Injection of Urocortin 3 into the ventromedial hypothalamus modulates feeding, blood glucose levels, and hypothalamic POMC gene expression but not the HPA axis

American Journal of Physiology - Endocrinology and Metabolism

Volumn 298, Issue 2, 2010, Pages

  Chen, Peilin ^a   Vaughan, Joan ^b   Donaldson, Cindy ^b   Vale, Wylie ^b   Li, Chien ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Blood glucose; Corticotrophin releasing factor; Feeding; Hypothalamic pituitary adrenal axis; Hypothalamus; Urocortin

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; GLUCOSE; INSULIN; MELANOCORTIN; MESSENGER RNA; PROOPIOMELANOCORTIN; UROCORTIN III;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; FEEDING; FOOD INTAKE; GENE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HORMONE RELEASE; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; INJECTION; INSULIN BLOOD LEVEL; MALE; NONHUMAN; POMC GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ZONA INCERTA;

ADRENOCORTICOTROPIC HORMONE; ANALYSIS OF VARIANCE; ANIMALS; APPETITE REGULATION; ARCUATE NUCLEUS; BLOOD GLUCOSE; ENERGY METABOLISM; GENE EXPRESSION REGULATION; HOMEOSTASIS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INSULIN; MALE; MICROINJECTIONS; PITUITARY-ADRENAL SYSTEM; PRO-OPIOMELANOCORTIN; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; UROCORTINS; VENTROMEDIAL HYPOTHALAMIC NUCLEUS;

EID: 74949083784     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00402.2009     Document Type: Article

References (57)

