Responses to cholecystokinin in the ventromedial nucleus of the rat hypothalamus in vivo

European Journal of Neuroscience

Volumn 31, Issue 6, 2010, Pages 1127-1135

  Sabatier, Nancy ^a   Leng, Gareth ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Appetite; CCK; Electrophysiology; Leptin

Indexed keywords

CHOLECYSTOKININ; LEPTIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FOOD INTAKE; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; IN VIVO STUDY; MALE; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SATIETY; SIGNAL TRANSDUCTION;

ACTION POTENTIALS; ANIMALS; CHOLAGOGUES AND CHOLERETICS; CHOLECYSTOKININ; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION ROUTES; LEPTIN; MALE; NEURAL INHIBITION; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; VENTROMEDIAL HYPOTHALAMIC NUCLEUS;

EID: 77949554007     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07144.x     Document Type: Article

References (68)

1. Barrachina, M.D., Martinez, V., Wang, L., Wei, J.Y. Tache, Y. (1997) Synergistic interaction between leptin and cholecystokinin to reduce short-term food intake in lean mice. Proc. Natl Acad. Sci. USA, 94, 10455 10460.
2. Bechtold, D.A. Luckman, S.M. (2006) Prolactin-releasing peptide mediates cholecystokinin-induced satiety in mice. Endocrinology, 147, 4723 4729.
3. Blevins, J.E., Stanley, G.B. Reiderbelger, R.D. (2000) Brain regions where cholecystokinin suppresses feeding in rats. Brain Res., 860, 1 10.
4. Blevins, J.E., Morton, G.J., Williams, D.L., Caldwell, D.W., Bastian, L.S., Wisse, B.E., Schwartz, M.W. Baskin, D.G. (2009) Forebrain melanocortin signaling enhances the hindbrain satiety response to CCK-8. Am. J. Physiol. Regul. Integr. Comp. Physiol., 296, R476 R484.
5. Borg, W.P., During, M.J., Sherwin, R.S., Borg, M.A., Brines, M.L. Shulman, G.I. (1994) Ventromedial hypothalamic lesions in rats suppress counterregulatory responses to hypoglycemia. J. Clin. Invest., 93, 1677 1682.
6. Borg, W.P., Sherwin, R.S., During, M.J., Borg, M.A. Shulman, G.I. (1995) Local ventromedial hypothalamus glucopenia triggers counterregulatory hormone release. Diabetes, 44, 180 184.
7. Borg, M.A., Sherwin, R.S., Borg, W.P., Tamborlane, W.V. Shulman, G.I. (1997) Local ventromedial hypothalamus glucose perfusion blocks counterregulation during systemic hypoglycemia in awake rats. J. Clin. Invest., 99, 361 365.
8. Broberger, C. Hokfelt, T. (2001) Hypothalamic and vagal neuropeptide circuitries regulating food intake. Physiol. Behav., 74, 669 682.
9. Chen, X., Ge, Y.L., Jiang, Z.Y., Liu, C.Q., Depoortere, I. Peeters, T.L. (2005) Effects of ghrelin on hypothalamic glucose responding neurons in rats. Brain Res., 1055, 131 136.
10. Cheung, G.W.C., Kokorovic, A., Lam, C.K.L., Chari, M. Lam, T.K.T. (2009) Intestinal cholecystokinin controls glucose production through a neuronal network. Cell Metab., 10, 99 109.
11. Conner, J.M., Lauterborn, J.C., Yan, Q., Gall, C.M. Varon, S. (1997) Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J. Neurosci., 17, 2295 2313.
12. Daniels, D. Flanagan-Cato, L.M. (2000) Functionally-defined compartments of the lordosis neural circuit in the ventromedial hypothalamus in female rats. J. Neurobiol., 45, 1 13.
13. Day, H.E., McKnight, A.T., Poat, J.A. Hughes, J. (1994) Evidence that cholecystokinin induces immediate early gene expression in the brainstem, hypothalamus and amygdala of the rat by a CCKA receptor mechanism. Neuropharmacology, 33, 719 727.
