Intrathecal melanin-concentrating hormone reduces sympathetic tone and blocks cardiovascular reflexes

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 303, Issue 6, 2012, Pages

  Egwuenu, Eyitemi J ^a   Fong, Angelina Y ^a   Pilowsky, Paul M ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

Blood pressure; Cardiovascular physiology; Melaninconcentrating hormone; Neuropeptide; Neurophysiology

Indexed keywords

MELANIN CONCENTRATING HORMONE; ADRENERGIC RECEPTOR BLOCKING AGENT; HYPOPHYSIS HORMONE; HYPOTHALAMUS HORMONE; MELANIN; MELANIN-CONCENTRATING HORMONE; SODIUM CHLORIDE; URETHAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; AUTONOMIC NERVOUS SYSTEM; CARDIOVASCULAR REFLEX; CONTROLLED STUDY; HEART RATE; HYPERCAPNIA; MALE; MEAN ARTERIAL PRESSURE; NONHUMAN; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; RAT; SPINAL CORD; SPRAGUE DAWLEY RAT; SYMPATHETIC REFLEX; SYMPATHETIC TONE; VAGOTOMY; ADRENERGIC SYSTEM; ANIMAL; CARDIOVASCULAR FUNCTION; DRUG EFFECT; INTRASPINAL DRUG ADMINISTRATION; PHYSIOLOGY; REFLEX; RESPIRATORY FUNCTION; BAROSYMPATHETIC REFLEX; BRADYCARDIA; CHEMOSYMPATHETIC REFLEX; HYPOTENSION; SOMATOSYMPATHETIC REFLEX; SYMPATHETIC NERVE;

ANIMALS; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; HYPOTHALAMIC HORMONES; INJECTIONS, SPINAL; MALE; MELANINS; PITUITARY HORMONES; RATS; RATS, SPRAGUE-DAWLEY; REFLEX; RESPIRATORY PHYSIOLOGICAL PHENOMENA; SYMPATHETIC NERVOUS SYSTEM; SYMPATHOLYTICS;

EID: 84866387915     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00215.2012     Document Type: Article

References (52)