1. Aravich PF, Beltt BM. Perifornical fiber system mediates VMH electrically-induced suppression of feeding. Physiol Behav 29: 195-200, 1982.
2. Ashcroft FM. Adenosine 5′-triphosphate-sensitive potassium channels. Annu Rev Neurosci 11: 97-118, 1988.
3. Avrith D, Mogenson GJ. Reversible hyperphagia and obesity following intracerebral microinjections of colchicine into the ventromedial hypothalamus of the rat. Brain Res 153: 99-107, 1978.
4. Bingham NC, Anderson KK, Reuter AL, Stallings NR, Parker KL. Selective loss of leptin receptors in the ventromedial hypothalamic nucleus results in increased adiposity and a metabolic syndrome. Endocrinology 149: 2138-2148, 2008.
5. Brown FD, Fessler RG, Rachlin JR, Mullan S. Changes in food intake with electrical stimulation of the ventromedial hypothalamus in dogs. J Neurosurg 60: 1253-1257, 1984.
6. 1 receptor mRNA expression. J Neurosci 15: 6340-6350, 1995.
7. Chen P, Li C, Haskell-Luevano C, Cone RD, Smith MS. Altered expression of agouti-related protein and its colocalization with neuropeptide Y in the arcuate nucleus of the hypothalamus during lactation. Endocrinology 140: 2645-2650, 1999.
8. de Jong A, Strubbe JH, Steffens AB. Hypothalamic influence on insulin and glucagon release in the rat. Am J Physiol Endocrinol Metab Gastrointest Physiol 233: E380-E388, 1977.
9. Dhillon H, Zigman JM, Ye C, Lee CE, McGovern RA, Tang V, Kenny CD, Christiansen LM, White RD, Edelstein EA, Coppari R, Balthasar N, Cowley MA, Chua S, Jr, Elmquist JK, Lowell BB. Leptin directly activates SF1 neurons in the VMH, and this action by leptin is required for normal body-weight homeostasis. Neuron 49: 191-203, 2006.
10. Digruccio M, Chen P, Cheng J, Moenter S, Li C. Generation of transgenic mice expressing Cre recombinase in type 2 corticotropin-releasing factor receptor (CRFR2) neurons in the brain. Soc Neurosci Abst: 198.111, 2007.
11. Dunn JD, Whitener J. Plasma corticosterone responses to electrical stimulation of the amygdaloid complex: cytoarchitectural specificity. Neuroendocrinology 42: 211-217, 1986.
12. Ellacott KL, Cone RD. The central melanocortin system and the integration of short- and long-term regulators of energy homeostasis. Recent Prog Horm Res 59: 395-408, 2004.
13. Elmquist JK, Bjorbaek C, Ahima RS, Flier JS, Saper CB. Distributions of leptin receptor mRNA isoforms in the rat brain. J Comp Neurol 395: 535-547, 1998.
14. Fekete EM, Inoue K, Zhao Y, Rivier JE, Vale WW, Szucs A, Koob GF, Zorrilla EP. 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, 2007.
15. Fekete EM, Zhao Y, Li C, Sabino V, Vale WW, Zorrilla EP. Social defeat stress activates medial amygdala cells that express type 2 corticotropin-releasing factor receptor mRNA. Neuroscience 162: 5-13, 2009.
16. Fremeau RT Jr, royer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31: 247-260, 2001.
17. Herzog E, Bellenchi GC, Gras C, Bernard V, Ravassard P, Bedet C, Gasnier B, Giros B, El Mestikawy S. The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21: RC181, 2001.
18. Hetherington AW, Ranson SW. Hypothalamic lesions and adiposity in the rat. Anat Rec 78: 149-161, 1940.
19. Hochgeschwender U, Costa JL, Reed P, Bui S, Brennan MB. Altered glucose homeostasis in proopiomelanocortin-null mouse mutants lacking central and peripheral melanocortin. Endocrinology 144: 5194-5202, 2003.
20. Hsu SY, Hsueh AJ. Human stresscopin and stresscopin-related peptide are selective ligands for the type 2 corticotropin-releasing hormone receptor. Nat Med 7: 605-611, 2001.
21. Jacob RJ, Dziura J, Medwick MB, Leone P, Caprio S, During M, Shulman GI, Sherwin RS. The effect of leptin is enhanced by microinjection into the ventromedial hypothalamus. Diabetes 46: 150-152, 1997.
22. Jamieson PM, Li C, Kukura C, Vaughan J, Vale W. Urocortin 3 modulates the neuroendocrine stress response and is regulated in rat amygdala and hypothalamus by stress and glucocorticoids. Endocrinology 147: 4578-4588, 2006.
23. Kalra PS, Dube MG, Xu B, Kalra SP. Increased receptor sensitivity to neuropeptide Y in the hypothalamus may underlie transient hyperphagia and body weight gain. Regul Pept 72: 121-130, 1997.
24. Kang L, Dunn-Meynell AA, Routh VH, Gaspers LD, Nagata Y, Nishimura T, Eiki J, Zhang BB, Levin BE. Glucokinase is a critical regulator of ventromedial hypothalamic neuronal glucosensing. Diabetes 55: 412-420, 2006.
25. Kang L, Routh VH, Kuzhikandathil EV, Gaspers LD, Levin BE. Physiological and molecular characteristics of rat hypothalamic ventromedial nucleus glucosensing neurons. Diabetes 53: 549-559, 2004.
26. King BM. The rise, fall, and resurrection of the ventromedial hypothalamus in the regulation of feeding behavior and body weight. Physiol Behav 87: 221-244, 2006.
27. King BM, Cook JT, Dallman MF. Hyperinsulinemia in rats with obesity-inducing amygdaloid lesions. Am J Physiol Regul Integr Comp Physiol 271: R1156-R1159, 1996.
28. King BM, Cook JT, Rossiter KN, Rollins BL. Obesity-inducing amygdala lesions: examination of anterograde degeneration and retrograde transport. Am J Physiol Regul Integr Comp Physiol 284: R965-R982, 2003.
29. King BM, Zansler CA, Tatford AC, 3rd Neville KL, Sam H, Kass JM, Dallman MF. Level of corticosterone replacement determines body weight gain in adrenalectomized rats with VMH lesions. Physiol Behav 54: 1187-1190, 1993.