14. Dhillon, H., Zigman, J.M., Ye, C., Lee, C.E., McGovern, R.A., Tang, V., Kenny, C.D., Christiansen, L.M., White, R.D., Edelstein, E.A., Coppari, R., Balthasar, N., Cowley, M.A., Chua, S. Jr., Elmquist, J.K. Lowell, B.B. (2006) Leptin directly activates SF1 neurons in the VMH, and this action by leptin is required for normal body-weight homeostasis. Neuron, 49, 191 203.
15. Dielenberg, R.A., Hunt, G.E. McGregor, I.S. (2001) "When a rat smells a cat": the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience, 104, 1085 1097.
16. Dunning, B.E. Gerich, J.E. (2007) The role of alpha-cell dysregulation in fasting and postprandial hyperglycemia in type 2 diabetes and therapeutic implications. Endocr. Rev., 28, 253 283.
17. Dyball, R.E. Leng, G. (1986) Regulation of the milk ejection reflex in the rat. J. Physiol., 380, 239 256.
18. Elmquist, J.K., Ahima, R.S., Maratos-Flier, E., Flier, J.S. Saper, C.B. (1997) Leptin activates neurons in ventrobasal hypothalamus and brainstem. Endocrinology, 138, 839 842.
19. Fan, W., Ellacott, K.L., Halatchev, I.G., Takahashi, K., Yu, P. Cone, R.D. (2004) Cholecystokinin-mediated suppression of feeding involves the brainstem melanocortin system. Nat. Neurosci., 7, 335 336.
20. Fraser, K.A. Davison, J.S. (1992) Cholecystokinin-induced c-fos expression in the rat brain stem is influenced by vagal nerve integrity. Exp. Physiol., 77, 225 228.
21. Gibbs, J. Smith, G.P. (1977) Cholecystokinin and satiety in rats and rhesus monkeys. Am. J. Clin. Nutr., 30, 758 761.
22. Hara, A. Harris, R.A. (2002) The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anesth. Analg., 94, 313 318.
23. Heidel, E. Davidowa, H. (1998) Interactive effects of cholecystokinin-8S and serotonin on spontaneously active neurons in ventromedial hypothalamic slices. Neuropeptides, 32, 423 429.
24. Hewson, A.K., Viltart, O., McKenzie, D.N., Dyball, R.E. Dickson, S.L. (1999) GHRP-6-induced changes in electrical activity of single cells in the arcuate, ventromedial and periventricular nucleus neurones [correction of nuclei] of a hypothalamic slice preparation in vitro. J. Neuroendocrinol., 11, 919 923.
25. Hommel, J.D., Trinko, R., Sears, R.M., Georgescu, D., Liu, Z.W., Gao, X.B., Thurmon, J.J., Marinelli, M. DiLeone, R.J. (2006) Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron, 51, 678 680.
26. Kendrick, K., Leng, G. Higuchi, T. (1991) Noradrenaline, dopamine and serotonin release in the paraventricular and supraoptic nuclei of the rat in response to intravenous cholecystokinin injections. J. Neuroendocrinol., 3, 139 144.
27. King, B.M. (2006) The rise, fall, and resurrection of the ventromedial hypothalamus in the regulation of feeding behavior and body weight. Physiol. Behav., 87, 221 244.
28. Kobelt, P., Paulitsch, S., Goebel, M., Stengel, A., Schmidtmann, M., van der Voort, I.R., Tebbe, J.J., Veh, R.W., Klapp, B.F., Wiedenmann, B., Tache, Y. Monnikes, H. (2006) Peripheral injection of CCK-8S induces Fos expression in the dorsomedial hypothalamic nucleus in rats. Brain Res., 1117, 109 117.
29. Kow, L.M. Pfaff, D.W. (1986) CCK-8 stimulation of ventromedial hypothalamic neurons in vitro: a feeding-relevant event? Peptides, 7, 473 479.
30. Kumarnsit, E., Johnstone, L.E. Leng, G. (2003) Actions of neuropeptide Y and growth hormone secretagogues in the arcuate nucleus and ventromedial hypothalamic nucleus. Eur. J. Neurosci., 17, 937 944.
31. Lawrence, C.B., Celsi, F., Brennand, J. Luckman, S.M. (2000) Alternative role for prolactin-releasing peptide in the regulation of food intake. Nat. Neurosci., 3, 645 646.
