Sympathoinhibitory mechanism of moxonidine: Role of the inducible nitric oxide synthase in the rostral ventrolateral medulla

Cardiovascular Research

Volumn 84, Issue 2, 2009, Pages 283-291

  Peng, Jie ^a,b   Wang, Yang Kai ^a   Wang, Li Gang ^a   Yuan, Wen Jun ^a,c   Su, Ding Feng ^a   Ni, Xin ^a   Deng, Xiao Ming ^b   Wang, Wei Zhong ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c NINGXIA MEDICAL UNIVERSITY   (China)

Author keywords

Blood pressure; Centrally acting drug; Imidazoline receptor; Microinjection; Nitric oxide

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; MOXONIDINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; S METHYLPSEUDOTHIOUREA; UNCLASSIFIED DRUG;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MEASUREMENT; BRAIN; CARDIOVASCULAR RESPONSE; DRUG INHIBITION; HEART RATE; IMMUNOHISTOCHEMISTRY; MALE; MEDULLA OBLONGATA; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ROSTRAL VENTROLATERAL MEDULLA; SOLITARY TRACT NUCLEUS; STAINING; SYMPATHETIC NERVE; UPREGULATION; WESTERN BLOTTING;

ACTION POTENTIALS; ANIMALS; ANTIHYPERTENSIVE AGENTS; BLOOD PRESSURE; BLOTTING, WESTERN; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; HEART RATE; IMIDAZOLES; IMMUNOHISTOCHEMISTRY; INFUSIONS, PARENTERAL; INJECTIONS, INTRAVENOUS; INJECTIONS, INTRAVENTRICULAR; ISOTHIURONIUM; KIDNEY; MALE; MEDULLA OBLONGATA; NEURAL INHIBITION; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, SPRAGUE-DAWLEY; SYMPATHETIC NERVOUS SYSTEM; SYMPATHOLYTICS; TIME FACTORS;

EID: 71549153787     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvp202     Document Type: Article

References (60)

