The subfornical organ: A central target for circulating feeding signals

Journal of Neuroscience

Volumn 26, Issue 7, 2006, Pages 2022-2030

  Pulman, Katherine J ^a   Fry, W Mark ^a   Cottrell, G Trevor ^a   Ferguson, Alastair V ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Amylin; Circumventricular organ; Electrophysiology; Feeding; Ghrelin; Subfornical organ

Indexed keywords

AMYLIN; CALCIUM; CATION; GHRELIN; GROWTH HORMONE SECRETAGOGUE RECEPTOR; MESSENGER RNA;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN VENTRICLE; CALCIUM CELL LEVEL; CELL MEMBRANE DEPOLARIZATION; CELL SUBPOPULATION; CONTROLLED STUDY; DISSOCIATION; ELECTRIC CURRENT; ELECTRIC POTENTIAL; EXAMINATION; FEEDBACK SYSTEM; FOOD INTAKE; FREQUENCY MODULATION; HYPOTHALAMUS; ION CONDUCTANCE; MALE; NERVE CELL EXCITABILITY; NONHUMAN; OBSERVATION; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECORDING; SATIETY; SIGNAL TRANSDUCTION; SUBFORNICAL ORGAN; VOLTAGE CLAMP; WHOLE CELL;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM SIGNALING; FEEDING BEHAVIOR; HIPPOCAMPUS; MALE; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEASES; SUBFORNICAL ORGAN;

EID: 33644553529     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3218-05.2006     Document Type: Article

References (63)

