Brain stem NOS and ROS in neural mechanisms of hypertension

Antioxidants and Redox Signaling

Volumn 20, Issue 1, 2014, Pages 146-163

  Chan, Samuel H H ^a   Chan, Julie Y H ^a  

^a CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; GUANYLATE CYCLASE; NITRIC OXIDE SYNTHASE; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN 2;

ANTIHYPERTENSIVE THERAPY; BLOOD PRESSURE REGULATION; BRAIN STEM; ENZYMATIC DEGRADATION; HUMAN; HYPERTENSION; MITOCHONDRION; NERVE CELL; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXIDATIVE STRESS; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTIHYPERTENSIVE AGENTS; BRAIN STEM; HUMANS; HYPERTENSION; NITRIC OXIDE SYNTHASE; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84891783632     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5230     Document Type: Review

References (190)

1. Agarwal D, Welsch MA, Keller JN, and Francis J. Chronic exercise modulates RAS components and improves balance between pro-And anti-inflammatory cytokines in the brain of SHR. Basic Res Cardiol 106: 1069-1085, 2011.
2. Ahern GP, Klyachko VA, and Jackson MB. cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci 25: 510-517, 2002.
3. Aicher SA, Milner TA, Pickel VM, and Reis DJ. Anatomical substrates for baroreflex sympathoinhibition in the rat. Brain Res Bull 51: 107-110, 2000.
4. Ally A, Phattanarudee S, Kabadi S, Patel M, and Maher TJ. Cardiovascular responses and neurotransmitter changes during static muscle contraction following blockade of inducible nitric oxide synthase (iNOS) within the ventrolateral medulla. Brain Res 1090: 123-133, 2006.
5. Biancardi VD, Son SJ, Sonner PM, Zheng H, Patel KP, and Stern JE. Contribution of central nervous system endothelial nitric oxide synthase to neurohumoral activation in heart failure rats. Hypertension 58: 454-463, 2011.
6. Campese VM, Shaohua Y, and Huiquin Z. Oxidative stress mediates angiotensin II-dependent stimulation of sympathetic nerve activity. Hypertension 46: 533-539, 2005.
7. Campese VM, Ye S, Zhong H, Yanamadala V, Ye Z, and Chiu J. Reactive oxygen species stimulate central and peripheral sympathetic nervous system activity. Am J Physiol Heart Circ Physiol 287: H695-H703, 2004.
8. Cardinale JP, Sriramula S, Mariappan N, Agarwal D, and Francis J. Angiotensin II-induced hypertension is modulated by nuclear factor-jBin the paraventricular nucleus. Hypertension 59: 113-121, 2012.
9. Cardoso LM, Colombari DS, Menani JV, Toney GM, Chianca DA Jr., and Colombari E. Cardiovascular responses to hydrogen peroxide into the nucleus tractus solitarius. Am J Physiol Regul Integr Comp Physiol 297: R462-R469, 2009.
10. Carvalho TH, Lopes OU, and Tolentino-Silva FR. Baroreflex responses in neuronal nitric oxide synthase knoukout mice (nNOS). Auton Neurosci 126: 163-168, 2006.
11. Chan JYH, Chan SHH, Li FC, Tsai CY, Cheng HL, and Chang AYW. Phasic cardiovascular responses to mevinphos are mediated through differential activation of cGMP/PKG cascade and peroxynitrite via nitric oxide generated in the rat rostral ventrolateral medulla by NOS I and II isoforms. Neuropharmacology 48: 161-172, 2005.
12. Chan JYH, Chen WC, Lee HY, and Chan SHH. Elevated Fos expression in the NTS is associated with reduced baroreflex response in SHR. Hypertension 32: 939-944, 1998.
13. Chan JYH, Shih CD, and Chan SHH. Enhancement of spontaneous baroreflex by antisense c-fos oligonucleotide treatment in the NTS of the rat. Am J Physiol 273: H2200-H2208, 1997.
14. Chan JYH, Wang LL, Chao YM, and Chan SHH. Downregulation of basal iNOS at the rostral ventrolateral medulla is innate in SHR. Hypertension 41: 563-570, 2003.
