. CrossRef Medline
8. Blevins JE, Chelikani PK, Haver AC, Reidelberger RD (2008) PYY(3-36) induces Fos in the arcuate nucleus and in both catecholaminergic and non-catecholaminergic neurons in the nucleus tractus solitarius of rats. Peptides 29:112-119. CrossRef Medline
9. Blomqvist AG, Herzog H (1997) Y-receptor subtypes-how many more? Trends Neurosci 20:294-298. CrossRef Medline
10. Boey D, Lin S, Karl T, Baldock P, Lee N, Enriquez R, Couzens M, Slack K, Dallmann R, Sainsbury A, HerzogH (2006) Peptide YY ablation in mice leads to the development of hyperinsulinaemia and obesity. Diabetologia 49:1360-1370. CrossRef Medline
11. Chelikani PK, Haver AC, Reidelberger RD (2005) Intravenous infusion of peptide YY(3-36) potently inhibits food intake in rats. Endocrinology 146:879-888. CrossRef Medline
12. Chelikani PK, Haver AC, Reidelberger RD (2006) Dose-dependent effects of peptide YY(3-36) on conditioned taste aversion in rats. Peptides 27: 3193-3201. CrossRef Medline
13. Cho YK, Li CS, Smith DV (2002) Taste responses of neurons of the hamster solitary nucleus are enhanced by lateral hypothalamic stimulation. J Neurophysiol 87:1981-1992. CrossRef Medline
14. Contreras RJ, Beckstead RM, Norgren R (1982) The central projections of the trigeminal, facial, glossopharyngeal and vagus nerves: an autoradiographic study in the rat. J Auton Nerv Syst 6:303-322. CrossRef Medline
15. Corson J, Aldridge A, Wilmoth K, Erisir A (2012) A survey of oral cavity afferents to the rat nucleus tractus solitarii. J Comp Neurol 520:495-527. CrossRef Medline
16. Cunningham ET Jr, Miselis RR, Sawchenko PE (1994) The relationship of efferent projections from the area postrema to vagal motor and brain stem catecholamine-containing cell groups: an axonal transport and immunohistochemical study in the rat. Neuroscience 58:635-648. CrossRef Medline
17. Currie PJ, Coscina DV, Bishop C, Coiro CD, Koob GF, Rivier J, Vale W (2001) Hypothalamic paraventricular nucleus injections of urocortin alter food intake and respiratory quotient. Brain Res 916:222-228. CrossRef Medline
18. Date Y, Shimbara T, Koda S, Toshinai K, Ida T, Murakami N, Miyazato M, Kokame K, Ishizuka Y, Ishida Y, Kageyama H, Shioda S, Kangawa K, Nakazato M (2006) Peripheral ghrelin transmits orexigenic signals through the noradrenergic pathway from the hindbrain to the hypothalamus. Cell Metab 4:323-331. CrossRef Medline
19. Degen L, Oesch S, Casanova M, Graf S, Ketterer S, Drewe J, Beglinger C (2005) Effect of peptide YY3-36 on food intake in humans. Gastroenterology 129:1430-1436. CrossRef Medline
20. Deutsch JA, Hardy WT (1977) Cholecystokinin produces bait shyness in rats. Nature 266:196. CrossRef Medline
21. Di Lorenzo PM, Monroe S (1995) Corticofugal influence on taste responses in the nucleus of the solitary tract in the rat. J Neurophysiol 74:258-272. Medline
22. Di Patrizio NV, Simansky KJ (2008) Activating parabrachial cannabinoid CB1 receptors selectively stimulates feeding of palatable foods in rats. J Neurosci 28:9702-9709. CrossRef Medline
23. Doods H, Gaida W, Wieland HA, Dollinger H, Schnorrenberg G, Esser F, Engel W, Eberlein W, Rudolf K (1999) BIIE0246: a selective and high affinity neuropeptide Y Y(2) receptor antagonist. Eur J Pharmacol 384: R3-R5. CrossRef Medline
