Activation of the melanocortin-4 receptor causes enhanced excitation in presympathetic paraventricular neurons in obese Zucker rats

Regulatory Peptides

Volumn 166, Issue 1-3, 2011, Pages 112-120

  Ye, Zeng You ^a   Li, De Pei ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Hypothalamus; Melanocortin 4 receptors; Obese zucker rats; Sympathetic nervous system

Indexed keywords

ALPHA INTERMEDIN; GUANOSINE 5' O (2 THIODIPHOSPHATE); MELANOCORTIN 4 RECEPTOR; MELANOTAN II; N ACETYL ALPHA INTERMEDIN[4-10]CYCLO[4 NORLEUCINE 5 ASPARTIC ACID 7 [3 (2 NAPHTHYL)ALANINE] 10 LYSINAMIDE];

ADRENERGIC SYSTEM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIALYSIS; LEAN BODY WEIGHT; MALE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NEUROMODULATION; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SYNAPTIC TRANSMISSION; THALAMUS MIDLINE NUCLEUS; ZUCKER RAT;

ALPHA-MSH; ANIMALS; BICUCULLINE; GUANOSINE DIPHOSPHATE; KYNURENIC ACID; MALE; MELANOCYTE-STIMULATING HORMONES; NEURONS; OBESITY; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PATCH-CLAMP TECHNIQUES; PEPTIDES, CYCLIC; RATS; RATS, ZUCKER; RECEPTOR, MELANOCORTIN, TYPE 4; THIONUCLEOTIDES;

RATTUS;

EID: 78650177925     PISSN: 01670115     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.regpep.2010.10.001     Document Type: Article

References (56)