15. Chan JYH, Wang LL, Lee HY, and Chan SHH. Augmented up-regulation by c-fos of angiotensin subtype 1 receptors in nucleus tractus solitarii of spontaneously hypertensive rats. Hypertension 40: 335-341, 2002.
16. Chan JYH, Wang LL, Wu KLH, and Chan SHH. Reduced functional expression and molecular synthesis of inducible nitric oxide synthase in rostral ventrolateral medulla of spontaneously hypertensive rats. Circulation 104: 1676-1681, 2001.
17. Chan SHH and Chan JYH. Angiotensin-generated reactive oxygen species in brain and pathogenesis of cardiovascular diseases. Antioxid Redox Signal 19: 1074-1084, 2013.
18. Chan SHH and Chan JYH. Brain stem oxidative stress and its associated signaling in the regulation of sympathetic vasomotor tone. J Appl Physiol 113: 1921-1928, 2012.
19. Chan SHH, Chao YM, Tseng CJ, and Chan JYH. Downregulation of basal Fos expression at nucleus tractus solitarii underlies restoration of baroreflex response after antihypertensive treatment in spontaneously hypertensive rats. Neuroscience 112: 113-120, 2002.
20. Chan SHH, Hsu KS, Huang CC, Wang LL, Ou CC, and Chan JYH. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced pressor effect via activation of p38 mitogen-Activated protein kinase in the rostral ventrolateral medulla. Circ Res 97: 772-780, 2005.
21. Chan SHH, Tai MH, Li CY, and Chan JYH. Reduction in molecular synthesis or enzyme activity of superoxide dismutases and catalase contributes to oxidative stress and neurogenic hypertension in spontaneously hypertensive rats. Free Radic Biol Med 40: 2028-2039, 2006.
22. Chan SHH, Wang LL, and Chan JYH. Differential engagements of glutamate and GABA receptors in cardiovascular actions of endogenous nNOS or iNOS at rostral ventrolateral medulla of rats. Br J Pharmacol 138: 584-593, 2003.
23. Chan SHH, Wang LL, Tseng HL, and Chan JYH. Upregulation of AT1 receptor gene on activation of PKCb-NADPH oxidase-ERK1/2-c-fos signaling cascade mediates longterm pressor effect of angiotensin II in rostral ventrolateral medulla. J Hypertens 25: 1845-1861, 2007.
24. Chan SHH, Wang LL, Wang SH, and Chan JYH. Differential cardiovascular responses to blockade of nNOS or iNOS in rostral ventrolateral medulla of the rat. Br J Pharmacol 133: 606-614, 2001.
25. Chan SHH, Wu CA, Wu KLH, Ho YH, Chang AYW, and Chan JYH. Transcriptional upregulation of mitochondrial uncoupling protein 2 protects against oxidative stress-Associated neurogenic hypertension. Circ Res 105: 886-896, 2009.
26. Chan SHH, Wu CW, Chang AYW, Hsu KS, and Chan JYH. Transcriptional upregulation of brain-derived neurotrophic factor in rostral ventrolateral medulla by angiotensin II: significance in superoxide homeostasis and neural regulation of arterial pressure. Circ Res 107: 1127-1139, 2010.
27. Chan SHH, Wu KLH, Chang AYW, Tai MH, and Chan JYH. Oxidative impairment of mitochondrial electron transport chain complexes in rostral ventrolateral medulla contributes to neurogenic hypertension. Hypertension 53: 217-227, 2009.
28. Chan SHH, Wu KLH, Kung PS, and Chan JYH. Oral intake of rosiglitazone promotes central antihypertensive effect via upregulation of PPAR-c and alleviation of oxidative stress in RVLM of SHR. Hypertension 55: 1444-1453, 2010.
29. Chang AYW, Chan JYH, and Chan SHH. Differential distribution of nitric oxide synthase isoforms in rostral ventrolateral medulla of the rat. J Biomed Sci 10: 285-291, 2003.
30. Cheng WH, Lu PJ, Ho WY, Tung CS, Cheng PW, Hsiao M, and Tseng CJ. Angiotensin II inhibits neuronal nitric oxide synthase activation through the ERK1/2-RSK signaling pathway to modulate central control of blood pressure. Circ Res 106: 788-795, 2010.