1. Ernsberger P, Giuliano R, Willette RN, Reis DJ. Role of imidazole receptors in the vasodepressor response to clonidine analogs in the rostral ventro-lateral medulla. J Pharmacol Exp Ther 1990;253:408-418.
2. Gomez RE, Ernsberger P, Feinland G, Reis DJ. Rilmenidine lowers arterial pressure via imidazole receptors in brainstem C1 area. Eur J Pharmacol 1991;195:181-191.
3. Ernsberger P, Damon TH, Graff LM, Schafer SG, Christen MO. Moxonidine, a centrally acting antihypertensive agent, is a selective ligand for I1-imidazoline sites. J Pharmacol Exp Ther 1993;264:172-182.
4. Guyenet PG. Is the hypotensive effect of clonidine and related drugs due to imidazoline binding sites? Am J Physiol 1997;273:R1580-R1584.
5. Haxhiu MA, Dreshaj I, Schafer SG, Ernsberger P. Selective antihyperten-sive action of moxonidine is mediated mainly by I1-imidazoline receptors in the rostral ventrolateral medulla. J Cardiovasc Pharmacol 1994; 24(Suppl. 1):S1-S8.
6. Dobrucki LW, Cabrera CL, Bohr DF, Malinski T. Central hypotensive action of clonidine requires nitric oxide. Circulation 2001;104:1884-1886.
7. Moreira TS, Takakura AC, Menani JV, Sato MA, Colombari E. Central blockade of nitric oxide synthesis reduces moxonidine-induced hypotension. Br J Pharmacol 2004;142:765-771.
8. Moreira TS, Takakura AC, Sato MA, Menani JV, Colombari E. Antihyperten-sive responses elicited by central moxonidine in rats: possible role of nitric oxide. J Cardiovasc Pharmacol 2006;47:780-787.
9. Gairard A, Lopez-Miranda V, Pernot F, Beck JF, Coumaros G, Van Overloop B et al. Effect of i1 imidazoline receptor agonist, moxonidine, in nitric oxide-deficient hypertension in pregnant rats. J Cardiovasc Pharmacol 2004;43:731-736.
10. Sy GY, Bruban V, Bousquet P, Feldman J. Nitric oxide discriminates the sites and mechanisms of action of centrally acting anti-hypertensive drugs in rabbits. Neuropharmacology 2002;43:1330-1338.
11. Krukoff TL. Central actions of nitric oxide in regulation of autonomic functions. Brain Res Rev 1999;30:52-65.
12. Zanzinger J. Role of nitric oxide in the neural control of cardiovascular function. Cardiovasc Res 1999;43:639-649.
13. Ricciardolo FL, Sterk PJ, Gaston B, Folkerts G. Nitric oxide in health and disease of the respiratory system. Physiol Rev 2004;84:731-765.
14. De Vente J, Hopkins DA, Markerink-Van Ittersum M, Emson PC, Schmidt HH, Steinbusch HW. Distribution of nitric oxide synthase and nitric oxide-receptive, cyclic GMP-producing structures in the rat brain. Neuroscience 1998;87:207-241.
15. Vincent SR, Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 1992;46:755-784.
16. Hirooka Y, Polson JW, Dampney RA. Pressor and sympathoexcitatory effects of nitric oxide in the rostral ventrolateral medulla. J Hypertens 1996;14:1317-1324.
17. Martins-Pinge MC, Baraldi-Passy I, Lopes OU. Excitatory effects of nitric oxide within the rostral ventrolateral medulla of freely moving rats. Hypertension 1997;30:704-707.
18. Morimoto S, Sasaki S, Miki S, Kawa T, Nakamura K, Itoh H et al. Nitric oxide is an excitatory modulator in the rostral ventrolateral medulla in rats. Am J Hypertens 2000;13:1125-1134.
19. Tseng CJ, Liu HY, Lin HC, Ger LP, Tung CS, Yen MH. Cardiovascular effects of nitric oxide in the brain stem nuclei of rats. Hypertension 1996;27: 36-42.
20. Zanzinger J, Czachurski J, Seller H. Inhibition of basal and reflex-mediated sympathetic activity in the RVLM by nitric oxide. Am J Physiol 1995;268:R958-R962.
21. Chan SH, Wang LL, Wang SH, Chan JY. Differential cardiovascular responses to blockade of nNOS or iNOS in rostral ventrolateral medulla of the rat. Br J Pharmacol 2001;133:606-614.
22. Chan JY, Wang LL, Wu KL, Chan SH. Reduced functional expression and molecular synthesis of inducible nitric oxide synthase in rostral ventrolat-eral medulla of spontaneously hypertensive rats. Circulation 2001;104: 1676-1681.