1. Hall J.E., da Silva A.A., do Carmo J.M., Dubinion J., Hamza S., Munusamy S., Smith G., Stec D.E. Obesity-induced Hypertension: Role of Sympathetic Nervous System, Leptin and Melanocortins. J Biol Chem 2010, 285(23):17271-17276.
2. Hall J.E., Brands M.W., Hildebrandt D.A., Kuo J., Fitzgerald S. Role of sympathetic nervous system and neuropeptides in obesity hypertension. Braz J Med Biol Res 2000, 33:605-618.
3. Rocchini A.P., Mao H.Z., Babu K., Marker P., Rocchini A.J. Clonidine prevents insulin resistance and hypertension in obese dogs. Hypertension 1999, 33:548-553.
4. Carlson S.H., Shelton J., White C.R., Wyss J.M. Elevated sympathetic activity contributes to hypertension and salt sensitivity in diabetic obese Zucker rats. Hypertension 2000, 35:403-408.
5. Xiang L., Dearman J., Abram S.R., Carter C., Hester R.L. Insulin resistance and impaired functional vasodilation in obese Zucker rats. Am J Physiol Heart Circ Physiol 2008, 294:H1658-H1666.
6. Ruggeri P., Brunori A., Cogo C.E., Storace D., Di Nardo F., Burattini R. Enhanced sympathetic reactivity associates with insulin resistance in the young Zucker rat. Am J Physiol Regul Integr Comp Physiol 2006, 291:R376-R382.
7. Kasiske B.L., O'Donnell M.P., Keane W.F. The Zucker rat model of obesity, insulin resistance, hyperlipidemia, and renal injury. Hypertension 1992, 19:I110-I115.
8. Overton J.M., Williams T.D., Chambers J.B., Rashotte M.E. Cardiovascular and metabolic responses to fasting and thermoneutrality are conserved in obese Zucker rats. Am J Physiol Regul Integr Comp Physiol 2001, 280:R1007-R1015.
9. Morgan D.A., Anderson E.A., Mark A.L. Renal sympathetic nerve activity is increased in obese Zucker rats. Hypertension 1995, 25:834-838.
10. D'Angelo G., Mintz J.D., Tidwell J.E., Schreihofer A.M., Pollock D.M., Stepp D.W. Exaggerated cardiovascular stress responses and impaired beta-adrenergic-mediated pressor recovery in obese Zucker rats. Hypertension 2006, 48:1109-1115.
11. Frisbee J.C. Hypertension-independent microvascular rarefaction in the obese Zucker rat model of the metabolic syndrome. Microcirculation 2005, 12:383-392.
12. Schreihofer A.M., Hair C.D., Stepp D.W. Reduced plasma volume and mesenteric vascular reactivity in obese Zucker rats. Am J Physiol Regul Integr Comp Physiol 2005, 288:R253-R261.
13. Mountjoy K.G., Mortrud M.T., Low M.J., Simerly R.B., Cone R.D. Localization of the melanocortin-4 receptor (MC4-R) in neuroendocrine and autonomic control circuits in the brain. Mol Endocrinol 1994, 8:1298-1308.
14. Mountjoy K.G., Wong J. Obesity, diabetes and functions for proopiomelanocortin-derived peptides. Mol Cell Endocrinol 1997, 128:171-177.
15. Cone R.D. The central melanocortin system and energy homeostasis. Trends Endocrinol Metab 1999, 10:211-216.
16. Greenfield J.R., Miller J.W., Keogh J.M., Henning E., Satterwhite J.H., Cameron G.S., Astruc B., Mayer J.P., Brage S., See T.C., Lomas D.J., O'Rahilly S., Farooqi I.S. Modulation of blood pressure by central melanocortinergic pathways. N Engl J Med 2009, 360:44-52.
17. da Silva A.A., Kuo J.J., Hall J.E. Role of hypothalamic melanocortin 3/4-receptors in mediating chronic cardiovascular, renal, and metabolic actions of leptin. Hypertension 2004, 43:1312-1317.
18. Huszar D., Lynch C.A., Fairchild-Huntress V., Dunmore J.H., Fang Q., Berkemeier L.R., Gu W., Kesterson R.A., Boston B.A., Cone R.D., Smith F.J., Campfield L.A., Burn P., Lee F. Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 1997, 88:131-141.
19. Tallam L.S., Stec D.E., Willis M.A., da Silva A.A., Hall J.E. Melanocortin-4 receptor-deficient mice are not hypertensive or salt-sensitive despite obesity, hyperinsulinemia, and hyperleptinemia. Hypertension 2005, 46:326-332.
20. Schwartz M.W., Woods S.C., Porte D., Seeley R.J., Baskin D.G. Central nervous system control of food intake. Nature 2000, 404:661-671.
21. Ahima R.S., Flier J.S. Leptin. Annu Rev Physiol 2000, 62:413-437.
22. Elias C.F., Aschkenasi C., Lee C., Kelly J., Ahima R.S., Bjorbaek C., Flier J.S., Saper C.B., Elmquist J.K. Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron 1999, 23:775-786.
23. Harrold J.A., Widdowson P.S., Williams G. Altered energy balance causes selective changes in melanocortin-4(MC4-R), but not melanocortin-3 (MC3-R), receptors in specific hypothalamic regions: further evidence that activation of MC4-R is a physiological inhibitor of feeding. Diabetes 1999, 48:267-271.
24. Swanson L.W., Sawchenko P.E. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 1983, 6:269-324.
25. Coote J.H., Yang Z., Pyner S., Deering J. Control of sympathetic outflows by the hypothalamic paraventricular nucleus. Clin Exp Pharmacol Physiol 1998, 25:461-463.
26. Dampney R.A., Horiuchi J., Killinger S., Sheriff M.J., Tan P.S., McDowall L.M. Long-term regulation of arterial blood pressure by hypothalamic nuclei: some critical questions. Clin Exp Pharmacol Physiol 2005, 32:419-425.
27. Allen A.M. Inhibition of the hypothalamic paraventricular nucleus in spontaneously hypertensive rats dramatically reduces sympathetic vasomotor tone. Hypertension 2002, 39:275-280.
28. Pyner S., Coote J.H. Identification of branching paraventricular neurons of the hypothalamus that project to the rostroventrolateral medulla and spinal cord. Neuroscience 2000, 100:549-556.