31. Cheng WH, Lu PJ, Hsiao M, Hsiao CH, Ho WY, Cheng PW, Lin CT, Hong LZ, and Tseng CJ. Renin activates PI3K-Akt-eNOS signalling through the angiotensin AT(1) and Mas receptors to modulate central blood pressure control in the nucleus tractus solitarii. Br J Pharmacol 166: 2024-2035, 2012.
32. Chianca DA Jr., Lin LH, Dragon DN, and Talman WT. NMDA receptors in nucleus tractus solitarii are linked to soluble guanylate cyclase. Am J Physiol Heart Circ Physiol 286: H1521-H1527, 2004.
33. Dampney RA. Functional organization of central pathways regulating the cardiovascular system. Physiol Rev 74: 323-364, 1994.
34. Dampney RA, Horiuchi J, Killinger S, Sheriff MJ, Tan PS, and McDowall LM. Long-term regulation of arterial blood pressure by hypothalamic nuclei: some critical questions. Clin Exp Pharmacol Physiol 32: 419-425, 2005.
35. Dampney RA, Horiuchi J, Tagawa T, Fontes MA, Potts PD, and Polson JW. Medullary and supramedullary mechanisms regulating sympathetic vasomotor tone. Acta Physiol Scand 177: 209-218, 2003.
36. de Oliveira-Sales EB, Nishi EE, Boim MA, Dolnikoff MS, Bergamaschi CT, and Campos RR. Upregulation of AT1R and iNOS in the rostral ventrolateral medulla (RVLM) is essential for the sympathetic hyperactivity and hypertension in the 2K-1C Wistar rat model. Am J Hypertens 23: 708-715, 2010.
37. Dikalov S. Cross talk between mitochondria and NADPH oxidases. Free Radic Biol Med 51: 1289-1301, 2011.
38. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, Harrison DG, and Dikalov SI. Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 107: 106-116, 2010.
39. Diz DI, Garcia-Espinosa MA, Gegick S, Tommasi EN, Ferrario CM, Ann Tallant E, Chappell MC, and Gallagher PE. Injections of angiotensin-converting enzyme 2 inhibitor MLN4760 into nucleus tractus solitarii reduce baroreceptor reflex sensitivity for heart rate control in rats. Exp Physiol 93: 694-700, 2008.
40. Edwards MA, Loxley RA, Powers-Martin K, Lipski J, McKitrick DJ, Arnolda LF, and Phillips JK. Unique levels of expression of N-methyl-D-Aspartate receptor subunits and neuronal nitric oxide synthase in the rostral ventrolateral medulla of the spontaneously hypertensive rat. Brain Res Mol Brain Res 129: 33-43, 2004.
41. Elfering SL, Sarkela TM, and Giulivi C. Biochemistry of mitochondrial nitric-oxide synthase. J Biol Chem 277: 38079-38086, 2002.
42. Esler M, Lambert E, and Schlaich M. Point: chronic activation of the sympathetic nervous system is the dominant contributor to systemic hypertension. J Appl Physiol 109: 1996-1998, 2010.
43. Feng Y, Xia H, Cai Y, Halabi CM, Becker LK, Santos RA, Speth RC, Sigmund CD, and Lazartigues E. Brain-selective overexpression of human angiotensin-converting enzyme type 2 attenuates neurogenic hypertension. Circ Res 106: 373-382, 2010.
44. Feron O, Dessy C, Desager JP, and Balligand JL. Hydroxymethylglutaryl- coenzyme A reductase inhibition promotes endothelial nitric oxide synthase activation through a decrease in caveolin abundance. Circulation 103: 113-118, 2001.
45. Ferrari MF and Fior-Chadi DR. Differential expression of nNOS mRNA and protein in the nucleus tractus solitarii of young and aged Wistar-Kyoto and spontaneously hypertensive rats. J Hypertens 23: 1683-1690, 2005.
46. Fletcher J, Moody WE, Chowdhary S, and Coote JH. NOcGMP pathway at ventrolateral medullary cardiac inhibitory sites enhances the baroreceptor reflex bradycardia in the rat. Brain Res 1123: 125-134, 2006.
