Inhibition of Rac1-derived reactive oxygen species in nucleus tractus solitarius decreases blood pressure and heart rate in stroke-prone spontaneously hypertensive rats

Hypertension

Volumn 50, Issue 1, 2007, Pages 62-68

  Nozoe, Masatsugu ^a   Hirooka, Yoshitaka ^a   Koga, Yasuaki ^a   Sagara, Yoji ^a   Kishi, Takuya ^a   Engelhardt, John F ^b   Sunagawa, Kenji ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Blood pressure; Brain; Heart rate; Hypertension; Sympathetic nervous system

Indexed keywords

ADENOVIRUS VECTOR; COPPER ZINC SUPEROXIDE DISMUTASE; NORADRENALIN; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MEASUREMENT; BLOOD PRESSURE REGULATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENETIC CODE; HEART RATE; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SOLITARY TRACT NUCLEUS; STATISTICAL ANALYSIS; STROKE PRONE SPONTANEOUSLY HYPERTENSIVE RAT; URINARY EXCRETION; WISTAR KYOTO RAT;

ADENOVIRIDAE; ANIMALS; BLOOD PRESSURE; CEREBROVASCULAR ACCIDENT; GENE TRANSFER TECHNIQUES; GENETIC PREDISPOSITION TO DISEASE; GENETIC VECTORS; HEART RATE; HUMANS; HYPERTENSION; MALE; NADPH OXIDASE; OXIDATIVE STRESS; RAC1 GTP-BINDING PROTEIN; RATS; RATS, INBRED SHR; RATS, INBRED WKY; REACTIVE OXYGEN SPECIES; SOLITARY NUCLEUS; SUPEROXIDE DISMUTASE;

EID: 34250828562     PISSN: 0194911X     EISSN: None     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.107.087981     Document Type: Article

References (39)