24. Fan W, Boston BA, Kesterson RA, Hruby VJ, Cone RD (1997) Role of melanocortinergic neurons in feeding and the agouti obesity syndrome. Nature 385:165-168. CrossRef Medline
25. Fekete EM, Inoue K, Zhao Y, Rivier JE, Vale WW, Szücs A, Koob GF, Zorrilla EP (2007) Delayed satiety-like actions and altered feeding microstructure by a selective type 2 corticotropin-releasing factor agonist in rats: intra-hypothalamic urocortin 3 administration reduces food intake by prolonging the post-meal interval. Neuropsychopharmacology 32:1052-1068. CrossRef Medline
26. Fetissov SO, Byrne LC, Hassani H, Ernfors P, Hökfelt T (2004) Characterization of neuropeptide Y Y2 and Y5 receptor expression in the mouse hypothalamus. J Comp Neurol 470:256-265. CrossRef Medline
27. Fulwiler CE, Saper CB (1984) Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res 319:229-259. Medline
28. Gantz I, Erondu N, Mallick M, Musser B, Krishna R, Tanaka WK, Snyder K, Stevens C, Stroh MA, Zhu H, Wagner JA, Macneil DJ, Heymsfield SB, Amatruda JM (2007) Efficacy and safety of intranasal peptide YY3-36 for weight reduction in obese adults. J Clin Endocrinol Metab 92:1754-1757. CrossRef Medline
29. Glauser DA, Schlegel W (2007) Sequential actions of ERK1/2 on the AP-1 transcription factor allow temporal integration of metabolic signals in pancreatic beta cells. FASEB J 21:3240-3249. CrossRef Medline
30. Gorbatyuk OS, Milner TA, Wang G, Regunathan S, Reis DJ (2001) Localization of agmatine in vasopressin and oxytocin neurons of the rat hypothalamic paraventricular and supraoptic nuclei. Exp Neurol 171:235-245. CrossRef Medline
31. Halatchev IG, Cone RD (2005) Peripheral administration of PYY(3-36) produces conditioned taste aversion in mice. Cell Metab 1:159-168. CrossRef Medline
32. Hamilton RB, Norgren R (1984) Central projections of gustatory nerves in the rat. J Comp Neurol 222:560-577. CrossRef Medline
33. Hashimoto K, Obata K, Ogawa H (2009) Characterization of parabrachial subnuclei in mice with regard to salt tastants: possible independence of taste relay from visceral processing. Chem Senses 34:253-267. CrossRef Medline
34. Hayama T, Ito S, Ogawa H (1985) Responses of solitary tract nucleus neurons to taste and mechanical stimulations of the oral cavity in decerebrate rats. Exp Brain Res 60:235-242. Medline
35. Hermann GE, Kohlerman NJ, Rogers RC (1983) Hepatic-vagal and gustatory afferent interactions in the brainstem of the rat. J Auton Nerv Syst 9:477-495. CrossRef Medline
36. Hurtado MD, Acosta A, Riveros PP, Baum BJ, Ukhanov K, Brown AR, Dotson CD, Herzog H, Zolotukhin S (2012) Distribution of Y-receptors in murine lingual epithelia. PLoS One 7:e46358. CrossRef Medline
37. Jenks BG (2009) Regulation of proopiomelanocortin gene expression: an overview of the signaling cascades, transcription factors, and responsive elements involved. Ann N Y Acad Sci 1163:17-30. CrossRef Medline
38. Johnstone LE, Fong TM, Leng G (2006) Neuronal activation in the hypothalamus and brainstem during feeding in rats. Cell Metab 4:313-321. CrossRef Medline
39. Kalia M, Sullivan JM (1982) Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol 211:248-265. CrossRef Medline
