Leptin signaling in the nucleus of the solitary tract alters the cardiovascular responses to activation of the chemoreceptor reflex

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 303, Issue 7, 2012, Pages

  Ciriello, John ^a   Moreau, Jason M ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

Baroreceptor reflex; Chemoreceptor reflex; Chronic intermittent hypoxia; Leptin receptor; Nucleus of the solitary tract; Sympathetic nervous activity; Vagal bradycardia

Indexed keywords

GLUTAMIC ACID; LEPTIN; LEPTIN RECEPTOR;

ADRENERGIC SYSTEM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL PRESSURE; ARTICLE; BRADYCARDIA; CARDIOVASCULAR RESPONSE; CHEMORECEPTOR; CHEMORECEPTOR REFLEX; CHRONIC INTERMITTENT HYPOXIA; CONCENTRATION RESPONSE; CONTROLLED STUDY; HEART RATE; HISTOLOGY; MALE; MICROINJECTION; NONHUMAN; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SOLITARY TRACT NUCLEUS; ANIMAL; BLOOD PRESSURE; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECT; GENETICS; METABOLISM; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY; WISTAR RAT; ZUCKER RAT;

ANIMALS; BAROREFLEX; BLOOD PRESSURE; CHEMORECEPTOR CELLS; DISEASE MODELS, ANIMAL; GLUTAMIC ACID; HEART RATE; LEPTIN; MALE; MICROINJECTIONS; OBESITY; RATS; RATS, WISTAR; RATS, ZUCKER; RECEPTORS, LEPTIN; SIGNAL TRANSDUCTION; SOLITARY NUCLEUS;

EID: 84867281917     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00068.2012     Document Type: Article

References (77)