1. Allen GV, Cechetto DF. Functional and anatomical organization of cardiovascular pressor and depressor sites in the lateral hypothalamic area. I. Descending projections. J Comp Neurol 315: 313-32, 1992.
2. Alexander S, Harmar A, McGrath I. Guide to receptors and channels. Br J Pharmacol 164: 1749-1750, 2011.
3. Astrand A, Bohlooly YM, Larsdotter S, Mahlapuu M, Andersen H, Tornell J, Ohlsson C, Snaith M, Morgan DG. Mice lacking melaninconcentrating hormone receptor 1 demonstrate increased heart rate associated with altered autonomic activity. Am J Physiol Regul Integr Comp Physiol 287: R749-R758, 2004.
4. Bachner D, Kreienkamp H, Weise C, Buck F, Richter D. Identification of melanin concentrating hormone (MCH) as the natural ligand for the orphan somatostatin-like receptor 1 (SLC-1). FEBS Lett 457: 522-524, 1999.
5. Berthoud H, Neuhuber WL. Functional and chemical anatomy of the afferent vagal system. Autonom Neurosci 85: 1-17, 2000.
6. Bittencourt JC, Elias CF. Melanin-concentrating hormone and neuropeptide EI projections from the lateral hypothalamic area and zona incerta to the medial septal nucleus and spinal cord: a study using multiple neuronal tracers. Brain Res 805: 1-19, 1998.
7. Bittencourt JC, Presse F, Arias C, Peto C, Vaughan J, Nahon JL, Vale W, Sawchenko PE. The melanin-concentrating hormone system of the rat brain: an immuno-and hybridization histochemical characterization. J Comp Neurol 319: 218-245, 1992.
8. Borowsky B, Durkin MM, Ogozalek K, Marzabadi MR, DeLeon J, Heurich R, Lichtblau H, Shaposhnik Z, Daniewska I, Blackburn TP, Branchek TA, Gerald C, Vaysse PJ, Forray C. Antidepressant, anxiolytic and anorectic effects of a melanin-concentrating hormone-1 receptor antagonist. Nat Med 8: 825-830, 2002.
9. Brown SN, Chitravanshi VC, Kawabe K, Sapru HN. Microinjections of melanin concentrating hormone into the nucleus tractus solitarius of the rat elicit depressor and bradycardic responses. Neuroscience 150: 796-806, 2007.
10. Burdyga G, Varro A, Dimaline R, Thompson DG, Dockray GJ. Feedingdependent depression of melanin-concentrating hormone receptor-1 expression in vagal afferent neurons. Neuroscience 137: 1405-1415, 2006.
11. Burke PG, Abbott SB, McMullan S, Goodchild AK, Pilowsky PM. Somatostatin selectively ablates post-inspiratory activity after injection into the Botzinger complex. Neuroscience 167: 528-539, 2010.
12. Chambers J, Ames RS, Bergsma D, Muir A, Fitzgerald LR, Hervieu G, Dytko GM, Foley JJ, Martin J, Liu WS, Park J, Ellis C, Ganguly S, Konchar S, Cluderay J, Leslie R, Wilson S, Sarau HM. Melaninconcentrating hormone is the cognate ligand for the orphan G-proteincoupled receptor SLC-1. Nature 400: 261-265, 1999.
13. Farnham MM, Li Q, Goodchild AK, Pilowsky PM. PACAP is expressed in sympathoexcitatory bulbospinal C1 neurons of the brain stem and increases sympathetic nerve activity in vivo. Am J Physiol Regul Integr Comp Physiol 294: R1304-R1311, 2008.
14. Farnham MM, Pilowsky PM. The role of PACAP in central cardiorespiratory regulation. Respir Physiol Neurobiol 174: 65-75, 2010.
15. Gaede AH, Lung MS, Pilowsky PM. Catestatin attenuates the effects of intrathecal nicotine and isoproterenol. Brain Res 1305: 85-95, 2009.
16. Gao XB, van den Pol AN. Melanin concentrating hormone depresses synaptic activity of glutamate and GABA neurons from rat lateral hypothalamus. J Physiol 533: 237-52, 2001.
17. Hill J, Duckworth M, Murdock P, Rennie G, Sabido-David C, Ames RS, Szekeres P, Wilson S, Bergsma DJ, Gloger IS, Levy DS, Chambers JK, Muir AI. Molecular cloning and functional characterization of MCH2, a novel human MCH receptor. J Biol Chem 276: 20125-20129, 2001.