40. Karimnamazi H, Travers JB (1998) Differential projections from gustatory responsive regions of the parabrachial nucleus to the medulla and forebrain. Brain Res 813:283-302. CrossRef Medline
41. Katz DM, Karten HJ (1983) Visceral representation within the nucleus of the tractus solitarius in the pigeon, Columba livia. J Comp Neurol 218:42-73. CrossRef Medline
42. Kinzeler NR, Travers SP (2011) mu-Opioid modulation in the rostral solitary nucleus and reticular formation alters taste reactivity: evidence for a suppressive effect on consummatory behavior. Am J Physiol Regul Integr Comp Physiol 301:R690-R700. CrossRef Medline
43. Koda S, Date Y, Murakami N, Shimbara T, Hanada T, Toshinai K, Niijima A, Furuya M, Inomata N, Osuye K, Nakazato M (2005) The role of the vagal nerve in peripheral PYY3-36-induced feeding reduction in rats. Endocrinology 146:2369-2375. CrossRef Medline
44. Kolterman OG, Buse JB, Fineman MS, Gaines E, Heintz S, Bicsak TA, Taylor K, Kim D, Aisporna M, Wang Y, Baron AD (2003) Synthetic exendin-4 (exenatide) significantly reduces postprandial and fasting plasma glucose in subjects with type 2 diabetes. J Clin Endocrinol Metab 88:3082-3089. CrossRef Medline
45. Kuribara M, Kidane AH, Vos GA, de Gouw D, Roubos EW, Scheenen WJ, Jenks BG (2011) Extracellular-signal regulated kinase regulates production of pro-opiomelanocortin in pituitary melanotroph cells. J Neuroendocrinol 23:261-268. CrossRef Medline
46. Llewellyn-Smith IJ, Reimann F, Gribble FM, Trapp S (2011) Preproglucagon neurons project widely to autonomic control areas in the mouse brain. Neuroscience 180:111-121. CrossRef Medline
47. Lundy RF Jr, Norgren R (2001) Pontine gustatory activity is altered by electrical stimulation in the central nucleus of the amygdala. J Neurophysiol 85:770-783. Medline
48. Moran TH, Smedh U, Kinzig KP, Scott KA, Knipp S, Ladenheim EE (2005) Peptide YY(3-36) inhibits gastric emptying and produces acute reductions in food intake in rhesus monkeys. Am J Physiol Regul Integr Comp Physiol 288:R384-R388. CrossRef Medline
49. Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz MW (2006) Central nervous system control of food intake and body weight. Nature 443:289-295. CrossRef Medline
50. Nishijo H, Ono T, Uwano T, Kondoh T, Torii K (2000) Hypothalamic and amygdalar neuronal responses to various tastant solutions during ingestive behavior in rats. J Nutr 130 [Suppl 4S]:954S-959S.
51. Nonaka N, Shioda S, Niehoff ML, Banks WA (2003) Characterization of blood-brain barrier permeability to PYY3-36 in the mouse. J Pharmacol Exp Ther 306:948-953. CrossRef Medline
52. Olson BR, Drutarosky MD, Stricker EM, Verbalis JG (1991a) Brain oxytocin receptor antagonism blunts the effects of anorexigenic treatments in rats: evidence for central oxytocin inhibition of food intake. Endocrinology 129:785-791. CrossRef Medline
53. Olson BR, Drutarosky MD, Stricker EM, Verbalis JG (1991b) Brain oxytocin receptors mediate corticotropin-releasing hormone-induced anorexia. Am J Physiol 260:R448-R452. Medline
54. Paues J, Mackerlova L, Blomqvist A (2006) Expression of melanocortin-4 receptor by rat parabrachial neurons responsive to immune and aversive stimuli. Neuroscience 141:287-297. CrossRef Medline
55. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. San Diego: Academic.