23. Kishi T, Hirooka Y, Ito K, Sakai K, Shimokawa H, Takeshita A. Cardiovascular effects of overexpression of endothelial nitric oxide synthase in the rostral ventrolateral medulla in stroke-prone spontaneously hypertensive rats. Hypertension 2002;39:264-268.
24. Wong ML, Rettori V, Al-Shekhlee A, Bongiorno PB, Canteros G, McCann SM et al. Inducible nitric oxide synthase gene expression in the brain during systemic inflammation. Nat Med 1996;2:581-584.
25. Chan SH, Wang LL, Chan JY. Differential engagements of glutamate and GABA receptors in cardiovascular actions of endogenous nNOS or iNOS at rostral ventrolateral medulla of rats. Br J Pharmacol 2003;138: 584-593.
26. Chan JY, Wang LL, Chao YM, Chan SH. Downregulation of basal iNOS at the rostral ventrolateral medulla is innate in SHR. Hypertension 2003;41: 563-570.
27. Wang WZ, Yuan WJ, Su DF. Blockade of N-methyl-D-aspartate receptors within the rostral ventrolateral medulla antagonizes clonidine-induced cardiovascular effects. Auton Neurosci 2003;109:21-28.
28. Wang LG, Zeng J, Yuan WJ, Su DF, Wang WZ. Comparative study of NMDA and AMPA/kainate receptors involved in cardiovascular inhibition produced by imidazoline-like drugs in anaesthetized rats. Exp Physiol 2007;92:849-858.
29. Lu Y, Wang LG, Liao Z, Tang CS, Wang WZ, Yuan WJ. Cardiovascular effects of centrally applied endothelin-1 1-31 and its relationship to endothelin-1 1-21 in rats. Auton Neurosci 2007;133:146-152.
30. Wallenius K, Wallenius V, Sunter D, Dickson SL, Jansson JO. Intracerebro-ventricular interleukin-6 treatment decreases body fat in rats. Biochem Biophys Res Commun 2002;293:560-565.
31. Kawasaki H, Nakamura S, Takasaki K. Central alpha 2-adrenoceptor-mediated pressor response to clonidine in conscious, spontaneously hypertensive rats. Jpn J Pharmacol 1992;59:321-331.
32. Southan GJ, Szabo C, Thiemermann C. Isothioureas: potent inhibitors of nitric oxide synthases with variable isoform selectivity. Br J Pharmacol 1995;114:510-516.
33. Wang WZ, Wang LG, Gao L, Wang W. Contribution of AMPA/kainate receptors in the rostral ventrolateral medulla to the hypotensive and sym-pathoinhibitory effects of clonidine. Am J Physiol Regul Integr Comp Physiol 2007;293:R1232-R1238.
34. Guo W, Xu X, Gao X, Burnstock G, He C, Xiang Z. Expression of P2X5 receptors in the mouse CNS. Neuroscience 2008;156:673-692.
35. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. New York, NY: Academic Press; 1998.
36. Garvey EP, Oplinger JA, Tanoury GJ, Sherman PA, Fowler M, Marshall S et al. Potent and selective inhibition of human nitric oxide synthases. Inhibition by non-amino acid isothioureas. J Biol Chem 1994;269: 26669-26676.
37. Stratman NC, Fici GJ, Sethy VH. U-19451A: a selective inducible nitric oxide synthase inhibitor. Life Sci 1996;59:945-951.
38. Mayorov DN. Selective sensitization by nitric oxide of sympathetic baror-eflex in rostral ventrolateral medulla of conscious rabbits. Hypertension 2005;45:901-906.
39. Kimura Y, Hirooka Y, Sagara Y, Ito K, Kishi T, Shimokawa H et al. Overex-pression of inducible nitric oxide synthase in rostral ventrolateral medulla causes hypertension and sympathoexcitation via an increase in oxidative stress. Circ Res 2005;96:252-260.
40. King PR, Suzuki S, Louis WJ, Gundlach AL. Distribution of nonadrenergic [3H]rilmenidine binding in rat brain and kidney. Ann NY Acad Sci 1995; 763:194-207.
41. Turcani M. Biphasic dose-dependent modulation of cardiac parasympa-thetic activity by moxonidine, an imidazoline I1-receptor agonist. J Cardiovasc Pharmacol 2008;52:524-535.
42. Unnerstall JR, Kopajtic TA, Kuhar MJ. Distribution of alpha 2 agonist binding sites in the rat and human central nervous system: analysis of some functional, anatomic correlates of the pharmacologic effects of clonidine and related adrenergic agents. Brain Res 1984;319:69-101.