18. Kennedy AR, Todd JF, Dhillo WS, Seal LJ, Ghatei MA, O'Toole CP, Jones M, Witty D, Winborne K, Riley G, Hervieu G, Wilson S, Bloom SR. Effect of direct injection of melanin-concentrating hormone into the paraventricular nucleus: further evidence for a stimulatory role in the adrenal axis via SLC-1. J Neuroendocrinol 15: 268-272, 2003.
19. Kerman IA, Bernard R, Rosenthal D, Beals J, Akil H, Watson SJ. Distinct populations of presympathetic-premotor neurons express orexin or melanin-concentrating hormone in the rat lateral hypothalamus. J Comp Neurol 505: 586-601, 2007.
20. Kolakowski LF, Jung BP, Nguyen T, Johnson MP, Lynch KR, Cheng R, Heng HHQ, George SR, O'Dowd BF. Characterization of a human gene related to genes encoding somatostatin receptors. FEBS Lett 398: 253-258, 1996.
21. Lakaye B, Minet A, Zorzi W, Grisar T. Cloning of the rat brain cDNA encoding for the SLC-1 G protein-coupled receptor reveals the presence of an intron in the gene. Biophys Acta Mol Res 1401: 216-220, 1998.
22. Lembo PM, Grazzini E, Cao J, Hubatsch DA, Pelletier M, Hoffert C, St-Onge S, Pou C, Labrecque J, Groblewski T, O'Donnell D, Payza K, Ahmad S, Walker P. The receptor for the orexigenic peptide melaninconcentrating hormone is a G protein-coupled receptor. Nat Cell Biol 1: 267-271, 1999.
23. Ludwig DS, Tritos NA, Mastaitis JW, Kulkarni R, Kokkotou E, Elmquist J, Lowell B, Flier JS, Maratos-Flier E. Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J Clin Invest 107: 379-386, 2001.
24. Luong LN, Carrive P. Orexin microinjection in the medullary raphe increases heart rate and arterial pressure but does not reduce tail skin blood flow in the awake rat. Neuroscience 202: 209-17, 2012.
25. Makeham JM, Goodchild AK, Pilowsky PM. NK1 receptor activation in rat rostral ventrolateral medulla selectively attenuates somato-sympathetic reflex while antagonism attenuates sympathetic chemoreflex. Am J Physiol Regul Integr Comp Physiol 288: R1707-R1715, 2005.
26. Messina MM, Overton JM. Cardiovascular effects of melanin-concentrating hormone. Regul Pept 139: 23-30, 2007.
27. Miyawaki T, Goodchild AK, Pilowsky PM. Activation of mu-opioid receptors in rat ventrolateral medulla selectively blocks baroreceptor reflexes while activation of delta opioid receptors blocks somato-sympathetic reflexes. Neuroscience 109: 133-144, 2002.
28. Miyawaki T, Goodchild AK, Pilowsky PM. Maintenance of sympathetic tone by a nickel chloride-sensitive mechanism in the rostral ventrolateral medulla of the adult rat. Neuroscience 116: 455-464, 2003.
29. Miyawaki T, Goodchild AK, Pilowsky PM. Rostral ventral medulla 5-HT1A receptors selectively inhibit the somatosympathetic reflex. Am J Physiol Regul Integr Comp Physiol 280: R1261-R1268, 2001.
30. Miyawaki T, Suzuki S, Minson J, Arnolda L, Chalmers J, Llewellyn-Smith I, Pilowsky P. Role of AMPA/kainate receptors in transmission of the sympathetic baroreflex in rat CVLM. Am J Physiol Regul Integr Comp Physiol 272: R800-R812, 1997.
31. Molander C, Grant G. Laminar distribution of and somatotopic organization of primary afferent fibers from hindlimb nerves in the dorsal horn. A study by transganglionic transport of horseradish peroxidise in the rat. Neuroscience 19: 297-312, 1986.
32. Oldfield BJ, McLachlan EM. An analysis of the sympathetic preganglionic neurons projecting from the upper thoracic spinal roots of the cat. J Comp Neurol 196: 329-345, 1981.
33. Pajolla GP, de Aguiar Correa FM. Cardiovascular responses to the injection of L-glutamate in the lateral hypothalamus of unanesthetized or anesthetized rats. Auton Neurosci 116: 19-29, 2004.
34. Pereira-da-Silva M, Torsoni MA, Nourani HV, Augusto VD, Souza CT, Gasparetti AL, Carvalheira JB, Ventrucci G, Marcondes MC, Cruz-Neto AP, Saad MJ, Boschero AC, Carneiro EM, and Velloso LA. Hypothalamic melanin-concentrating hormone is induced by cold exposure and participates in the control of energy expenditure in rats. Endocrinology 144: 4831-4840, 2003.