1. Anderson JW, Smith PM, Ferguson AV (2001) Subfornical organ neurons projecting to paraventricular nucleus: whole-cell properties. Brain Res 921:78-85.
2. Bagnasco M, Kalra PS, Kalra SP (2002) Ghrelin and leptin pulse discharge in fed and fasted rats. Endocrinology 143:726-729.
3. Baldo BA, Kelley AE (2001) Amylin infusion into rat nucleus accumbens potently depresses motor activity and ingestive behaviour. Am J Physiol Regul Integr Comp Physiol 281:R1232-R1242.
4. Banks WA, Kastin AJ (1992) Bidirectional passage of peptides across the blood-brain barrier. Prog Brain Res 91:139-148.
5. Banks WA, Kastin AJ (1998) Differential permeability of the blood-brain barrier to two pancreatic peptides: insulin and amylin. Peptides 19:883-889.
6. Banks WA, Tschop M, Robinson SM, Heiman ML (2002) Extent and direction of ghrelin transport across the blood-brain barrier is determined by its unique primary structure. J Pharmacol Exp Ther 302:822-827.
7. Barreiro ML, Suominen JS, Gaytan F, Pinilla L, Chopin LK, Casanueva FF, Dieguez C, Aguilar E, Toppari J, Tena-Sempere M (2003) Developmental, stage-specific, and hormonally regulated expression of growth hormone secretagogue receptor messenger RNA in rat testis. Biol Reprod 68:1631-1640.
8. Butler PC, Chou J, Carter WB, Wang YN, Bu BH, Chang D, Chang JK, Rizza RA (1990) Effects of meal ingestion on plasma amylin concentration in NIDDM and nondiabetic humans. Diabetes 39:752-756.
9. Caminos JE, Tena-Sempere M, Gaytan F, Sanchez-Criado JE, Barreiro ML, Nogueiras R, Casanueva FF, Aguilar E, Dieguez C (2003) Expression of ghrelin in the cyclic and pregnant rat ovary. Endocrinology 144:1594-1602.
10. Cheng K, Chan WW, Barreto Jr A, Convey EM, Smith RG (1989) The synergistic effects of His-D-Trp-Ala-Trp-D-Phe-Lys-NH2 on growth hormone (GH)-releasing factor-stimulated GH release and intracellular adenosine 3′,5′-monophosphate accumulation in rat primary pituitary cell culture. Endocrinology 124:2791-2798.
11. Cottrell GT, Ferguson AV (2004) Sensory circumventricular organs: central roles in integrated autonomic regulation. Regul Pept 117:11-23.
12. Cottrell GT, Zhou QY, Ferguson AV (2004) Prokineticin 2 modulates the excitability of subfornical organ neurons. J Neurosci 24:2375-2379.
13. Cowley MA, Smith RG, Diano S, Tschop M, Pronchuk N, Grove KL, Strasburger CJ, Bidlingmaier M, Esterman M, Heiman ML, Garcia-Segura LM, Nillni EA, Mendez P, Low MJ, Sotonyi P, Friedman JM, Liu H, Pinto S, Colmers WF, Cone RD, et al. (2003) The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron 37:649-661.
14. Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, Weigle DS (2001) A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 50:1714-1719.
15. Date Y, Kojima M, Hosoda H, Sawaguchi A, Mondal MS, Suganuma T, Matsukura S, Kangawa K, Nakazato M (2000) Ghrelin, a novel growth hormone-releasing acylated peptide, is synthesized in a distinct endocrine cell type in the gastrointestinal tracts of rats and humans. Endocrinology 141:4255-4261.
16. 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.
17. Desson SE, Ferguson AV (2003) Interleukin 1beta modulates rat subfornical organ neurons as a result of activation of a non-selective cationic conductance. J Physiol (Lond) 550:113-122.
18. Ferguson AV, Bains JS (1997) Actions of angiotensin in the subfornical organ and area postrema: implications for long term control of autonomic output. Clin Exp Pharmacol Physiol 24:96-101.
19. Ferguson AV, Bicknell RJ, Carew MA, Mason WT (1997) Dissociated adult rat subfornical organ neurons maintain membrane properties and angiotensin responsiveness for up to 6 days. Neuroendocrinology 66:409-415.
20. Fitzsimons JT (1979) The physiology of thirst and sodium appetite. Cambridge, UK: Cambridge UP.
21. Gruber K, McRae-Degueurce A, Wilkin LD, Mitchell LD, Johnson AK (1987) Forebrain and brainstem afferents to the arcuate nucleus in the rat: potential pathways for the modulation of hypophyseal secretions. Neurosci Lett 75:1-5.
22. Kamegai J, Tamura H, Shimizu T, Ishii S, Sugihara H, Wakabayashi I (2001) Chronic central infusion of ghrelin increases hypothalamic neuropeptide Y and Agouti-related protein mRNA levels and body weight in rats. Diabetes 50:2438-2443.
23. 2+ signaling via protein kinase A and N-type channel-dependent mechanisms and cross-talk with leptin and orexin. Diabetes 52:948-956.
24. 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.
25. Korbonits M, Bustin SA, Kojima M, Jordan S, Adams EF, Lowe DG, Kangawa K, Grossman AB (2001) The expression of the growth hormone secretagogue receptor ligand ghrelin in normal and abnormal human pituitary and other neuroendocrine tumors. J Clin Endocrinol Metab 86:881-887.
26. Kozaka T, Fujii Y, Ando M (2003) Central effects of various ligands on drinking behavior in eels acclimated to seawater. J Exp Biol 206:687-692.
27. 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.
28. Lind RW, Van Hoesen GW, Johnson AK (1982) An HRP study of the connections of the subfornical organ of the rat. J Comp Neurol 210:265-277.
29. Lu S, Guan JL, Wang QP, Uehara K, Yamada S, Goto N, Date Y, Nakazato M, Kojima M, Kangawa K, Shioda S (2002) Immunocytochemical observation of ghrelin-containing neurons in the rat arcuate nucleus. Neurosci Lett 321:157-160.
30. Lutz TA, Del Prete E, Scharrer E (1994) Reduction of food intake in rats by intraperitoneal injection of low doses of amylin. Physiol Behav 55:891-895.
31. Lutz TA, Geary N, Szabady MM, Del Prete E, Scharrer E (1995) Amylin decreases meal size in rats. Physiol Behav 58:1197-1202.