47. Forstermann U, Kleinert H, Gath I, Schwarz P, Closs E, and Dun N. Expression and expressional control of nitric oxide synthases in various cell types. Adv Pharmacol 34: 171-186, 1995.
48. Forstermann U and Li H. Therapeutic effect of enhancing endothelial nitric oxide synthase (eNOS) expression and preventing eNOS uncoupling. Br J Pharmacol 164: 213-223, 2011.
49. Gao J, Zhang H, Le KD, Chao J, and Gao L. Activation of central angiotensin type 2 receptors suppresses norepinephrine excretion and blood pressure in conscious rats. Am J Hypertens 24: 724-730, 2011.
50. Gao L, Li Y, Schultz HD, Wang WZ, Wang W, Finch M, Smith LM, and Zucker IH. Downregulation of Kv4.3 expression in RVLM as a potential mechanism for sympathoexcitation in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 298: H945-H955, 2010.
51. Gao L, Wang W, Li YL, Schultz HD, Liu D, Cornish KG, and Zucker IH. Superoxide mediates sympathoexcitation in heart failure: roles of angiotensin II and NAD(P)H oxidase. Circ Res 95: 937-944, 2004.
52. Gao L, Wang W, Li YL, Schultz HD, Liu D, Cornish KG, and Zucker IH. Sympathoexcitation by central ANG II: roles for AT1 receptor upregulation and NAD(P)H oxidase in RVLM. Am J Physiol Heart Circ Physiol 288: H2271-H2279, 2005.
53. Gao L, Wang W, and Zucker IH. Simvastatin inhibits central sympathetic outflow in heart failure by a nitric-oxide synthase mechanism. J Pharmacol Exp Ther 326: 278-285, 2008.
54. Gao Y. The multiple actions of NO. Pflugers Arch 459: 829-839, 2010.
55. Garthwaite J. Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 27: 2783-2802, 2008.
56. Ghafourifar P and Cadenas E. Mitochondrial nitric oxide synthase. Trends Pharmacol Sci 26: 190-195, 2005.
57. Gilmore JL, Yi X, Quan L, and Kabanov AV. Novel nanomaterials for clinical neuroscience. J Neuroimmune Pharmacol 3: 83-94, 2008.
58. Giulivi C, Poderoso JJ, and Boveris A. Production of nitric oxide by mitochondria. J Biol Chem 273: 11038-11043, 1998.
59. Giusti MF, Sato MA, Cardoso LM, Braga VA, and Colombari E. Central antioxidant therapy inhibits parasympathetic baroreflex control in conscious rats. Neurosci Lett 489: 115-118, 2011.
60. Gregg D, Rauscher FM, and Goldschmidt-Clermont PJ. Rac regulates cardiovascular superoxide through diverse molecular interactions: more than a binary GTP switch. Am J Physiol 285: C723-C734, 2003.
61. Guo ZL, Tjen-A-Looi SC, Fu LW, and Longhurst JC. Nitric oxide in rostral ventrolateral medulla regulates cardiacsympathetic reflexes: role of synthase isoforms. Am J Physiol Heart Circ Physiol 297: H1478-H1486, 2009.
62. Guyenet PG, Haselton JR, and Sun MK. Sympathoexcitatory neurons of rostroventrolateral medulla and the origin of the sympathetic vasomotor tone. Prog Brain Res 81: 105-116, 1989.
63. Hattori Y, Nakanishi N, Akinoto K, Yoshida M, and Kasai K. HMG-CoA reductase inhibitor increase GTP cyclohydrolase I mRNA and tetrahydrobiopterin in vascular endothelial cells. Arterioscler Thromb Vasc Biol 23: 176-182, 2003.
64. Hirooka Y. Role of reactive oxygen species in brainstem in neural mechanisms of hypertension. Auton Neurosci 142: 20-24, 2008.
65. Hirooka Y. Oxidative stress in the cardiovascular center has a pivotal role in the sympathetic activation in hypertension. Hypertens Res 34: 407-412, 2011.
66. Hirooka Y, Kimura Y, Nozoe M, Sagara Y, Ito K, and Sunagawa K. Amlodipine-induced reduction of oxidative stress in the brain is associated with sympatho-inhibitory effects in stroke-prone spontaneously hypertensive rats. Hypertens Res 29: 49-56, 2006.