30. Levin BE, Dunn-Meynell AA, Routh VH. Brain glucose sensing and body energy homeostasis: role in obesity and diabetes. Am J Physiol Regul Integr Comp Physiol 276: R1223-R1231, 1999.
31. Lewis K, Li C, Perrin MH, Blount A, Kunitake K, Donaldson C, Vaughan J, Reyes TM, Gulyas J, Fischer W, Bilezikjian L, Rivier J, Sawchenko PE, Vale WW. Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proc Natl Acad Sci USA 98: 7570-7575, 2001.
32. Li C, Vaughan J, Vale W. Urocortin III afferents into the ventromedial hypothalamaus of the rat. Soc Neurosci Abst 396: 320, 2003.
33. Li C, Vaughan J, Sawchenko PE, Vale WW. Urocortin III-immunoreactive projections in rat brain: partial overlap with sites of type 2 corticotrophin-releasing factor receptor expression. J Neurosci 22: 991-1001, 2002.
34. Lynch RM, Tompkins LS, Brooks HL, Dunn-Meynell AA, Levin BE. Localization of glucokinase gene expression in the rat brain. Diabetes 49: 693-700, 2000.
35. Majdic G, Young M, Gomez-Sanchez E, Anderson P, Szczepaniak LS, Dobbins RL, McGarry JD, Parker KL. Knockout mice lacking steroidogenic factor 1 are a novel genetic model of hypothalamic obesity. Endocrinology 143: 607-614, 2002.
36. McCrimmon RJ, Song Z, Cheng H, McNay EC, Weikart-Yeckel C, Fan X, Routh VH, Sherwin RS. Corticotrophin-releasing factor receptors within the ventromedial hypothalamus regulate hypoglycemia-induced hormonal counterregulation. J Clin Invest 116: 1723-1730, 2006.
37. Miki T, Liss B, Minami K, Shiuchi T, Saraya A, Kashima Y, Horiuchi M, Ashcroft F, Minokoshi Y, Roeper J, Seino S. ATP-sensitive K+ channels in the hypothalamus are essential for the maintenance of glucose homeostasis. Nat Neurosci 4: 507-512, 2001.
38. Narita K, Nishihara M, Takahashi M. Concomitant regulation of running activity and metabolic change by the ventromedial nucleus of the hypothalamus. Brain Res 642: 290-296, 1994.
39. Ohata H, Shibasaki T. Effects of urocortin 2 and 3 on motor activity and food intake in rats. Peptides 25: 1703-1709, 2004.
40. Ohata H, Suzuki K, Oki Y, Shibasaki T. Urocortin in the ventromedial hypothalamic nucleus acts as an inhibitor of feeding behavior in rats. Brain Res 861: 1-7, 2000.
41. Parton LE, Ye CP, Coppari R, Enriori PJ, Choi B, Zhang CY, Xu C, Vianna CR, Balthasar N, Lee CE, Elmquist JK, Cowley MA, Lowell BB. Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity. Nature 449: 228-232, 2007.
42. Paxions G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 1998.
43. Pelleymounter MA, Joppa M, Ling N, Foster AC. Behavioral and neuroendocrine effects of the selective CRF2 receptor agonists urocortin II and urocortin III. Peptides 25: 659-666, 2004.
44. Penicaud L, Kinebanyan MF, Ferre P, Morin J, Kande J, Smadja C, Marfaing-Jallat P, Picon L. Development of VMH obesity: in vivo insulin secretion and tissue insulin sensitivity. Am J Physiol Endocrinol Metab 257: E255-E260, 1989.
45. Rohner F, Dufour AC, Karakash C, Le Marchand Y, Ruf KB, Jeanrenaud B. Immediate effect of lesion of the ventromedial hypothalamic area upon glucose-induced insulin secretion in anaesthetized rats. Diabetologia 13: 239-242, 1977.
46. Rollins BL, King BM. Amygdala-lesion obesity: what is the role of the various amygdaloid nuclei? Am J Physiol Regul Integr Comp Physiol 279: R1348-R1356, 2000.
47. Routh VH. Glucosensing neurons in the ventromedial hypothalamic nucleus (VMN) and hypoglycemia-associated autonomic failure (HAAF). Diabetes Metab Res Rev 19: 348-356, 2003.
48. Shimazu T, Ishikawa K. Modulation by the hypothalamus of glucagon and insulin secretion in rabbits: studies with electrical and chemical stimulations. Endocrinology 108: 605-611, 1981.
49. Shimizu N, Oomura Y, Plata-Salaman CR, Morimoto M. Hyperphagia and obesity in rats with bilateral ibotenic acid-induced lesions of the ventromedial hypothalamic nucleus. Brain Res 416: 153-156, 1987.
50. Steffens AB. The modulatory effect of the hypothalamus on glucagon and insulin secretion in the rat. Diabetologia Suppl 20: 411-416, 1981.
51. Sternson SM, Shepherd GMG, Friedman JM. Topographic mapping of VMH -> arcuate nucleus microcircuits and their reorganization by fasting. Nat Neurosci 8: 1356-1363, 2005.
52. Suemaru S, Darlington DN, Akana SF, Cascio CS, Dallman MF. Ventromedial hypothalamic lesions inhibit corticosteroid feedback regulation of basal ACTH during the trough of the circadian rhythm. Neuroendocrinology 61: 453-463, 1995.
53. Takamori S, Rhee JS, Rosenmund C, Jahn R. Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGLUT2). J Neurosci 21: RC182, 2001.
54. Tokunaga K, Fukushima M, Kemnitz JW, Bray GA. Effect of vagotomy on serum insulin in rats with paraventricular or ventromedial hypothalamic lesions. Endocrinology 119: 1708-1711, 1986.
55. Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, Arias C, Prins GS, Perrin M, Vale W, Sawchenko PE. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428: 191-212, 2000.
56. Venihaki M, Sakihara S, Subramanian S, Dikkes P, Weninger SC, Liapakis G, Graf T, Majzoub JA. Urocortin III, a brain neuropeptide of the corticotropin-releasing hormone family: modulation by stress and attenuation of some anxiety-like behaviours. J Neuroendocrinol 16: 411-422, 2004.
57. Wang R, Liu X, Hentges ST, Dunn-Meynell AA, Levin BE, Wang W, Routh VH. The regulation of glucose-excited neurons in the hypothalamic arcuate nucleus by glucose and feeding-relevant peptides. Diabetes 53: 1959-1965, 2004.