32. Lutz TA, Mollet A, Rushing PA, Riediger T, Scharrer E (2001) The anorectic effect of a chronic peripheral infusion of amylin is abolished in area postrema/nucleus of the solitary tract (AP/NTS) lesioned rats. Int J Obes Relat Metab Disord 25:1005-1011.
33. McKee KK, Palyha OC, Feighner SD, Hreniuk DL, Tan CP, Phillips MS, Smith RG, Van der Ploeg LH, Howard AD (1997) Molecular analysis of rat pituitary and hypothalamic growth hormone secretagogue receptors. Mol Endocrinol 11:415-423.
34. McKinley MJ, Allen AM, Burns P, Colvill LM, Oldfield BJ (1998) Interaction of circulating hormones with the brain: the roles of the subfornical organ and the organum vasculosum of the lamina terminalis. Clin Exp Pharmacol Physiol [Suppl] 25:S61-S67.
35. Miselis RR (1981) The efferent projections of the subfornical organ of the rat: a circumventricular organ within a neural network subserving water balance. Brain Res 230:1-23.
36. Miselis RR (1982) The subfornical organ's neural connections and their role in water balance. Peptides 3:501-502.
37. Mori K, Yoshimoto A, Takaya K, Hosoda K, Ariyasu H, Yahata K, Mukoyama M, Sugawara A, Hosoda H, Kojima M, Kangawa K, Nakao K (2000) Kidney produces a novel acylated peptide, ghrelin. FEBS Lett 486:213-216.
38. Morley JE, Flood JF (1991) Amylin decreases food intake in mice. Peptides 12:865-869.
39. Morley JE, Flood JF, Horowitz M, Morley PM, Walter MJ (1994) Modulation of food intake by peripherally administered amylin. Am J Physiol 267:R178-R184.
40. Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, Matsukura S (2001) A role for ghrelin in the central regulation of feeding. Nature 409:194-198.
41. Oliet SHR, Bourque CW (1993) Steady-state osmotic modulation of cationic conductance in neurons of rat supraoptic nucleus. Am J Physiol 265:R1475-R1479.
42. Perez-Velazquez JL, Zhang L (1994) In vitro hypoxia induces expression of the NR2C subunit of the NMDA receptor in rat cortex and hippocampus. J Neurochem 63:1171-1173.
43. Pieber TR, Roitelman J, Lee Y, Luskey KL, Stein DT (1994) Direct plasma radioimmunoassay for rat amylin-(1-37): concentrations with acquired and genetic obesity. Am J Physiol 267:E156-E164.
44. Riediger T, Rauch M, Schmid HA (1999) Actions of amylin on subfornical organ neurons and on drinking behavior in rats. Am J Physiol 276:R514-R521.
45. Riediger T, Schmid HA, Lutz T, Simon E (2001) Amylin potently activates AP neurons possibly via formation of the excitatory second messenger cGMP. Am J Physiol Regul Integr Comp Physiol 281:R1833-R1843.
46. Rushing PA, Hagan MM, Seeley RJ, Lutz TA, Woods SC (2000) Amylin: a novel action in the brain to reduce body weight. Endocrinology 141:850-853.
47. Rushing PA, Hagan MM, Seeley RJ, Lutz TA, D'Alessio DA, Air EL, Woods SC (2001) Inhibition of central amylin signaling increases food intake and body adiposity in rats. Endocrinology 142:5035.
48. Seoane LM, Tovar S, Baldelli R, Arvat E, Ghigo E, Casanueva FF, Dieguez C (2000) Ghrelin elicits a marked stimulatory effect on GH secretion in freely-moving rats. Eur J Endocrinol 143:R7-R9.
49. Sexton PM, Paxinos G, Kenney MA, Wookey PJ, Beaumont K (1994) In vitro autoradiographic localization of amylin binding sites in rat brain. Neuroscience 62:553-567.
50. Silverman AJ, Hoffman DL, Zimmerman EA (1981) The descending afferent connections of the paraventricular nucleus of the hypothalamus (PVN). Brain Res Bull 6:47-61.
51. Simpson JB, Routtenberg JB (1975) Subfornical organ lesions reduce intravenous angiotensin-induced drinking. Brain Res 88:154-161.
52. Simpson JB, Epstein AN, Camardo JS (1978) Localization of receptors for dipsogenic action of angiotensin II in subfornical organ of rat. J Comp Physiol Psychol 92:581-608.
53. Smith RG, Cheng K, Schoen WR, Pong SS, Hickey G, Jacks T, Butler B, Chan WW, Chaung LY, Judith F (1993) A nonpeptidyl growth hormone secretagogue. Science 260:1640-1643.
54. Tschop M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodents. Nature 407:908-913.
55. Tschop M, Wawarta R, Riepl RL, Friedrich S, Bidlingmaier M, Landgraf R, Folwaczny C (2001) Post-prandial decrease of circulating human ghrelin levels. J Endocrinol Invest 24:RC19-RC21.
56. Volante M, Allia E, Gugliotta P, Funaro A, Broglio F, Deghenghi R, Muccioli G, Ghigo E, Papotti M (2002) Expression of ghrelin and of the GH secretagogue receptor by pancreatic islet cells and related endocrine tumors. J Clin Endocrinol Metab 87:1300-1308.
57. Washburn DLS, Beedle AM, Ferguson AV (1999) Inhibition of subfornical organ neuronal potassium channels by vasopressin. Neuroscience 93:349-359.
58. Washburn DLS, Anderson JW, Ferguson AV (2000) A subthreshold persistent sodium current mediates bursting in rat subfornical organ neurones. J Physiol (Lond) 529:359-371.
59. Williams DL, Grill HJ, Cummings DE, Kaplan JM (2003) Vagotomy dissociates short- and long-term controls of circulating ghrelin. Endocrinology 144:5184-5187.
60. Wren AM, Small CJ, Ward HL, Murphy KG, Dakin CL, Taheri S, Kennedy AR, Roberts GH, Morgan DG, Ghatei MA, Bloom SR (2000) The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology 141:4325-4328.
61. Wren AM, Small CJ, Abbott CR, Dhillo WS, Seal LJ, Cohen MA, Batterham RL, Taheri S, Stanley SA, Ghatei MA, Bloom SR (2001) Ghrelin causes hyperphagia and obesity in rats. Diabetes 50:2540-2547.
62. Yang B, Ferguson AV (2002) Orexin-A depolarizes dissociated rat area postrema neurons through activation of a nonselective cationic conductance. J Neurosci 22:6303-6308.
63. Yang B, Goulet M, Boismenu R, Ferguson AV (2004) Secretin depolarizes nucleus tractus solitarius neurons through activation of a nonselective cationic conductance. Am J Physiol Regul Integr Comp Physiol 286:R927-R934.