The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis

Neuron

Volumn 37, Issue 4, 2003, Pages 649-661

  Cowley, Michael A ^a,b   Smith, Roy G ^c   Diano, Sabrina ^d   Tschöp, Matthias ^e,f   Pronchuk, Nina ^g   Grove, Kevin L ^b   Strasburger, Christian J ^h   Bidlingmaier, Martin ^h   Esterman, Michael ^f   Heiman, Mark L ^f   Garcia Segura, Luis Miguel ⁱ   Nillni, Eduardo A ^j   Mendez, Pablo ⁱ   Low, Malcolm J ^a   Sotonyi, Peter ^d,k   Friedman, Jeffrey M ^l   Liu, Hongyan ^l   Pinto, Shirly ^l   Colmers, William F ^g   Cone, Roger D ^a   Horvath, Tamas L ^d,k   more..

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^f ELI LILLY AND COMPANY   (United States)

^g UNIVERSITY OF ALBERTA   (Canada)

^h LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

ⁱ INSTITUTO CAJAL   (Spain)

^j RHODE ISLAND HOSPITAL   (United States)

^k SZENT ISTVÁN UNIVERSITY   (Hungary)

^l ROCKEFELLER UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AGOUTI RELATED PROTEIN; CORTICOTROPIN RELEASING FACTOR; GHRELIN; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN;

ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARCUATE NUCLEUS; ARTICLE; BRAIN NERVE CELL; BRAIN THIRD VENTRICLE; CENTRAL NERVOUS SYSTEM; EFFERENT NERVE; ELECTROPHYSIOLOGY; ENERGY BALANCE; FEMALE; HOMEOSTASIS; HYPOTHALAMUS; NERVE ENDING; NERVE STIMULATION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT;

EID: 0037456519     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(03)00063-1     Document Type: Article

References (62)