56. Reilly S, Trifunovic R (2000) Lateral parabrachial nucleus lesions in the rat: aversive and appetitive gustatory conditioning. Brain Res Bull 52:269-278. CrossRef Medline
57. Rinaman L (1999a) Interoceptive stress activates glucagon-like peptide-1 neurons that project to the hypothalamus. Am J Physiol 277:R582-R590. Medline
58. Rinaman L (1999b) A functional role for central glucagon-like peptide-1 receptors in lithium chloride-induced anorexia. AmJ Physiol 277:R1537-R1540. Medline
59. Rinaman L, Dzmura V (2007) Experimental dissociation of neural circuits underlying conditioned avoidance and hypophagic responses to lithium chloride. Am J Physiol Regul Integr Comp Physiol 293:R1495-R1503. CrossRef Medline
60. Saha S, Batten TF, Henderson Z (2000) A GABAergic projection from the central nucleus of the amygdala to the nucleus of the solitary tract: a combined anterograde tracing and electron microscopic immunohistochemical study. Neuroscience 99:613-626. CrossRef Medline
61. Sandoval DA, Bagnol D, Woods SC, D'Alessio DA, Seeley RJ (2008) Arcuate glucagon-like peptide 1 receptors regulate glucose homeostasis but not food intake. Diabetes 57:2046-2054. CrossRef Medline
62. Seeley RJ, Blake K, Rushing PA, Benoit S, Eng J, Woods SC, D'Alessio D (2000) The role of CNS glucagon-like peptide-1 (7-36) amide receptors in mediating the visceral illness effects of lithium chloride. J Neurosci 20:1616-1621. Medline
63. Smith DV, Li CS (2000) GABA-mediated corticofugal inhibition of tasteresponsive neurons in the nucleus of the solitary tract. Brain Res 858:408-415. CrossRef Medline
64. Stanić D, Brumovsky P, Fetissov S, Shuster S, Herzog H, Hökfelt T (2006) Characterization of neuropeptide Y2 receptor protein expression in the mouse brain. I. Distribution in cell bodies and nerve terminals. J Comp Neurol 499:357-390. CrossRef Medline
65. Talsania T, Anini Y, Siu S, Drucker DJ, Brubaker PL (2005) Peripheral exendin-4 and peptide YY(3-36) synergistically reduce food intake through different mechanisms in mice. Endocrinology 146:3748-3756. CrossRef Medline
66. Thiele TE, Van Dijk G, Campfield LA, Smith FJ, Burn P, Woods SC, Bernstein IL, Seeley RJ (1997) Central infusion of GLP-1, but not leptin, produces conditioned taste aversions in rats. Am J Physiol 272:R726-R730. Medline
67. Tokita K, Inoue T, Boughter JD Jr (2010) Subnuclear organization of parabrachial efferents to the thalamus, amygdala and lateral hypothalamus in C57BL/6J mice: a quantitative retrograde double labeling study. Neuroscience 171:351-365. CrossRef Medline
68. Travers SP, Nicklas K (1990) Taste bud distribution in the rat pharynx and larynx. Anat Rec 227:373-379. CrossRef Medline
69. Travers SP, Norgren R (1995) Organization of orosensory responses in the nucleus of the solitary tract of rat. J Neurophysiol 73:2144-2162. Medline
70. Trifunovic R, Reilly S (2002) Medial versus lateral parabrachial nucleus lesions in the rat: effects on mercaptoacetate-induced feeding and conditioned taste aversion. Brain Res Bull 58:107-113. CrossRef Medline
71. van der Kooy D, Koda LY, McGinty JF, Gerfen CR, Bloom FE (1984) The organization of projections from the cortex, amygdala, and hypothalamus to the nucleus of the solitary tract in rat. J Comp Neurol 224:1-24. CrossRef Medline
72. Verbalis JG, Blackburn RE, Olson BR, Stricker EM (1993) Central oxytocin inhibition of food and salt ingestion: a mechanism for intake regulation of solute homeostasis. Regul Pept 45:149-154. CrossRef Medline
73. 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. Medline
74. Vrang N, Hansen M, Larsen PJ, Tang-Christensen M (2007) Characterization of brainstem preproglucagon projections to the paraventricular and dorsomedial hypothalamic nuclei. Brain Res 1149:118-126. CrossRef Medline
75. Vrang N, Larsen PJ, Jensen PB, Lykkegaard K, Artmann A, Larsen LK, Tang-Christensen M (2008) Upregulation of the brainstem preproglucagon system in the obese Zucker rat. Brain Res 1187:116-124. CrossRef Medline
76. Xu Z, Wang BR, Ding YQ, Kuang F, Wang X, Duan XL, Jiao XY, Ju G (2002) Extracellular signal-regulated kinases1/2 in neurons of the dorsal motor nucleus of the vagus nerve and nucleus of the solitary tract are activated by noxious visceral stimulus in mice. Neurosci Lett 334:103-106. CrossRef Medline
77. Yamamoto T (2008) Central mechanisms of roles of taste in reward and eating. Acta Physiol Hung 95:165-186. CrossRef Medline