1. Arnold AC, Shaltout HA, Gallagher PE, Diz DI. Leptin impairs cardiovagal baroreflex function at the level of the solitary tract nucleus. Hypertension 54: 1001-1008, 2009.
2. Baguet JP, Barone-Rochette G, Pépin JL. Hypertension and obstructive sleep apnoea syndrome: current perspectives. J Hum Hypertens 23: 431-43, 2009.
3. Baguet JP, Lévy P, Barone-Rochette G, Tamisier R, Pierre H, Peeters M, Mallion JM, Pépin JL. Masked hypertension in obstructive sleep apnea syndrome. J Hypertens 26: 885-892, 2008.
4. Banks WA. Leptin transport across the blood-brain barrier: implications for cause and treatment of obesity. Curr Pharm Des 7: 125-133, 2001.
5. Banks WA, Kastin AJ, Huang W, Jaspan JB, Maness LM. Leptin enters the brain by a saturable system independent of insulin. Peptides 17: 305-311, 1996.
6. Bradley TD, Floras JS. Obstructive sleep apnoea and its cardiovascular consequences. Lancet 373: 82-93, 2009.
7. Brooks D, Horner, RL, Kozar, LF, Render-Teixeira CL, Phillipson, EA. Obstructive sleep apnea as a cause of systemic hypertension evidence from a canine model. J Clin Invest 99: 106-109, 1997.
8. Burdyga G, Spiller D, Morris R, Lal S, Thompson DG, Saeed S, Dimaline R, Varro A, Dockray GJ. Expression of the leptin receptor in rat and human nodose ganglion neurones. Neuroscience 109: 339-347, 2002.
9. Buyse M, Ovesjö ML, Goïot H, Guilmeau S, Péranzi G, Moizo L, Walker F, Lewin MJ, Meister B, Bado A. Expression and regulation of leptin receptor proteins in afferent and efferent neurons of the vagus nerve. Eur J Neurosci 14: 64-72, 2001.
10. Calapai G, Corica F, Allegra A, Corsonello A, Sautebin L, De Gregorio T, Di Rosa M, Costantino G, Buemi M, Caputi AP. Effects of intracerebroventricular leptin administration on food intake, body weight gain and diencephalic nitric oxide synthase activity in the mouse. Br J Pharmacol 125: 798-802, 1998.
11. Calaresu FR, Knuepfer MM, Ciriello J, Stella A. An anomalous vagorenal reflex pathway in the cat. Exp Neurol 87: 278-290, 1985.
12. Chitravanshi VC, Sapru HN. Chemoreceptor-sensitive neurons in commissural subnucleus of nucleus tractus solitarius of the rat. Am J Physiol Regul Integr Comp Physiol 268: R851-R858, 1995.
13. Chitravanshi VC, Kachroo A, Sapru HN. A midline area in the nucleus commissuralis of NTS mediates the phrenic nerve responses to carotid chemoreceptor stimulation. Brain Res 662: 127-133, 1994.
14. Ciriello J. Brainstem projections of aortic baroreceptor afferent fibers in the rat. Neurosci Lett 36: 37-42, 1983.
15. Ciriello J. Effect of leptin in the nucleus of the solitary tract on the baroreceptor reflex. Program No. 453.15/Z5, 2006. Abstract Viewer and Itinerary Planner. Atlanta, GA: Society for Neuroscience, 2006.
16. Ciriello J, Calaresu FR. Central projections of afferent renal fibers in the rat: an anterograde transport study of horseradish peroxidase. J Auton Nerv Syst 8: 273-285, 1983.
17. Ciriello J, Caverson MM, Polosa C. Function of the ventrolateral medulla in the control of the circulation. Brain Res 396: 359-391, 1986.
18. Ciriello J, Solano-Flores LP, Rosas-Arellano MP, Kirouac GJ, Babic T. Medullary pathways mediating the parasubthalamic nucleus depressor response. Am J Physiol Regul Integr Comp Physiol 294: R1276-R1284, 2008.
19. Colombari E, Menani JV, Talman WT. Commissural NTS contributes to pressor responses to glutamate injected into the medial NTS of awake rats. Am J Physiol Regul Integr Comp Physiol 270: R1220-R1225, 1996.
20. Correia ML, Morgan DA, Sivitz WI, Mark AL, Haynes WG. Leptin acts in the central nervous system to produce dose-dependent changes in arterial pressure. Hypertension 37: 936-942, 2001.
21. Cruz JdeC, Bonagamba LG, Stern JE, Machado BH. Fos expression in the NTS in response to peripheral chemoreflex activation in awake rats. Auton Neurosci 152: 27-34, 2010.
22. Cruz JdeC, Bonagamba LG, Machado BH, Biancard VC, Stern JE. Intermittent activation of peripheral chemoreceptors in awake rats induces Fos expression in rostral ventrolateral medulla-projecting neurons in the paraventricular nucleus of the hypothalamus. Neuroscience 157: 463-472, 2008.s
23. Cruz JC, Machado BH. GABA and nitric oxide in the PVN are involved in arterial pressure control but not in the chemoreflex responses in rats. Auton Neurosci 146: 47-55, 2009.
24. Dampney RA. Functional organization of central pathways regulating the cardiovascular system. Physiol Rev 74: 323-364, 1994.