1. Ahima R.S., Saper C.B., Flier J.S., Elmquist J.K. Leptin regulation of neuroendocrine systems. Front. Neuroendocrinol. 21:2000;263-307.
2. Arvat E., Di Vito L., Broglio F., Papotti M., Muccioli G., Dieguez C., Casanueva F.F., Deghenghi R., Camanni F., Ghigo E. Preliminary evidence that Ghrelin, the natural GH secretagogue (GHS)- receptor ligand, strongly stimulates GH secretion in humans. J. Endocrinol. Invest. 23:2000;493-495.
3. Arvat E., Maccario M., Di Vito L., Broglio F., Benso A., Gottero C., Papotti M., Muccioli G., Dieguez C., Casanueva F.F.et al. Endocrine activities of ghrelin, a natural growth hormone secretagogue (GHS), in humans. comparison and interactions with hexarelin, a nonnatural peptidyl GHS, and GH-releasing hormone J. Clin. Endocrinol. Metab. 86:2001;1169-1174.
4. Banks W.A., Tschop M., Heiman M.L. Extent and direction of ghrelin transport across the blood brain barrier is determined by its unique primary structure. J. Pharmacol. Exp. Ther. 302:2002;822-827.
5. Batterham R.L., Cowley M.A., Small C.J., Herzog H., Cohen M.A., Dakin C.L., Wren A.M., Brynes A.E., Low M.J., Ghatei M.A.et al. Gut hormone PYY(3-36) physiologically inhibits food intake. Nature. 418:2002;650-654.
6. Bednarek M.A., Feighner S.D., Pong S.S., McKee K.K., Hreniuk D.L., Silva M.V., Warren V.A., Howard A.D., Van Der Ploeg L.H., Heck J.V. Structure-function studies on the new growth hormone-releasing peptide, ghrelin. minimal sequence of ghrelin necessary for activation of growth hormone secretagogue receptor 1a J. Med. Chem. 43:2000;4370-4376.
7. Brownstein M., Arimura A., Sato H., Schally A.V., Kizer J.S. The regional distribution of somatostatin in the rat brain. Endocrinology. 96:1975;1456-1461.
8. Chronwall B.M., DiMaggio D.A., Massari V.J., Pickel V.M., Ruggiero D.A., O'Donohue T.L. The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience. 15:1985;1159-1181.
9. Cowley M.A., Pronchuk N., Fan W., Dinulescu D.M., Colmers W.F., Cone R.D. Integration of NPY, AGRP, and melanocortin signals in the hypothalamic paraventricular nucleus. evidence of a cellular basis for the adipostat Neuron. 24:1999;155-163.
10. Cowley M.A., Smart J.L., Rubinstein M., Cerdan M.G., Diano S., Horvath T.L., Cone R.D., Low M.J. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature. 411:2001;480-484.
11. Cummings D.E., Purnell J.Q., Frayo R.S., Schmidova K., Wisse B.E., Weigle D.S. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes. 50:2001;1714-1719.
12. Date Y., Kojima M., Hosoda H., Sawaguchi A., Mondal M.S., Suganuma T., Matsukura S., Kangawa K., Nakazato M. 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. 141:2000;4255-4261.
13. Date Y., Murakami N., Toshinai K., Matsukura S., Niijima A., Matsuo H., Kangawa K., Nakazato M. The role of the gastric afferent vagal nerve in ghrelin-induced feeding and growth hormone secretion in rats. Gastroenterology. 123:2002;1120-1128.
14. de Lecea L., Kilduff T.S., Peyron C., Gao X., Foye P.E., Danielson P.E., Fukuhara C., Battenberg E.L., Gautvik V.T., Bartlett F.S. 2nd et al. The hypocretins. hypothalamus-specific peptides with neuroexcitatory activity Proc. Natl. Acad. Sci. USA. 95:1998;322-327.
15. DeFalco J., Tomishima M., Liu H., Zhao C., Cai X., Marth J.D., Enquist L., Friedman J.M. Virus-assisted mapping of neural inputs to a feeding center in the hypothalamus. Science. 291:2001;2608-2613.
16. Dickson S.L., Luckman S.M. Induction of c-fos messenger ribonucleic acid in neuropeptide Y and growth hormone (GH)-releasing factor neurons in the rat arcuate nucleus following systemic injection of the GH secretagogue, GH-releasing peptide-6. Endocrinology. 138:1997;771-777.
17. Dornonville de la Cour C., Bjorkqvist M., Sandvik A.K., Bakke I., Zhao C.M., Chen D., Hakanson R. A-like cells in the rat stomach contain ghrelin and do not operate under gastrin control. Regul. Pept. 99:2001;141-150.
18. Fong T.M., Mao C., MacNeil T., Kalyani R., Smith T., Weinberg D., Tota M.R., Van der Ploeg L.H. ART (protein product of agouti-related transcript) as an antagonist of MC-3 and MC-4 receptors. Biochem. Biophys. Res. Commun. 237:1997;629-631.
19. Fuxe K., Tinner B., Caberlotto L., Bunnemann B., Agnati L.F. NPY Y1 receptor like immunoreactivity exists in a subpopulation of beta-endorphin immunoreactive nerve cells in the arcuate nucleus. a double immunolabelling analysis in the rat Neurosci. Lett. 225:1997;49-52.
20. Gualillo O., Caminos J., Blanco M., Garcia-Caballero T., Kojima M., Kangawa K., Dieguez C., Casanueva F. Ghrelin, a novel placental-derived hormone. Endocrinology. 142:2001;788-794.