29. Hardy S.G. Hypothalamic projections to cardiovascular centers of the medulla. Brain Res 2001, 894:233-240.
30. Ranson R.N., Motawei K., Pyner S., Coote J.H. The paraventricular nucleus of the hypothalamus sends efferents to the spinal cord of the rat that closely appose sympathetic preganglionic neurones projecting to the stellate ganglion. Exp Brain Res 1998, 120:164-172.
31. Yamashita H., Inenaga K., Koizumi K. Possible projections from regions of paraventricular and supraoptic nuclei to the spinal cord: electrophysiological studies. Brain Res 1984, 296:373-378.
32. Li D.P., Pan H.L. Angiotensin II attenuates synaptic GABA release and excites paraventricular-rostral ventrolateral medulla output neurons. J Pharmacol Exp Ther 2005, 313:1035-1045.
33. Li D.P., Chen S.R., Pan H.L. Adenosine inhibits paraventricular pre-sympathetic neurons through ATP-dependent potassium channels. J Neurochem 2010, 113:530-542.
34. Li D.P., Yang Q., Pan H.M., Pan H.L. Plasticity of pre- and postsynaptic GABAB receptor function in the paraventricular nucleus in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 2008, 295:H807-H815.
35. Yang Y., Chen M., Lai Y., Gantz I., Georgeson K.E., Harmon C.M. Molecular determinants of human melanocortin-4 receptor responsible for antagonist SHU9119 selective activity. J Biol Chem 2002, 277:20328-20335.
36. Wan S., Browning K.N., Coleman F.H., Sutton G., Zheng H., Butler A., Berthoud H.R., Travagli R.A. Presynaptic melanocortin-4 receptors on vagal afferent fibers modulate the excitability of rat nucleus tractus solitarius neurons. J Neurosci 2008, 28:4957-4966.
37. Schioth H.B., Muceniece R., Mutulis F., Bouifrouri A.A., Mutule I., Wikberg J.E. Further pharmacological characterization of the selective melanocortin 4 receptor antagonist HS014: comparison with SHU9119. Neuropeptides 1999, 33:191-196.
38. Ross E.M. Signal sorting and amplification through G protein-coupled receptors. Neuron 1989, 3:141-152.
39. Haynes W.G., Morgan D.A., Djalali A., Sivitz W.I., Mark A.L. Interactions between the melanocortin system and leptin in control of sympathetic nerve traffic. Hypertension 1999, 33:542-547.
40. Tallam L.S., da Silva A.A., Hall J.E. Melanocortin-4 receptor mediates chronic cardiovascular and metabolic actions of leptin. Hypertension 2006, 48:58-64.
41. 2+-activated K+channels. J Physiol 2009, 587:4235-4247.
42. Hwa J.J., Ghibaudi L., Gao J., Parker E.M. Central melanocortin system modulates energy intake and expenditure of obese and lean Zucker rats. Am J Physiol Regul Integr Comp Physiol 2001, 281:R444-R451.
43. Hakansson M.L., Brown H., Ghilardi N., Skoda R.C., Meister B. Leptin receptor immunoreactivity in chemically defined target neurons of the hypothalamus. J Neurosci 1998, 18:559-572.
44. 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 2001, 411:480-484.
45. Mizuno T.M., Kleopoulos S.P., Bergen H.T., Roberts J.L., Priest C.A., Mobbs C.V. Hypothalamic pro-opiomelanocortin mRNA is reduced by fasting and [corrected] in ob/ob and db/db mice, but is stimulated by leptin. Diabetes 1998, 47:294-297.
46. Kim E.M., O'Hare E., Grace M.K., Welch C.C., Billington C.J., Levine A.S. ARC POMC mRNA and PVN alpha-MSH are lower in obese relative to lean zucker rats. Brain Res 2000, 862:11-16.
47. Ollmann M.M., Wilson B.D., Yang Y.K., Kerns J.A., Chen Y., Gantz I., Barsh G.S. Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science 1997, 278:135-138.
48. Gyte A., Pritchard L.E., Jones H.B., Brennand J.C., White A. Reduced expression of the KATP channel subunit, Kir6.2, is associated with decreased expression of neuropeptide Y and agouti-related protein in the hypothalami of Zucker diabetic fatty rats. J Neuroendocrinol 2007, 19:941-951.
49. Korner J., Wardlaw S.L., Liu S.M., Conwell I.M., Leibel R.L., Chua S.C. Effects of leptin receptor mutation on Agrp gene expression in fed and fasted lean and obese (LA/N-faf) rats. Endocrinology 2000, 141:2465-2471.
50. Wilson B.D., Bagnol D., Kaelin C.B., Ollmann M.M., Gantz I., Watson S.J., Barsh G.S. Physiological and anatomical circuitry between Agouti-related protein and leptin signaling. Endocrinology 1999, 140:2387-2397.
51. Fu L.Y., van den Pol A.N. Agouti-related peptide and MC3/4 receptor agonists both inhibit excitatory hypothalamic ventromedial nucleus neurons. J Neurosci 2008, 28:5433-5449.
52. 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 1999, 24:155-163.
53. Gilman A.G. G proteins: transducers of receptor-generated signals. Annu Rev Biochem 1987, 56:615-649.
54. Gantz I., Miwa H., Konda Y., Shimoto Y., Tashiro T., Watson S.J., DelValle J., Yamada T. Molecular cloning, expression, and gene localization of a fourth melanocortin receptor. J Biol Chem 1993, 268:15174-15179.
55. Czyzyk T.A., Sikorski M.A., Yang L., McKnight G.S. Disruption of the RIIbeta subunit of PKA reverses the obesity syndrome of Agouti lethal yellow mice. Proc Natl Acad Sci USA 2008, 105:276-281.
56. Buch T.R., Heling D., Damm E., Gudermann T., Breit A. Pertussis toxin-sensitive signaling of melanocortin-4 receptors in hypothalamic GT1-7 cells defines agouti-related protein as a biased agonist. J Biol Chem 2009, 284:26411-26420.