25. Dempsey JA, Veasey SC, Morgan BJ, O'Donell CP. Pathophysiology of sleep apnea. Physiol Rev 90: 47-112, 2010.
26. Dunbar JC, Hu Y, Lu H. Intracerebroventricular leptin increases lumbar and renal sympathetic nerve activity and blood pressure in normal rats. Diabetes 46: 2040-2043, 1997.
27. Elias CF, Kelly JF, Lee CE, Ahima RS, Drucker DJ, Saper CB, Elmquist JK. Chemical characterization of leptin-activated neurons in the rat brain. J Comp Neurol 423: 261-281, 2000.
28. Ellacott KL, Halatchev IG, Cone RD. Characterization of leptin-responsive neurons in the caudal brainstem. Endocrinology 147: 3190-3195, 2006.
29. Elmquist JK, Bjørbaek C, Ahima RS, Flier JS, Saper CB. Distributions of leptin receptor mRNA isoforms in the rat brain. J Comp Neurol 395: 535-547, 1998.
30. Elmquist JK, Ahima RS, Maratos-Flier E, Flier JS, Saper CB. Leptin activates neurons in ventrobasal hypothalamus and brainstem. Endocrinology 138: 839-842, 1997.
31. Erickson JT, Millhorn DE. Fos-like protein is induced in neurons of the medulla oblongata after stimulation of the carotid sinus nerve in awake and anesthetized rats. Brain Res 567: 11-24, 1991.
32. Faouzi M, Leshan R, Björnholm M, Hennessey T, Jones J, Münzberg H. Differential accessibility of circulating leptin to individual hypothalamic sites. Endocrinology 148: 5414-5423, 2007.
33. Finley JC, Katz DM. The central organization of carotid body afferent projections to the brainstem of the rat. Brain Res 572: 108-116, 1992.
34. Fox EA, Powley TL. False-positive artifacts of tracer strategies distort autonomic connectivity maps. Brain Res Brain Res Rev 14: 53-77, 1989.
35. Gao L, Pan YX, Wang WZ, Li YL, Schultz HD, Zucker IH, Wang W. Cardiac sympathetic afferent stimulation augments the arterial chemoreceptor reflex in anesthetized rats. J Appl Physiol 102: 37-43, 2007.
36. Grill HJ. Leptin and the systems neuroscience of meal size control. Front Neuroendocrinol 31: 61-78, 2010.
37. Grill HJ, Schwartz MW, Kaplan JM, Foxhall JS, Breininger J, Baskin DG. Evidence that the caudal brainstem is a target for the inhibitory effect of leptin on food intake. Endocrinology 143: 239-246, 2002.
38. Hall JE, Hildebrandt DA, Kuo J. Obesity hypertension: role of leptin and sympathetic nervous system. Am J Hypertens 14: 103S-115S, 2001.
39. Harsch IA, Konturek PC, Koebnick C, Kuehnlein PP, Fuchs FS, Pour Schahin S, Wiest GH, Hahn EG, Lohmann T, Ficker JH. Leptin and ghrelin levels in patients with obstructive sleep apnoea: effect of CPAP treatment. Eur Respir J 22: 251-257, 2003.
40. Haynes WG, Morgan DA, Walsh SA, Mark AL, Sivitz WI. Receptor-mediated regional sympathetic nerve activation by leptin. J Clin Invest 100: 270-278, 1997.
41. Hisadome K, Reimann F, Gribble FM, Trapp S. Leptin directly depolarizes preproglucagon neurons in the nucleus tractus solitarius: electrical properties of glucagon-like peptide 1 neurons. Diabetes 59: 1890-1898, 2010.
42. Hosoi T, Kawagishi T, Okuma Y, Tanaka J, Nomura Y. Brain stem is a direct target for leptin's action in the central nervous system. Endocrinology 143: 3498-3504, 2002.
43. Inyushkin AN, Inyushkina EM, Merkulova NA. Respiratory responses to microinjections of leptin into the solitary tract nucleus. Neurosci Behav Physiol 39: 231-240, 2009.
44. Inyushkina EM, Merkulova NA, Inyushkin AN. Mechanisms of the respiratory activity of leptin at the level of the solitary tract nucleus. Neurosci Behav Physiol 40: 707-713, 2010.
45. Kirouac GJ, Ciriello J. Cardiovascular depressor responses to stimulation of substantia nigra and ventral tegmental area. Am J Physiol Heart Circ Physiol 273: H2549-H2557, 1997.
46. Larkin EK, Elston RC, Patel SR, Tishler PV, Palmer LJ, Jenny NS, Redline S. Linkage of serum leptin levels in families with sleep apnea. Int J Obes 29: 260-267, 2005.
47. Lemus M, Montero S, Luquín S, García J, De Alvarez-Buylla ER. Nitric oxide in the solitary tract nucleus (STn) modulates glucose homeostasis and FOS-ir expression after carotid chemoreceptor stimulation. Adv Exp Med Biol 648: 403-410, 2009.
48. Leong SK, Ling EA. Labelling neurons with fluorescent dyes administered via intravenous, subcutaneous or intraperitoneal route. J Neurosci Methods 32: 15-23, 1990.
49. Logan AG, Bradley TD. Sleep apnea and cardiovascular disease. Curr Hypertens Rep 12: 182-188, 2010.
50. Madden CJ, Morrison SF. Hypoxic activation of arterial chemoreceptors inhibits sympathetic outflow to brown adipose tissue in rats. J Physiol 566: 559-573, 2005.