67. Hirooka Y, Kishi T, Sakai K, Takeshita A, and Sunagawa K. Imbalance of central nitric oxide and reactive oxygen species in the regulation of sympathetic activity and neural mechanisms of hypertension. Am J Physiol Regul Integr Comp Physiol 300: R818-R826, 2011.
68. Hirooka Y, Sagara Y, Kishi T, and Sunagawa K. Oxidative stress and central cardiovascular regulation: pathogenesis of hypertension and therapeutic aspects. Circ J 74: 827-835, 2010.
69. Hirooka Y, Sakai K, Kishi T, and Takeshita A. Adenovirus-mediated gene transfer into the NTS in conscious rats. A new approach to examining the central control of cardiovascular regulation. Ann N Y Acad Sci 940: 197-205, 2001.
70. Hirooka Y, Shigematsu H, Kishi T, Kimura Y, Ueta Y, and Takeshita A. Reduced nitric oxide synthase in the brainstem contributes to enhanced sympathetic drive in rats with heart failure. J Cardiovasc Pharmacol 42: S111-S115, 2003.
71. Hsieh HY, Robertson CL, Vermehren-Schmaedick A, and Balkowiec A. Nitric oxide regulates BDNF release from nodose ganglion neurons in a pattern-dependent and cGMP-independent manner. J Neurosci 88: 1285-1297, 2010.
72. Huang CC, Chan SHH, and Hsu KS. cGMP/protein kinase G-dependent potentiation of glutamatergic transmission induced by nitric oxide in immature rat rostral ventrolateral medulla neurons in vitro. Mol Pharmacol 64: 521-532, 2003.
73. Huang CC, Chan SHH, and Hsu KS. 3-Morpholinylsydnonimine inhibits glutamatergic transmission in rat rostral ventrolateral medulla via peroxynitrite formation and adenosine release. Mol Pharmacol 66: 492-501, 2004.
74. Huang HN, Lu PJ, Lo WC, Lin CH, Hsiao M, and Tseng CJ. In situ Akt phosphorylation in the nucleus tractus solitarii is involved in central control of blood pressure and heart rate. Circulation 110: 2476-2483, 2004.
75. Iadecola C, Zhang F, Xu S, Casey R, and Ross ME. Inducible nitric oxide synthase gene expression in brain following cerebral ischemia. J Cereb Blood Flow Metab 15: 378-384, 1995.
76. Imada I, Sato EF, Kira Y, and Inoue M. Effect of CoQ homologues on reactive oxygen generation by mitochondria. Biofactors 32: 41-48, 2008.
77. Kang YM, Ma Y, Zheng JP, Elks C, Sriramula S, Yang ZM, and Francis J. Brain nuclear factor-kappa B activation contributes to neurohumoral excitation in angiotensin II-induced hypertension. Cardiovasc Res 82: 503-512, 2009.
78. Kenney MJ, Weiss ML, and Haywood JR. The paraventricular nucleus: an important component of the central neurocircuitry regulating sympathetic nerve outflow. Acta Physiol Scand 177: 7-15, 2003.
79. Kimura Y, Hirooka Y, Kishi T, Ito K, Sagara Y, and Sunagawa K. Role of inducible nitric oxide synthase in rostral ventrolateral medulla in blood pressure regulation in spontaneously hypertensive rats. Clin Exp Hypertens 31: 281-286, 2009.
80. Kimura Y, Hirooka Y, Sagara Y, Ito K, Kishi T, Shimokawa H, Takeshita A, and Sunagawa K. Overexpression of inducible nitric oxide synthase in rostral ventrolateral medulla causes hypertension and sympathoexcitation via an increase in oxidative stress. Circ Res 96: 252-260, 2005.
81. Kishi T and Hirooka Y. Oxidative stress in the brain causes hypertension via sympathoexcitation. Front Physiol 3: 335, 2012.
82. Kishi T, Hirooka Y, Ito K, Sakai K, Shimokawa H, and Takeshita A. Cardiovascular effects of overexpression of endothelial nitric oxide synthase in the rostral ventrolateral medulla in stroke-prone spontaneously hypertensive rats. Hypertension 39: 264-268, 2002.