21. Guan X.M., Yu H., Palyha O.C., McKee K.K., Feighner S.D., Sirinathsinghji D.J., Smith R.G., Van der Ploeg L.H., Howard A.D. Distribution of mRNA encoding the growth hormone secretagogue receptor in brain and peripheral tissues. Brain Res. Mol. Brain Res. 48:1997;23-29.
22. Hahn T.M., Breininger J.F., Baskin D.G., Schwartz M.W. Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat. Neurosci. 1:1998;271-272.
23. Haskell-Luevano C., Chen P., Li C., Chang K., Smith M.S., Cameron J.L., Cone R.D. Characterization of the neuroanatomical distribution of agouti-related protein immunoreactivity in the rhesus monkey and the rat. Endocrinology. 140:1999;1408-1415.
24. Hattori N., Saito T., Yagyu T., Jiang B.H., Kitagawa K., Inagaki C. GH, GH receptor, GH secretagogue receptor, and ghrelin expression in human T cells, B cells, and neutrophils. J. Clin. Endocrinol. Metab. 86:2001;4284-4291.
25. Heisler L.K., Cowley M.A., Tecott L.H., Fan W., Low M.J., Smart J.L., Rubinstein M., Tatro J.B., Marcus J.N., Holstege H.et al. Activation of central melanocortin pathways by fenfluramine. Science. 297:2002;609-611.
26. Hewson A.K., Dickson S.L. Systemic administration of ghrelin induces Fos and Egr-1 proteins in the hypothalamic arcuate nucleus of fasted and fed rats. J. Neuroendocrinol. 12:2000;1047-1049.
27. Horvath T.L. Suprachiasmatic efferents avoid phenestrated capillaries but innervate neuroendocrine cells including those producing dopamine. Endocrinology. 138:1997;1312-1320.
28. Horvath T.L. An alternate pathway for visual signal integration into the hypothalamo-pituitary axis. retinorecipient intergeniculate neurons project to various regions of the hypothalamus and innervate neuroendocrine cells including those producing dopamine J. Neurosci. 18:1998;1546-1558.
29. Horvath T.L., Bechmann I., Naftolin F., Kalra S.P., Leranth C. Heterogeneity in the neuropeptide Y-containing neurons of the rat arcuate nucleus. GABAergic and non-GABAergic subpopulations Brain Res. 756:1997;283-286.
30. Horvath T.L., Diano S., Sotonyi P., Heiman M., Tschop M. Minireview. ghrelin and the regulation of energy balance - a hypothalamic perspective Endocrinology. 142:2001;4163-4169.
31. Kalra S.P., Dube M.G., Pu S., Xu B., Horvath T.L., Kalra P.S. Interacting appetite-regulating pathways in the hypothalamic regulation of body weight. Endocr. Rev. 20:1999;68-100.
32. Kamegai J., Tamura H., Shimizu T., Ishii S., Sugihara H., Wakabayashi I. Central effect of ghrelin, an endogenous growth hormone secretagogue, on hypothalamic peptide gene expression. Endocrinology. 141:2000;4797-4800.
33. Kamegai J., Tamura H., Shimizu T., Ishii S., Sugihara H., Wakabayashi I. Chronic central infusion of ghrelin increases hypothalamic neuropeptide Y and Agouti-related protein mRNA levels and body weight in rats. Diabetes. 50:2001;2438-2443.
34. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature. 402:1999;656-660.
35. Korbonits M., Bustin S.A., Kojima M., Jordan S., Adams E.F., Lowe D.G., Kangawa K., Grossman A.B. The expression of the growth hormone secretagogue receptor ligand ghrelin in normal and abnormal human pituitary and other neuroendocrine tumors. J. Clin. Endocrinol. Metab. 86:2001;881-887.
36. Lu S., Guan J.L., Wang Q.P., Uehara K., Yamada S., Goto N., Date Y., Nakazato M., Kojima M., Kangawa K., Shioda S. Immunocytochemical observation of ghrelin-containing neurons in the rat arcuate nucleus. Neurosci. Lett. 321:2001;157-160.
37. Mori K., Yoshimoto A., Takaya K., Hosoda K., Ariyasu H., Yahata K., Mukoyama M., Sugawara A., Hosoda H., Kojima M.et al. Kidney produces a novel acylated peptide, ghrelin. FEBS Lett. 486:2000;213-216.
38. Nakazato M., Murakami N., Date Y., Kojima M., Matsuo H., Kangawa K., Matsukura S. A role for ghrelin in the central regulation of feeding. Nature. 409:2001;194-198.
39. Oliver C., Barnea A., Warberg J., Eskay R.L., Porter J.C. Distribution, characterization, and subcellular localization of MSH in the brain. Front. Horm. Res. 4:1977;162-166.
40. Powis J.E., Bains J.S., Ferguson A.V. Leptin depolarizes rat hypothalamic paraventricular nucleus neurons. Am. J. Physiol. 274:1998;R1468-R1472.
41. Pronchuk N., Beck-Sickinger A.G., Colmers W.F. Multiple NPY receptors Inhibit GABA(A) synaptic responses of rat medial parvocellular effector neurons in the hypothalamic paraventricular nucleus. Endocrinology. 143:2002;535-543.
