Ghrelin inhibits visceral afferent activation of catecholamine neurons in the solitary tract nucleus

Journal of Neuroscience

Volumn 31, Issue 9, 2011, Pages 3484-3492

  Cui, Ran Ji ^a   Li, Xiaojun ^a   Appleyard, Suzanne M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; CATECHOLAMINE; CHOLECYSTOKININ; ENHANCED GREEN FLUORESCENT PROTEIN; GHRELIN; GLUTAMIC ACID; HISTIDYL DEXTRO TRYPTOPHYLALANYLTRYPTOPHYL DEXTRO PHENYLALANYLLYSINAMIDE; RECEPTOR BLOCKING AGENT; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CATECHOLAMINE NERVE CELL; CELL ACTIVATION; CONTROLLED STUDY; EVOKED RESPONSE; FEMALE; MALE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SENSORY NERVE; SOLITARY TRACT NUCLEUS; TRANSGENIC MOUSE;

ANIMALS; CATECHOLAMINES; EXCITATORY POSTSYNAPTIC POTENTIALS; FASTING; FEMALE; GHRELIN; MALE; MICE; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONS; SOLITARY NUCLEUS; VISCERAL AFFERENTS;

EID: 79952267286     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3187-10.2011     Document Type: Article

References (75)

1. Abizaid A (2009) Ghrelin and dopamine: new insights on the peripheral regulation of appetite. J Neuroendocrinol 21:787-793.
2. Andresen MC, Yang MY (1990) Non-NMDA receptors mediate sensory afferent synaptic transmission in medial nucleus tractus solitarius. Am J Physiol 259:H1307-H1311. (Pubitemid 20352336)
3. Appleyard SM, Bailey TW, Doyle MW, Jin YH, Smart JL, Low MJ, Andresen MC (2005) Proopiomelanocortin neurons in nucleus tractus solitarius are activated by visceral afferents: regulation by cholecystokinin and opioids. J Neurosci 25:3578-3585.
4. Appleyard SM, Marks D, Kobayashi K, Okano H, Low MJ, Andresen MC (2007) Visceral afferents directly activate catecholamine neurons in the solitary tract nucleus. J Neurosci 27:13292-13302. (Pubitemid 350220485)
5. Arnold M, Mura A, Langhans W, Geary N (2006) Gut vagal afferents are not necessary for the eating-stimulatory effect of intraperitoneally injected ghrelin in the rat. J Neurosci 26:11052-11060. (Pubitemid 44772195)
6. Bailey TW, Jin YH, Doyle MW, Smith SM, Andresen MC (2006) Vasopressin inhibits glutamate release via two distinct modes in the brainstem. J Neurosci 26:6131-6142.
7. Bailey TW, Hermes SM, Whittier KL, Aicher SA, Andresen MC (2007) A-type potassium channels differentially tune afferent pathways from rat solitary tract nucleus to caudal ventrolateral medulla or paraventricular hypothalamus. J Physiol 582:613-628. (Pubitemid 47040548)
8. Balcita-Pedicino JJ, Rinaman L (2007) Noradrenergic axon terminals contact gastric preautonomic neurons in the paraventricular nucleus of the hypothalamus in rats. J Comp Neurol 501:608-618. (Pubitemid 46622498)
9. Baptista V, Zheng ZL, Coleman FH, Rogers RC, Travagli RA (2005) Chole-cystokinin octapeptide increases spontaneous glutamatergic synaptic transmission to neurons of the nucleus tractus solitarius centralis. J Neurophysiol 94:2763-2771. (Pubitemid 41324694)
10. Berthoud HR (2008) Vagal and hormonal gut-brain communication: from satiation to satisfaction. Neurogastroenterol Motil 20 [Suppl 1]:64-72.
11. 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. (Pubitemid 50015273)
12. Browning KN, Travagli RA (2010) Plasticity of vagal brainstem circuits in the control of gastric function. Neurogastroenterol Motil 22:1154-1163.
13. Buller KM, Day TA (1996) Involvement of medullary catecholamine cells in neuroendocrine responses to systemic cholecystokinin. J Neuroendocrinol 8:819-824. (Pubitemid 26362794)
14. Burdyga G, Varro A, Dimaline R, Thompson DG, Dockray GJ (2006) Ghrelin receptors in rat and human nodose ganglia: putative role in regulating CB-1 and MCH receptor abundance. Am J Physiol Gastrointest Liver Physiol 290:G1289-G1297. (Pubitemid 43788312)