83. Kishi T, Hirooka Y, Kimura Y, Ito K, Shimokawa H, and Takeshita A. Increased reactive oxygen species in rostral ventrolateral medulla contribute to neural mechanisms of hypertension in stroke-prone spontaneously hypertensive rats. Circulation 109: 2357-2362, 2004.
84. Kishi T, Hirooka Y, Kimura Y, Sakai K, Ito K, Shimokawa H, and Takeshita A. Overexpression of eNOS in RVLM improves impaired baroreflex control of heart rate in SHRSP. Rostral ventrolateral medulla. Stroke-prone spontaneously hypertensive rats. Hypertension 41: 255-260, 2003.
85. Kishi T, Hirooka Y, Konno S, Ogawa K, and Sunagawa K. Angiotensin II type 1 receptor-Activated caspase-3 through ras/mitogen-Activated protein kinase/extracellular signal-regulated kinase in the rostral ventrolateral medulla is involved in sympathoexcitation in stroke-prone spontaneously hypertensive rats. Hypertension 55: 291-297, 2010.
86. Kishi T, Hirooka Y, Konno S, and Sunagawa K. Atorvastatin improves the impaired baroreflex sensitivity via antioxidant effect in the rostral ventrolateral medulla of SHRSP. Clin Exp Hypertens 31: 698-704, 2009.
87. Kishi T, Hirooka Y, Konno S, and Sunagawa K. Sympathoinhibition induced by centrally administered atorvastatin is associated with alteration of NAD(P)H and Mn superoxide dismutase activity in rostral ventrolateral medulla of stroke-prone spontaneously hypertensive rats. J Cardiovasc Pharmacol 55: 184-190, 2010.
88. Kishi T, Hirooka Y, Sakai K, Shigematsu H, Shimokawa H, and Takeshita A. Overexpression of eNOS in the RVLM causes hypotension and bradycardia via GABA release. Hypertension 38: 896-901, 2001.
89. Kishi T, Hirooka Y, Shimokawa H, Takeshita A, and Sunagawa K. Atorstatin reduces oxidative stress in the rostral ventrolateral medulla of stoke-prone spontaneously hypertensive rats. Clin Exp Hypertens 30: 3-11, 2008.
90. Kishi T, Hirooka Y, and Sunagawa K. Sympathoinhibition caused by orally administered telmisartan through inhibition of the AT(1) receptor in the rostral ventrolateral medulla of hypertensive rats. Hypertens Res 35: 940-946, 2012.
91. Koga Y, Hirooka Y, Araki S, Nozoe M, Kishi T, and Sunagawa K. High salt intake enhances blood pressure increase during development of hypertension via oxidative stress in rostral ventrolateral medulla of spontaneously hypertensive rats. Hypertens Res 31: 2075-2083, 2008.
92. Konno S, Hirooka Y, Araki S, Koga Y, Kishi T, and Sunagawa K. Azelnidipine decreases sympathetic nerve activity via antioxidant effect in the rostral ventrolateral medulla of stroke-prone spontaneously hypertensive rats. J Cardiovasc Pharmacol 52: 555-560, 2008.
93. Kumagai H, Oshima N, Matsuura T, Iigaya K, Imai M, Onimaru H, Sakata K, Osaka M, Onami T, Takimoto C, Kamayachi T, Itoh H, and Saruta T. Importance of rostral ventrolateral medulla neurons in determining efferent sympathetic nerve activity and blood pressure. Hypertens Res 35: 132-141, 2012.
94. Kung LC, Chan SHH, Wu KLH, Ou CC, Tai MH, and Chan JYH. Mitochondrial respiratory enzyme complexes in rostral ventrolateral medulla as cellular targets of nitric oxide and superoxide interaction in the antagonism of antihypertensive action of eNOS transgene. Mol Pharmacol 74: 1319-1332, 2008.
95. Laufs U, Le Fata V, Plutzky J, and Liao JK. Upregulation of endothelial nitric oxide synthase by HMG CoA reductases inhibitors. Circulation 97: 1129-1135, 1998.
96. Lawrence AJ and Jarrott B. Nitric oxide increases interstitial excitatory amino acid release in the rat dorsomedial medulla oblongata. Neurosci Lett 151: 126-129, 1993.