43. Li G, Abdel-Rahman AA. Direct evidence for imidazoline (I1) receptor modulation of ethanol action on norepinephrine-containing neurons in the rostral ventrolateral medulla in conscious spontaneously hypertensive rats. Alcohol Clin Exp Res 2007;31:684-693.
44. Chan CK, Burke SL, Zhu H, Piletz JE, Head GA. Imidazoline receptors associated with noradrenergic terminals in the rostral ventrolateral medulla mediate the hypotensive responses of moxonidine but not cloni-dine. Neuroscience 2005;132:991-1007.
45. Tingley FD III, Arneric SP. Evidence for clonidine presynaptically modulating amino acid release in the rostral ventral medulla: role in hypertension. Brain Res 1990;537:175-181.
46. Jastrzebski Z, Czyzewska-Szafran H, Gozlinska B, Remiszewska M, Mazurek AP. Clonidine hypotension in spontaneously hypertensive rats (SHR) depends on the functional state of GABAergic and glutamatergic systems. Neurosci Lett 1995;184:94-96.
47. Dampney RA. Functional organization of central pathways regulating the cardiovascular system. Physiol Rev 1994;74:323-364.
48. Sakai K, Hirooka Y, Matsuo I, Eshima K, Shigematsu H, Shimokawa H et al. Overexpression of eNOS in NTS causes hypotension and bradycardia in vivo. Hypertension 2000;36:1023-1028.
49. Harada S, Tokunaga S, Momohara M, Masaki H, Tagawa T, Imaizumi Tet al. Inhibition of nitric oxide formation in the nucleus tractus solitarius increases renal sympathetic nerve activity in rabbits. Circ Res 1993;72: 511-516.
50. Eshima K, Hirooka Y, Shigematsu H, Matsuo I, Koike G, Sakai K et al. Angiotensin in the nucleus tractus solitarii contributes to neurogenic hypertension caused by chronic nitric oxide synthase inhibition. Hypertension 2000;36:259-263.
51. Head GA, Burke SL. Relative importance of medullary brain nuclei for the sympatho-inhibitory actions of rilmenidine in the anaesthetized rabbit. J Hypertens 1998;16:503-517.
52. Wemer J, Frankhuyzen AL, Mulder AH. Pharmacological characterization of presynaptic alpha-adrenoceptors in the nucleus tractus solitarii and the cerebral cortex of the rat. Neuropharmacology 1982;21:499-506.
53. Punnen S, Urbanski R, Krieger AJ, Sapru HN. Ventrolateral medullary pressor area: site of hypotensive action of clonidine. Brain Res 1987; 422:336-346.
54. Venturini G, Colasanti M, Persichini T, Fioravanti E, Federico R, Ascenzi P. Selective inhibition of nitric oxide synthase type I by clonidine, an anti-hypertensive drug. Biochem Pharmacol 2000;60:539-544.
55. Edwards L, Fishman D, Horowitz P, Bourbon N, Kester M, Ernsberger P. The I1-imidazoline receptor in PC12 pheochromocytoma cells activates. protein kinases C, extracellular signal-regulated kinase (ERK) and c-jun N-terminal kinase (JNK). J Neurochem 2001;79:931-940.
56. Zhang J, El-Mas MM, Abdel-Rahman AA. Imidazoline I(1) receptor-induced activation of phosphatidylcholine-specific phospholipase C elicits mitogen-activated protein kinase phosphorylation in PC12 cells. Eur J Pharmacol 2001;415:117-125.
57. Separovic D, Kester M, Haxhiu MA, Ernsberger P. Activation of phosphatidylcholine-selective phospholipase C by I1-imidazoline receptors in PC12 cells and rostral ventrolateral medulla. Brain Res 1997; 749:335-339.
58. Chan JY, Chang AY, Wang LL, Ou CC, Chan SH. Protein kinase C-dependent mitochondrial translocation of proapoptotic protein Bax on activation of inducible nitric-oxide synthase in rostral ventrolateral medulla mediates cardiovascular depression during experimental endotoxemia. Mol Pharmacol 2007;71:1129-1139.
59. Da Silva J, Pierrat B, Mary JL, Lesslauer W. Blockade of p38 mitogen-activated protein kinase pathway inhibits inducible nitric-oxide synthase expression in mouse astrocytes. J Biol Chem 1997;272:28373-28380.
60. Su NY, Tsai PS, Huang CJ. Clonidine-induced enhancement of iNOS expression involves NF-kappaB. J Surg Res 2008;149:131-137.