35. Pilowsky PM, Goodchild AK. Baroreceptor reflex pathways and neurotransmitters: 10 years on. J Hypertens 20: 1675-1688, 2002.
36. Pilowsky PM, Lung MS, Spirovski D, McMullan S. Differential regulation of the central neural cardiorespiratory system by metabotropic neurotransmitters. Philos Trans R Soc Lond B Biol Sci 364: 2537-2552, 2009.
37. Pissios P, Bradley RL, Maratos-Flier E. Expanding the scales: The multiple roles of MCH in regulating energy balance and other biological functions. Endocr Rev 27: 606-620, 2006.
38. Rossi M, Choi SJ, O'Shea D, Miyoshi T, Ghatei MA, Bloom SR. Melanin-concentrating hormone acutely stimulates feeding, but chronic administration has no effect on body weight. Endocrinology 138: 351-355, 1997.
39. Sailer AW, Sano H, Zeng Z, McDonald TP, Pan J, Pong SS, Feighner SD, Tan CP, Fukami T, Iwaasa H, Hreniuk DL, Morin NR, Sadowski SJ, Ito M, Bansal A, Ky B, Figueroa DJ, Jiang Q, Austin CP, MacNeil DJ, Ishihara A, Ihara M, Kanatani A, Van der Ploeg LH, Howard AD, Liu Q. Identification and characterization of a second melanin-concentrating hormone receptor, MCH-2R. Proc Natl Acad Sci USA 98: 7564-7569, 2001.
40. Saito Y, Nothacker HP, Wang Z, Lin SH, Leslie F, Civelli O. Molecular characterization of the melanin-concentrating-hormone receptor. Nature 400: 265-269, 1999.
41. Sato A, Schmidt RF, Somatosympathetic reflex: afferent fibers central pathways, discharge characteristics. Physiol Rev 53: 916-947, 1973.
42. Shahid IZ, Rahman AA, Pilowsky PM. Intrathecal orexin A increases sympathetic outflow and respiratory drive, enhances baroreflex sensitivity and blocks the somato-sympathetic reflex. Br J Pharmacol 162: 961-973, 2010.
43. Shimada M, Tritos NA, Lowell BB, Flier JS, Maratos-Flier E. Mice lacking melanin-concentrating hormone are hypophagic and lean. Nature 396: 670-674, 1998.
44. Shimomura Y, Mori M, Sugo T, Ishibashi Y, Abe M, Kurokawa T, Onda H, Nishimura O, Sumino Y, Fujino M. Isolation and identification of melanin-concentrating hormone as the endogenous ligand of the SLC-1 receptor. Biochem Biophys Res Commun 261: 622-626, 1999.
45. Skofitsch G, Jacobowitz DM, Zamir N. Immunohistochemical localization of a melanin concentrating hormone-like peptide in the rat brain. Brain Res Bull 15: 635-649, 1985.
46. Spirovski D, Li Q, Pilowsky PM. Brainstem galanin-synthesizing neurons are differentially activated by chemoreceptor stimuli and represent a subpopulation of respiratory neurons. J Comp Neurol 520: 154-173, 2011.
47. Stornetta RL, Morrison SF, Ruggiero DA, Reis DJ. Neurons of rostral ventrolateral medulla mediate somatic pressor reflex. Am J Physiol Regul Integr Comp Physiol 256: R448-R462, 1989.
48. Strack AM, Sawyer WB, Marubio LM, Loewy AD. Spinal origin of sympathetic preganglionic neurons in rat. Brain Res 455: 187-191.
49. Tan CP, Sano H, Iwaasa H, Pan J, Sailer AW, Hreniuk DL, Feighner SD, Palyha OC, Pong SS, Figueroa DJ, Austin CP, Jiang MM, Yu H, Ito J, Ito M, Guan XM, MacNeil DJ, Kanatani A, Van der Ploeg LH, Howard AD. Melanin-concentrating hormone receptor subtypes 1 and 2: species-specific gene expression. Genomics 79: 785-792, 2002.
50. Wang L, Spary E, Deuchars J, Deuchars SA. Tonic GABAergic inhibition of sympathetic preganglionic neurons: a novel substrate for sympathetic control. J Neurosci 28: 12445-12452, 2008.
51. Zogovic B, Pilowsky PM. Intrathecal bombesin is sympathoexcitatory and pressor in rat. Am J Physiol Regul Integr Comp Physiol 301: R1486-R1494, 2011.
52. Zogovic B, Pilowsky PM. Intrathecal neurotensin is hypotensive, sympathoinhibitory and enhances the baroreflex in anaesthetized rat. Br J Pharmacol 166: 378-89, 2012.