1. Kishi T, Hirooka Y, Kimura Y, Ito K, Shimokawa H, Takeshita A. Increased reactive oxygen species in rostral ventrolateral medulla contribute to neural mechanisms of hypertension in stroke-prone spontaneously hypertensive rats. Circulation. 2004;109:2357-2362.
2. Zimmerman MC, Dunlay RP, Lazartigues E, Zhang Y, Sharma RV, Engelhardt JF, Davisson RL. Requirement for Rac1-dependent NADPH oxidase in the cardiovascular and dipsogenic actions of angiotensin II in the brain. Circ Res. 2004;95:532-539.
3. Kimura Y, Hirooka Y, Sagara Y, Ito K, Kishi T, Shimokawa H, Takeshita A, Sunagawa K. Overexpression 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.
4. Lindley TE, Doobay MF, Sharma RV, Davisson RL. Superoxide is involved in the central nervous system activation and sympathoexcitation of myocardial infarction-induced heart failure. Circ Res. 2004;94:402-409.
5. Gao L, Wang W, Li YL, Schultz HD, Liu D, Cornish KG, Zucker IH. Superoxide mediates sympathoexcitation in heart failure: roles of angiotensin II and NAD(P)H oxidase. Circ Res. 2004;95:937-944.
6. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res. 2000;87:840-844.
7. Wang G, Anrather J, Huang J, Speth RC, Pickel VM, Iadecola C. NADPH oxidase contributes to angiotensin II signaling in the nucleus tractus solitarius. J Neurosci. 2004;24:5516-5524.
8. Vecchione C, Aretini A, Marino G, Bettarini U, Poulet R, Maffei A, Sbroggio M, Pastore L, Gentile MT, Notte A, Iorio L, Hirsch E, Tarone G, Lembo G. Selective Rac-1 inhibition protects from diabetes-induced vascular injury. Circ Res. 2006;98:218-225.
9. Abo A, Pick E, Hall A, Totty N, Teahan CG, Segal AW. Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature. 1991;353:668-670.
10. Sakai K, Hirooka Y, Matsuo I, Eshima K, Shigematsu H, Shimokawa H, Takeshita A. Overexpression of eNOS in NTS causes hypotension and bradycardia in vivo. Hypertension. 2000;36:1023-1028.
11. Ito K, Hirooka Y, Sakai K, Kishi T, Kaibuchi K, Shimokawa H, Takeshita A. Rho/Rho-kinase pathway in brain stem contributes to blood pressure regulation via sympathetic nervous system: possible involvement in neural mechanisms of hypertension. Circ Res. 2003;92:1337-1343.
12. Weston M, Wang H, Stornetta RL, Sevigny CP, Guyenet PG. Fos expression by glutamatergic neurons of the solitary tract nucleus after phenylephrine-induced hypertension in rats. J Comp Neurol. 2003;460:525-541.
13. Healy DP, Rettig R, Nguyen T, Printz MP. Quantitative autoradiography of angiotensin II receptors in the rat solitary-vagal area: effects of nodose ganglionectomy or sinoaortic denervation. Brain Res. 1989;484:1-12.
14. Gutkind JS, Kurihara M, Castren E, Saavedra JM. Increased concentration of angiotensin II binding sites in selected brain areas of spontaneously hypertensive rats. J Hypertens. 1988;6:79-84.
15. Sato AM, Vanderlei Menani J, Ubriaco Lopes O, Colombari E. Lesions of the commissural nucleus of the solitary tract reduce arterial pressure in spontaneously hypertensive rats. Hypertension. 2001;38:560-564.
16. Wong LF, Polson JW, Murphy D, Paton JF, Kasparov S. Genetic and pharmacological dissection of pathways involved in the angiotensin II-mediated depression of baroreflex function. FASEB J. 2002;16:1595-1601.
17. Loewy AD, McKellar S. The neuroanatomical basis of central cardiovascular control. Fed Proc. 1980;39:2495-2503.
18. Tanaka M, Umemoto S, Kawahara S, Kubo M, Itoh S, Umeji K, Matsuzaki M. Angiotensin II type 1 receptor antagonist and angiotensin-converting enzyme inhibitor altered the activation of Cu/Zn-containing superoxide dismutase in the heart of stroke-prone spontaneously hypertensive rats. Hypertens Res. 2005;28:67-77.
19. Miller FJ Jr, Griendling KK. Functional evaluation of nonphagocytic NAD(P)H oxidases. Methods Enzymol. 2002;353:220-233.
20. Zwacka RM, Dudus L, Epperly MW, Greenberger JS, Engelhardt JF. Redox gene therapy protects human IB-3 lung epithelial cells against ionizing radiation-induced apoptosis. Hum Gene Ther. 1998;9:1381-1386.
21. Lehmann TG, Wheeler MD, Schwabe RF, Connor HD, Schoonhoven R, Bunzendahl H, Brenner DA, Jude Samulski R, Zhong Z, Thurman RG. Gene delivery of Cu/Zn-superoxide dismutase improves graft function after transplantation of fatty livers in the rat. Hepatology. 2000;32:1255-1264.
22. Korzhevskii DE, Gilerovich EG, Zin'kova NN, Grigor'ev IP, Otellin VA. Immunocytochemical detection of brain neurons using the selective marker NeuN. Neurosci Behav Physiol. 2006;36:857-859.
23. 2+-, and protein kinase C play a role in angiotensin II-induced free radical production in nucleus tractus solitarius. Hypertension. 2006;48:482-489.
24. 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.
25. Li HW, Gao YX, Matsuura T, Martynyuk A, Raizada MK, Sumners C. Adenoviral-mediated neuron specific transduction of angiotensin II type 2 receptors. Regul Pept. 2005;126:213-222.
26. Allen AM, Dosanjh J, Dassanayake S, Tan G, Thomas WG. Baroreceptor reflex stimulation does not induce cytomegalovirus promoter-driven transgene expression in the ventrolateral medulla in vivo. Auton Neurosci. 2006;126-127:150-155.
27. Glass MJ, Huang J, Oselkin M, Tarsitano MJ, Wang G, Iadecola C, Pickel VM. Subcellular localization of nicotinamide adenine dinucleotide phosphate oxidase subunits in neurons and astroglia of the rat medial nucleus tractus solitarius: relationship with tyrosine hydroxylase immunoreactive neurons. Neuroscience. 2006;143:547-564.
28. Sakai K, Chapleau MW, Morimoto S, Cassell MD, Sigmund CD. Differential modulation of baroreflex control of heart rate by neuron- vs. glia-derived angiotensin II. Physiol Genomics. 2004;20:66-72.
29. Dampney RA. Angiotensin type 1A receptors on glial cells in rostral ventrolateral medulla and hypertension. Hypertension. 2006;47:1052-1053.
30. Zimmerman MC, Lazartigues E, Sharma RV, Davisson RL. Hypertension caused by angiotensin II infusion involves increased superoxide production in the central nervous system. Circ Res. 2004;95:210-216.
31. Gehlert DR, Gackenheimer SL, Schober DA. Autoradiographic localization of subtypes of angiotensin II antagonist binding in the rat brain. Neuroscience. 1991;44:501-514.
32. Diz DI, Barnes KL, Ferrario CM. Hypotensive actions of microinjections of angiotensin II into the dorsal motor nucleus of the vagus. J Hypertens. 1984;2(suppl):S53-S56.
33. Fow JE, Averill DB, Barnes KL. Mechanisms of angiotensin-induced hypotension and bradycardia in the medial solitary tract nucleus. Am J Physiol. 1994;267:H259-H266.
34. Rettig R, Healy DP, Printz MP. Cardiovascular effects of microinjections of angiotensin II into the nucleus tractus solitarii. Brain Res. 1986;364:233-240.
35. Chen Y, Chen H, Hoffmann A, Cool DR, Diz DI, Chappell MC, Chen AF, Morris M. Adenovirus-mediated small-interference RNA for in vivo silencing of angiotensin AT1a receptors in mouse brain. Hypertension. 2006;47:230-237.
36. Zanzinger J. Role of nitric oxide in the neural control of cardiovascular function. Cardiovasc Res. 1999;43:639-649.
37. Dias AC, Vitela M, Colombari E, Mifflin SW. Nitric oxide modulation of glutamatergic, baroreflex, and cardiopulmonary transmission in the nucleus of the solitary tract. Am J Physiol Heart Circ Physiol. 2005;288:H256-H262.
38. Hirooka Y, Sakai K, Kishi T, Ito K, Shimokawa H, Takeshita A. Enhanced depressor response to endothelial nitric oxide synthase gene transfer into the nucleus tractus solitarii of spontaneously hypertensive rats. Hypertens Res. 2003;26:325-331.
39. Matsuo I, Hirooka Y, Hironaga K, Eshima K, Shigematsu H, Shihara M, Sakai K, Takeshita A. Glutamate release via NO production evoked by NMDA in the NTS enhances hypotension and bradycardia in vivo. Am J Physiol Regul Integr Comp Physiol. 2001;280:R1285-R1291.