15. Castañeda TR, Tong J, Datta R, Culler M, Tschöp MH (2010) Ghrelin in the regulation of body weight and metabolism. Front Neuroendocrinol 31:44-60.
16. Chan RK, Sawchenko PE (1998) Organization and transmitter specificity of medullary neurons activated by sustained hypertension: implications for understanding baroreceptor reflex circuitry. J Neurosci 18:371-387. (Pubitemid 28046795)
17. Chen CY, Horowitz JM, Bonham AC (1999) A presynaptic mechanism contributes to depression of autonomic signal transmission in NTS. Am J Physiol 277:H1350-H1360. (Pubitemid 29522663)
18. Cowley MA, Smart JL, Rubinstein M, Cerdán MG, Diano S, Horvath TL, Cone RD, Low MJ (2001) Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411:480-484. (Pubitemid 32494394)
19. Cummings DE (2006) Ghrelin and the short- and long-term regulation of appetite and body weight. Physiol Behav 89:71-84.
20. Cunningham ET Jr, Sawchenko PE (1988) Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus. J Comp Neurol 274:60-76.
21. Date Y, Murakami N, Toshinai K, Matsukura S, Niijima A, Matsuo H, Kangawa K, Nakazato M (2002) The role of the gastric afferent vagal nerve in ghrelin-induced feeding and growth hormone secretion in rats. Gastroenterology 123:1120-1128.
22. Date Y, Toshinai K, Koda S, Miyazato M, Shimbara T, Tsuruta T, Niijima A, Kangawa K, Nakazato M (2005) Peripheral interaction of ghrelin with cholecystokinin on feeding regulation. Endocrinology 146:3518-3525. (Pubitemid 41058123)
23. 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. (Pubitemid 44430917)
24. Depoortere I, Thijs T, Peeters T (2006) The contractile effect of the ghrelin receptor antagonist, D-Lys3-GHRP-6, in rat fundic strips is mediated through 5-HT receptors. Eur J Pharmacol 537:160-165.
25. Dockray GJ (2009) The versatility of the vagus. Physiol Behav 97:531-536.
26. Doyle MW, Andresen MC (2001) Reliability of monosynaptic sensory transmission in brain stem neurons in vitro. J Neurophysiol 85:2213-2223. (Pubitemid 32440698)
27. Emanuel AJ, Ritter S (2010) Hindbrain catecholamine neurons modulate the growth hormone but not the feeding response to ghrelin. Endocrinology 151:3237-3246.
28. Erriquez J, Bernascone S, Ciarletta M, Filigheddu N, Graziani A, Distasi C (2009) Calcium signals activated by ghrelin and D-Lys(3)-GHRP-6 ghrelin antagonist in developing dorsal root ganglion glial cells. Cell Calcium 46:197-208.
29. Faulconbridge LF, Cummings DE, Kaplan JM, Grill HJ (2003) Hyperphagic effects of brainstem ghrelin administration. Diabetes 52:2260-2265. (Pubitemid 37059495)
30. Faulconbridge LF, Grill HJ, Kaplan JM, Daniels D (2008) Caudal brainstem delivery of ghrelin induces fos expression in the nucleus of the solitary tract, but not in the arcuate or paraventricular nuclei of the hypothalamus. Brain Res 1218:151-157.
31. Fry M, Ferguson AV (2010) Ghrelin: central nervous system sites of action in regulation of energy balance. Int J Pept pii:616757.
32. Grill HJ, Hayes MR (2009) The nucleus tractus solitarius: a portal for visceral afferent signal processing, energy status assessment and integration of their combined effects on food intake. Int J Obes (Lond) 33 [Suppl 1]:S11-S15.
33. Hollis JH, Lightman SL, Lowry CA (2004) Integration of systemic and visceral sensory information by medullary catecholaminergic systems during peripheral inflammation. Ann N Y Acad Sci 1018:71-75. (Pubitemid 38951392)
34. Jin YH, Bailey TW, Doyle MW, Li BY, Chang KS, Schild JH, Mendelowitz D, Andresen MC (2003) Ketamine differentially blocks sensory afferent synaptic transmission in medial nucleus tractus solitarius (mNTS). Anesthesiology 98:121-132. (Pubitemid 36043418)
35. Kline DD (2008) Plasticity in glutamatergic NTS neurotransmission. Respir Physiol Neurobiol 164:105-111.