32. Lawrence, C.B., Ellacott, K.L. Luckman, S.M. (2002) PRL-releasing peptide reduces food intake and may mediate satiety signaling. Endocrinology, 143, 360 367.
33. Leng, G., Dyball, R.E.J. Way, S.A. (1992) Naloxone potentiates the release of oxytocin induced by systemic administration of cholecystokinin without enhancing the electrical activity of supraoptic oxytocin neurones. Exp. Brain Res., 88, 321 325.
34. Levin, B.E., Routh, V.H., Kang, L., Sanders, N.M. Dunn-Meynell, A.A. (2004) Neuronal glucosensing: what do we know after 50 years? Diabetes, 53, 2521 2528.
35. Liddle, R.A., Green, G.M., Conrad, C.K. Williams, J.A. (1986) Proteins but not amino acids, carbohydrates, or fats stimulate cholecystokinin secretion in the rat. Am. J. Physiol., 251, G243 G248.
36. Liu, W., Liu, M., Fan, W., Nawata, H. Yanase, T. (2006) The Gly146Ala variation in human SF-1 gene: its association with insulin resistance and type 2 diabetes in Chinese. Diabetes Res. Clin. Pract., 73, 322 328.
37. Maggi, C.A. Meli, A. (1986) Suitability of urethane anesthesia for physiopharmacological investigations in various systems. Part 2: cardiovascular system. Experientia, 42, 292 297.
38. Majdic, G., Young, M., Gomez-Sanchez, E., Anderson, P., Szczepaniak, L.S., Dobbins, R.L., McGarry, J.D. Parker, K.L. (2002) Knockout mice lacking steroidogenic factor 1 are a novel genetic model of hypothalamic obesity. Endocrinology, 143, 607 614.
39. Matson, C.A., Wiater, M.F., Kuijper, J.L. Weigle, D.S. (1997) Synergy between leptin and cholecystokinin (CCK) to control daily caloric intake. Peptides, 18, 1275 1278.
40. Matson, C.A., Reid, D.F., Cannon, T.A. Ritter, R.C. (2000) Cholecystokinin and leptin act synergistically to reduce body weight. Am. J. Physiol. Regul. Integr. Comp. Physiol., 278, R882 R890.
41. Meister, B. (2007) Neurotransmitters in key neurons of the hypothalamus that regulate feeding behavior and body weight. Physiol. Behav., 92, 263 271.
42. Mercer, J.G., Hoggard, N., Williams, L.M., Lawrence, C.B., Hannah, L.T. Trayhurn, P. (1996) Localization of leptin receptor mRNA and the long form splice variant (Ob-Rb) in mouse hypothalamus and adjacent brain regions by in situ hybridization. FEBS Lett., 387, 113 116.
43. Moran, H.T. Kinzig, K.P. (2004) Gastrointestinal satiety signals II. Cholecystokinin. Am. J. Physiol., 286, g183 g188.
44. Oldendorf, W.H. (1981) Blood-brain barrier permeability to peptides: pitfalls in measurement. Peptides, 2, 109 111.
45. Raybould, H.E. (2007) Mechanisms of CCK signaling from gut to brain. Curr. Opin. Pharmacol., 7, 570 574.
46. Rinaman, L. (2003) Hindbrain noradrenergic lesions attenuate anorexia and alter central cFos expression in rats after gastric viscerosensory stimulation. J. Neurosci., 23, 10084 10092.
47. Rinaman, L., Hoffman, G.E., Dohanics, J., Le, W.W., Stricker, E.M. Verbalis, J.G. (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.
48. Sabatier, N. Leng, G. (2008) Spontaneous discharge characteristic of neurons in the ventromedial nucleus of the rat hypothalamus in vivo. Eur. J. Neurosci., 28, 693 706.
49. Sabatier, N., Brown, C.H., Ludwig, M. Leng, G. (2004) Phasic spike patterning in rat supraoptic neurones in vivo and in vitro. J. Physiol., 558, 161 180.
50. Schwartz, G.J. (2006) Integrative capacity of the caudal brainstem in the control of food intake. Philos. Trans. R. Soc. Lond. B Biol. Sci., 361, 1275 1280.
51. Schwartz, M.W., Seeley, R.J., Campfield, L.A., Burn, P. Baskin, D.G. (1996) Identification of targets of leptin action in rat hypothalamus. J. Clin. Invest., 98, 1101 1106.