51. Mark AL, Agassandian K, Morgan DA, Liu X, Cassell MD, Rahmouni K. Leptin signaling in the nucleus tractus solitarii increases sympathetic nerve activity to the kidney. Hypertension 53: 375-380, 2009.
52. Marsh AJ, Fontes MA, Killinger S, Pawlak DB, Polson JW, Dampney RA. Cardiovascular responses evoked by leptin acting on neurons in the ventromedial and dorsomedial hypothalamus. Hypertension 42: 488-493, 2003.
53. Mercer JG, Moar KM, Hoggard N. Localization of leptin receptor (Ob-R) messenger ribonucleic acid in the rodent hindbrain. Endocrinology 139: 29, 1998.
54. Messenger SA, Moreau J, Ciriello J. Intermittent hypoxia and systemic leptin administration induces pSTAT3 and Fos/Fra-1 in the carotid body. Brain Res 1446: 56-70, 2012.
55. Mifflin SW. Arterial chemoreceptor input to nucleus tractus solitarius. Am J Physiol Regul Integr Comp Physiol 263: R368-R375, 1992.
56. Morgan DA, Thedens DR, Weiss R, Rahmouni K. Mechanisms mediating renal sympathetic activation to leptin in obesity. Am J Physiol Regul Integr Comp Physiol 295: R1730-R1736, 2008.
57. Munzberg H. Differential leptin access into the brain-A hierarchial organization of hypothalamic leptin target sites? Physiol Behav 94: 664-669, 2008.
58. Muzzin P, Cusin I, Charnay Y, Rohner-Jeanrenaud F. Single intracerebroventricular bolus injection of a recombinant adenovirus expressing leptin results in reduction of food intake and body weight in both lean and obese Zucker fa/fa rats. Regul Pept 92: 57-64, 2000.
59. Narkiewicz K, Wolf J, Lopez-Jimenez F, Somers VK. Obstructive sleep apnea and hypertension. Curr Cardiol Rep 7: 435-440, 2005.
60. Patel SR, Palmer LJ, Larkin EK, Jenny NS, White DP, Redline S. Relationship between obstructive sleep apnea and diurnal leptin rhythms. Sleep 27: 235-239, 2004.
61. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates, 2nd ed., New York: Academic, 1986.
62. Peiser C, Springer J, Groneberg DA, McGregor GP, Fischer A, Lang RE. Leptin receptor expression in nodose ganglion cells projecting to the rat gastric fundus. Neurosci Lett 320: 41-44, 2002.
63. Rahmouni K, Morgan DA. Hypothalamic arcuate nucleus mediates the sympathetic and arterial pressure responses to leptin. Hypertension 49: 647-652, 2007.
64. Schäfer H, Pauleit D, Sudhop T, Gouni-Berthold I, Ewig S, Berthold HK. Body fat distribution, serum leptin, and cardiovascular risk factors in men with obstructive sleep apnea. Chest 122: 829-839, 2002.
65. Sachot C, Rummel C, Bristow AF, Luheshi GN. The role of the vagus nerve in mediating the long-term anorectic effects of leptin. J Neuroendocrinol 19: 250-261, 2007.
66. Sapru HN. Carotid chemoreflex. Neural pathways and transmitters. Adv Exp Med Biol 410: 357-364, 1996.
67. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature 404: 661-671, 2000.
68. Shioda S, Funahashi H, Nakajo S, Yada T, Maruta O, Nakai Y. Immunohistochemical localization of leptin receptor in the rat brain. Neurosci Lett 243: 41-44, 1998.
69. Shirasaka T, Takasaki M, Kannan H. Cardiovascular effects of leptin and orexins. Am J Physiol Regul Integr Comp Physiol 284: R639-R651, 2003.
70. Solano-Flores LP, Rosas-Arellano MP, Ciriello J. Fos induction in central structures after afferent renal nerve stimulation. Brain Res 753: 102-119, 1997.
71. Spyer KM. Central nervous integration of cardiovascular control. J Exp Biol 100: 109-128, 1982.
72. Spyer KM, Gourine AV. Chemosensory pathways in the brainstem controlling cardiorespiratory activity. Philos Trans R Soc Lond B Biol Sci 364: 2603-2610, 2009.
73. Tang-Christensen M, Havel PJ, Jacobs RR, Larsen PJ, Cameron JL. Central administration of leptin inhibits food intake and activates the sympathetic nervous system in rhesus macaques. J Clin Endocrinol Metab 84: 711-717, 1999.
74. Vardhan A, Kachroo A, Sapru HN. Excitatory amino acid receptors in commissural nucleus of the NTS mediate carotid chemoreceptor responses. Am J Physiol Regul Integr Comp Physiol 264: R41-R50, 1993.
75. White DP. Sleep apnea. Proc Am Thoracic Soc 3: 124-128, 2006.
76. Yuan CS, Dey L, Xie JT, Aung HH. Gastric effects of galanin and its interaction with leptin on brainstem neuronal activity. J Pharmacol Exp Ther 301: 488-493, 2002.
77. Yuan CS, Dey L, Xie JT. Gastric effects of cholecystokinin and its interaction with leptin on brainstem neuronal activity in neonatal rats. J Pharmacol Exp Ther 295: 177-182, 2000.