42. Sakata I., Nakamura K., Yamazaki M., Matsubara M., Hayashi Y., Kangawa K., Sakai T. Ghrelin-producing cells exist as two types of cells, closed- and opened- type cells, in the rat gastrointestinal tract. Peptides. 23:2002;531-536.
43. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., Williams S.C., Richardson J.A., Kozlowski G.P., Wilson S.et al. Orexins and orexin receptors. a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior Cell. 92:1998;573-585.
44. Shintani M., Ogawa Y., Ebihara K., Aizawa-Abe M., Miyanaga F., Takaya K., Hayashi T., Inoue G., Hosoda K., Kojima M.et al. Ghrelin, an endogenous growth hormone secretagogue, is a novel orexigenic peptide that antagonizes leptin action through the activation of hypothalamic neuropeptide Y/Y1 receptor pathway. Diabetes. 50:2001;227-232.
45. Smith R.G., Van der Ploeg L.H., Howard A.D., Feighner S.D., Cheng K., Hickey G.J., Wyvratt M.J. Jr., Fisher M.H., Nargund R.P., Patchett A.A. Peptidomimetic regulation of growth hormone secretion. Endocr. Rev. 18:1997;621-645.
46. Spanswick D., Smith M.A., Groppi V.E., Logan S.D., Ashford M.L. Leptin inhibits hypothalamic neurons by activation of ATP-sensitive potassium channels. Nature. 390:1997;521-525.
47. Tanaka M., Hayashida Y., Nakao N., Nakai N., Nakashima K. Testis-specific and developmentally induced expression of a ghrelin gene-derived transcript that encodes a novel polypeptide in the mouse. Biochim. Biophys. Acta. 1522:2001;62-65.
48. Toran-Allerand C.D., Guan X., MacLusky N.J., Horvath T.L., Diano S., Singh M., Connolly E.S. Jr., Nethrapalli I.S., Tinnikov A.A. Er-x. a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury J. Neurosci. 22:2002;8391-8401.
49. Toshinai K., Mondal M.S., Nakazato M., Date Y., Murakami N., Kojima M., Kangawa K., Matsukura S. Upregulation of Ghrelin expression in the stomach upon fasting, insulin-induced hypoglycemia, and leptin administration. Biochem. Biophys. Res. Commun. 281:2001;1220-1225.
50. Tschop M., Smiley D.L., Heiman M.L. Ghrelin induces adiposity in rodents. Nature. 407:2000;908-913.
51. Tschop M., Wawarta R., Riepl R.L., Friedrich S., Bidlingmaier M., Landgraf R., Folwaczny C. Post-prandial decrease of circulating human ghrelin levels. J. Endocrinol. Invest. 24:2001;RC19-RC21. a.
52. Tschop M., Weyer C., Tataranni P.A., Devanarayan V., Ravussin E., Heiman M.L. Circulating ghrelin levels are decreased in human obesity. Diabetes. 50:2001;707-709. b.
53. Tschop M., Statnick M.A., Suter T.M., Heiman M.L. GH-releasing peptide-2 increases fat mass in mice lacking NPY. indication for a crucial mediating role of hypothalamic agouti-related protein Endocrinology. 143:2002;558-568.
54. Tung Y.C., Hewson A.K., Dickson S.L. Actions of leptin on growth hormone secretagogue-responsive neurones in the rat hypothalamic arcuate nucleus recorded in vitro. J. Neuroendocrinol. 13:2001;209-215.
55. Volante M., Allia E., Gugliotta P., Funaro A., Broglio F., Deghenghi R., Muccioli G., Ghigo E., Papotti M. Expression of ghrelin and of the GH secretagogue receptor by pancreatic islet cells and related endocrine tumors. J. Clin. Endocrinol. Metab. 87:2002;1300-1308.
56. Wang L., Saint-Pierre D.H., Tache Y. Peripheral ghrelin selectively increases Fos expression in neuropeptide Y - synthesizing neurons in mouse hypothalamic arcuate nucleus. Neurosci. Lett. 325:2002;47-51.
57. Watts A.G., Swanson L.W., Sanchez-Watts G. Efferent projections of the suprachiasmatic nucleus. I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat J. Comp. Neurol. 258:1987;204-229.
58. Willesen M.G., Kristensen P., Romer J. Co-localization of growth hormone secretagogue receptor and NPY mRNA in the arcuate nucleus of the rat. Neuroendocrinology. 70:1999;306-316.
59. Wren A.M., Small C.J., Ward H.L., Murphy K.G., Dakin C.L., Taheri S., Kennedy A.R., Roberts G.H., Morgan D.G., Ghatei M.A., Bloom S.R. The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology. 141:2000;4325-4328.
60. Wren A.M., Seal L.J., Cohen M.A., Brynes A.E., Frost G.S., Murphy K.G., Dhillo W.S., Ghatei M.A., Bloom S.R. Ghrelin enhances appetite and increases food intake in humans. J. Clin. Endocrinol. Metab. 86:2001;5992. a.
61. Wren A.M., Small C.J., Abbott C.R., Dhillo W.S., Seal L.J., Cohen M.A., Batterham R.L., Taheri S., Stanley S.A., Ghatei M.A., Bloom S.R. Ghrelin causes hyperphagia and obesity in rats. Diabetes. 50:2001;2540-2547. b.
62. Zamir N., Skofitsch G., Jacobowitz D.M. Distribution of immunoreactive melanin-concentrating hormone in the central nervous system of the rat. Brain Res. 373:1986;240-245.