36. Kline DD, Hendricks G, Hermann G, Rogers RC, Kunze DL (2009) Dopamine inhibits N-type channels in visceral afferents to reduce synaptic transmitter release under normoxic and chronic intermittent hypoxic conditions. J Neurophysiol 101:2270-2278.
37. Kobashi M, Yanagihara M, Fujita M, Mitoh Y, Matsuo R (2009) Fourth ventricular administration of ghrelin induces relaxation of the proximal stomach in the rat. Am J Physiol Regul Integr Comp Physiol 296:R217-R223.
38. Kojima M, Kangawa K (2010) Ghrelin: more than endogenous growth hormone secretagogue. Ann N Y Acad Sci 1200:140-148.
39. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402:656-660. (Pubitemid 129516334)
40. Krout KE, Mettenleiter TC, Karpitskiy V, Nguyen XV, Loewy AD (2005) CNS neurons with links to both mood-related cortex and sympathetic nervous system. Brain Res 1050:199-202. (Pubitemid 40922734)
41. Lacroix S, Rivest S (1997) Functional circuitry in the brain of immune-challenged rats: partial involvement of prostaglandins. J Comp Neurol 387:307-324. (Pubitemid 27430353)
42. Lam DD, Zhou L, Vegge A, Xiu PY, Christensen BT, Osundiji MA, Yueh CY, Evans ML, Heisler LK (2009) Distribution and neurochemical characterization of neurons within the nucleus of the solitary tract responsive to serotonin agonist-induced hypophagia. Behav Brain Res 196:139-143.
43. Laorden ML, Castells MT, Milanés MV (2002) Effects of morphine and morphine withdrawal on brainstem neurons innervating hypothalamic nuclei that control the pituitary-adrenocortical axis in rats. Br J Pharmacol 136:67-75. (Pubitemid 34499317)
44. Lee MC, Yasuda R, Ehlers MD (2010) Metaplasticity at single glutamatergic synapses. Neuron 66:859-870.
45. le Roux CW, Neary NM, Halsey TJ, Small CJ, Martinez-Isla AM, Ghatei MA, Theodorou NA, Bloom SR (2005) Ghrelin does not stimulate food intake in patients with surgical procedures involving vagotomy. J Clin Endocrinol Metab 90:4521-4524. (Pubitemid 41159336)
46. Lin Y, Matsumura K, Fukuhara M, Kagiyama S, Fujii K, Iida M (2004) Ghrelin acts at the nucleus of the solitary tract to decrease arterial pressure in rats. Hypertension 43:977-982. (Pubitemid 38579901)
47. Madden CJ, Sved AF (2003) Cardiovascular regulation after destruction of the C1 cell group of the rostral ventrolateral medulla in rats. Am J Physiol Heart Circ Physiol 285:H2734-H2748. (Pubitemid 37443095)
48. Mönnikes H, Lauer G, Arnold R (1997) Peripheral administration of chole-cystokinin 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 770:277-288. (Pubitemid 27468078)
49. Moran TH, Ladenheim EE, Schwartz GJ (2001) Within-meal gut feedback signaling. Int J Obes Relat Metab Disord 25 [Suppl 5]:S39-S41. (Pubitemid 34146321)
50. Onaka T (2000) Catecholaminergic mechanisms underlying neurohypophysial hormone responses to unconditioned or conditioned aversive stimuli in rats. Exp Physiol 85 Spec No:101S-110S.
51. Page AJ, Slattery JA, Milte C, Laker R, O'Donnell T, Dorian C, Brierley SM, Blackshaw LA (2007) Ghrelin selectively reduces mechanosensitivity of upper gastrointestinal vagal afferents. Am J Physiol Gastrointest Liver Physiol 292:G1376-G1384. (Pubitemid 47084656)
52. Peters JH, McDougall SJ, Kellett DO, Jordan D, Llewellyn-Smith IJ, Andresen MC (2008) Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus. J Neurosci 28:11731-11740.
53. Reyes BA, Van Bockstaele EJ (2006) Divergent projections of catecholamin-ergic neurons in the nucleus of the solitary tract to limbic forebrain and medullary autonomic brain regions. Brain Res 1117:69-79. (Pubitemid 44573104)
54. Rinaman L (2003) Hindbrain noradrenergic lesions attenuate anorexia and alter central cFos expression in rats after gastric viscerosensory stimulation. J Neurosci 23:10084-10092.
55. 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. (Pubitemid 47535767)