52. Segal, J.P., Stallings, N.R., Lee, C.E., Zhao, L., Socci, N., Viale, A., Harris, T.M., Soares, M.B., Childs, G., Elmquist, J.K., Parker, K.L. Friedman, J.M. (2005) Use of laser-capture microdissection for the identification of marker genes for the ventromedial hypothalamic nucleus. J. Neurosci., 25, 4181 4188.
53. Shiraishi, T., Oomura, Y., Sasaki, K. Wayner, M.J. (2000) Effects of leptin and orexin-A on food intake and feeding related hypothalamic neurons. Physiol. Behav., 71, 251 261.
54. Spanswick, D., Smith, M.A., Groppi, V.E., Logan, S.D. Ashford, M.L.J. (1997) Leptin inhibits hypothalamic neurons by activation of ATP-sensitive potassium channels. Nature, 390, 521 525.
55. + channels in hypothalamic neurons of lean, but not obese rats. Nat. Neurosci., 3, 757 758.
56. Steffens, A.B., Scheurink, A.J.W., Luiten, P.G.M. Bohus, B. (1988) Hypothalamic food intake regulating areas are involved in the homeostasis of blood glucose and plasma FFA levels. Physiol. Behav., 44, 581 589.
57. Strader, A.D. Woods, S.C. (2005) Gastrointestinal hormones and food intake. Gastroenterology, 128, 175 191.
58. Sun, K. Ferguson, A.V. (1997) Cholecystokinin activates area postrema neurons in rat brain slices. Am. J. Physiol., 272, R1625 R1630.
59. Takayanagi, Y., Matsumoto, H., Nakata, M., Mera, T., Fukusumi, S., Hinuma, S., Ueta, Y., Yada, T., Leng, G. Onaka, T. (2008) Endogenous prolactin-releasing peptide regulates food intake in rodents. J. Clin. Invest., 118, 4014 4024.
60. Tong, Q., Ye, C., McCrimmon, R.J., Dhillon, H., Choi, B., Kramer, M.D., Yu, J., Yang, Z., Christiansen, L.M., Lee, C.E., Choi, C.S., Zigman, J.M., Shulman, G.I., Sherwin, R.S., Elmquist, J.K. Lowell, B.B. (2007) Synaptic glutamate release by ventromedial hypothalamic neurons is part of the neurocircuitry that prevents hypoglycemia. Cell. Metab., 5, 383 393.
61. Van der Kooy, D. (1984) Area postrema: site where cholecystokinin acts to decrease food intake. Brain Res., 295, 345 347.
62. Vianna, D.M., Borelli, K.G., Ferreira-Netto, C., Macedo, C.E. Brandao, M.L. (2003) Fos-like immunoreactive neurons following electrical stimulation of the dorsal periaqueductal gray at freezing and escape thresholds. Brain Res. Bull., 62, 179 189.
63. Wang, L., Martinez, V., Barrachina, M.D. Tache, Y. (1998) Fos expression in the brain induced by peripheral injection of CCK or leptin plus CCK in fasted lean mice. Brain Res., 791, 157 166.
64. Yano, T., Iijima, N., Kataoka, Y., Hinuma, S., Tanaka, M. Ibata, Y. (2001) Developmental expression of prolactin releasing peptide in the rat brain: localization of messenger ribonucleic acid and immunoreactive neurons. Brain Res. Dev. Brain Res., 128, 101 111.
65. Zeng, J., Patterson, B.W., Klein, S., Martin, D.R., Dagogo-Jack, S.,. Kohrt, W.M., Miller, S.B. Landt, M. (1997) Whole body leptin kinetics and renal metabolism. Am. J. Physiol., 273, E1102 E1106.
66. Zhang, Z.H. Felder, R.B. (2004) Melanocortin receptors mediate the excitatory effects of blood-borne murine leptin on hypothalamic paraventricular neurons in rat. Am. J. Physiol., 286, R303 R310.
67. Ziegler, D.R., Cullinan, W.E. Herman, J.P. (2002) Distribution of vesicular glutamate transporter mRNA in rat hypothalamus. J. Comp. Neurol., 448, 217 229.
68. Zigman, J.M., Jones, J.E., Lee, C.E., Saper, C.B. Elmquist, J.K. (2006) Expression of ghrelin receptor mRNA in the rat and the mouse brain. J. Comp. Neurol., 494, 528 548.