56. Rinaman L, Hoffman GE, Dohanics J, Le WW, Stricker EM, Verbalis JG (1995) Cholecystokinin activates catecholaminergic neurons in the caudal medulla that innervate the paraventricular nucleus of the hypothalamus in rats. J Comp Neurol 360:246-256.
57. Rinaman L, Baker EA, Hoffman GE, Stricker EM, Verbalis JG (1998) Medullary c-Fos activation in rats after ingestion of a satiating meal. Am J Physiol 275:R262-R268.
58. Ritter S, Bugarith K, Dinh TT (2001) Immunotoxic destruction of distinct catecholamine subgroups produces selective impairment of glucoregulatory responses and neuronal activation. J Comp Neurol 432:197-216. (Pubitemid 32187012)
59. Rogers RC, Travagli RA, Hermann GE (2003) Noradrenergic neurons in the rat solitary nucleus participate in the esophageal-gastric relaxation reflex. Am J Physiol Regul Integr Comp Physiol 285:R479-R489. (Pubitemid 36898917)
60. Routh VH (2002) Glucose-sensing neurons: are they physiologically relevant? Physiol Behav 76:403-413.
61. Sato M, Nakahara K, Miyazato M, Kangawa K, Murakami N (2007) Regulation of GH secretagogue receptor gene expression in the rat nodose ganglion. J Endocrinol 194:41-46. (Pubitemid 47162885)
62. Sawchenko PE, Pfeiffer SW (1988) Ultrastructural localization of neuropeptide Y and galanin immunoreactivity in the paraventricular nucleus of the hypothalamus in the rat. Brain Res 474:231-245.
63. Sawchenko PE, Swanson LW (1981) Central noradrenergic pathways for the integration of hypothalamic neuroendocrine and autonomic responses. Science 214:685-687. (Pubitemid 12208596)
64. Schiöth HB, Muceniece R, Wikberg JE (1997) Characterization of the binding of MSH-B, HB-228, GHRP-6 and 153N-6 to the human melanocortin receptor subtypes. Neuropeptides 31:565-571. (Pubitemid 28037472)
65. Scott V, McDade DM, Luckman SM (2007) Rapid changes in the sensitivity of arcuate nucleus neurons to central ghrelin in relation to feeding status. Physiol Behav 90:180-185. (Pubitemid 44918018)
66. Silver RA (2010) Neuronal arithmetic. Nat Rev Neurosci 11:474-489.
67. Sutton MA, Ito HT, Cressy P, Kempf C, Woo JC, Schuman EM (2006) Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 125:785-799.
68. Tung YC, Hewson AK, Carter RN, Dickson SL (2005) Central responsiveness to a ghrelin mimetic (GHRP-6) is rapidly altered by acute changes in nutritional status in rats. J Neuroendocrinol 17:387-393. (Pubitemid 40796994)
69. Ueta Y, Kannan H, Higuchi T, Negoro H, Yamaguchi K, Yamashita H (2000) Activation of gastric afferents increases noradrenaline release in the paraventricular nucleus and plasma oxytocin level. J Auton Nerv Syst 78:69-76. (Pubitemid 30052941)
70. Van Bockstaele EJ, Menko AS, Drolet G (2001) Neuroadaptive responses in brainstem noradrenergic nuclei following chronic morphine exposure. Mol Neurobiol 23:155-171. (Pubitemid 33030097)
71. Wang ZJ, Rao ZR, Shi JW (1992) Tyrosine hydroxylase-, neurotensin-, or cholecystokinin-containing neurons in the nucleus tractus solitarii send projection fibers to the nucleus accumbens in the rat. Brain Res 578:347-350.
72. Williams DL, Schwartz MW, Bastian LS, Blevins JE, Baskin DG (2008) Immunocytochemistry and laser capture microdissection for real-time quantitative PCR identify hindbrain neurons activated by interaction between leptin and cholecystokinin. J Histochem Cytochem 56:285-293. (Pubitemid 351273000)
73. Willing AE, Berthoud HR (1997) Gastric distension-induced c-fos expression in catecholaminergic neurons of rat dorsal vagal complex. Am J Physiol 272:R59-R67.
74. Zigman JM, Elmquist JK (2003) Minireview: from anorexia to obesity - the yin and yang of body weight control. Endocrinology 144:3749-3756. (Pubitemid 37098305)
75. Zigman JM, Jones JE, Lee CE, Saper CB, Elmquist JK (2006) Expression of ghrelin receptor mRNA in the rat and the mouse brain. J Comp Neurol 494:528-548. (Pubitemid 41791000)