97. Li P, Zhang F, Zhou YB, Cui BP, and Han Y. Superoxide anions modulate the effects of angiotensin-(1-7) in the rostral ventrolateral medulla on cardiac sympathetic afferent reflex and sympathetic activity in rats. Neuroscience 223: 388-398, 2012.
98. Li Z, Chapleau MW, Bates JN, Bielefeldt K, Lee HC, and Abboud FM. Nitric oxide as an autocrine regulator of sodium currents in baroreceptor neurons. Neuron 20: 1039-1049, 1998.
99. Li Z, Iwai M, Wu L, Shiuchi T, Jinno T, Cui TX, and Horiuchi M. Role of AT2 receptor in the brain in regulation of blood pressure and water intake. Am J Physiol Heart Circ Physiol 284: H116-H121, 2003.
100. Liao JK and Laufs U. Pleiotropic effect of statins. Annu Rev Pharmacol Toxicol 45: 89-118, 2005.
101. Lin HC, Wan FJ, Cheng KK, and Tseng CJ. Nitric oxide signaling pathway mediates the L-Arginine-induced cardiovascular effects in the nucleus tractus solitarii of rats. Life Sci 65: 2439-2451, 1999.
102. Lin HC, Wan FJ, and Tseng CJ. Modulation of cardiovascular effects produced by nitric oxide and ionotropic glutamate receptor interaction in the nucleus tractus solitarii of rats. Neuropharmacology 38: 935-941, 1999.
103. Lin LH, Taktakishvili O, and Talman WT. Identification and localization of cell types that express endothelial and neuronal nitric oxide synthase in the rat nucleus tractus solitarii. Brain Res 1171: 42-51, 2007.
104. Logan EM, Aileru AA, Shaltout HA, Averill DB, and Diz DI. The functional role of PI3K in maintenance of blood pressure and baroreflex suppression in (mRen2)27 and mRen2.Lewis rat. J Cardiovasc Pharmacol 58: 367-373, 2011.
105. Ma S, Abboud FM, and Felder RB. Effects of L-Argininederived nitric oxide synthesis on neuronal activity in nucleus tractus solitarius. Am J Physiol 268: R487-R491, 1995.
106. Machado BH. Neurotransmission of the cardiovascular reflexes in the nucleus tractus solitarii of awake rats. Ann N Y Acad Sci 940: 179-196, 2001.
107. Malpas SC. Sympathetic nervous system overactivity and its role in the development of cardiovascular disease. Physiol Rev 90: 513-557, 2010.
108. Martnez-Ruiz A, Cadenas S, and Lamas S. Nitric oxide signaling: classical, less classical, and nonclassical mechanisms. Free Radic Biol Med 51: 17-29, 2011.
109. Martins-Pinge MC, Baraldi-Passy I, and Lopes OU. Excitatory effects of nitric oxide within the rostral ventrolateral medulla of freely moving rats. Hypertension 30: 704-707, 1997.
110. Martins-Pinge MC, Garcia MR, Zoccal DB, Crestani CC, and Pinge-Filho P. Differential influence of iNOS and nNOS inhibitors on rostral ventrolateral medullary mediated cardiovascular control in conscious rats. Auton Neurosci 131: 65-69, 2007.
111. Ma?ximo Cardoso L, de Almeida Colombari DS, Vanderlei Menani J, Alves Chianca D Jr., and Colombari E. Cardiovascular responses produced by central injection of hydrogen peroxide in conscious rats. Brain Res Bull 71: 37-44, 2006.
112. Mayorov DN. Selective sensitization by nitric oxide of sympathetic baroreflex in rostral ventrolateral medulla of conscious rabbits. Hypertension 45: 901-906, 2005.
113. Mayorov DN, Head GA, and De Matteo R. Tempol attenuates excitatory actions of angiotensin II in the rostral ventrolateral medulla during emotional stress. Hypertension 44: 101-106, 2004.
114. Montezano AC and Touyz RM. Reactive oxygen species and endothelial function-role of nitric oxidase synthase uncoupling and Nox family nicotinamide adenine dinucleotide phosphate oxidase. Basic Clin Pharamcol Toxicol 110: 87-94, 2012.
115. Morrison SF, Milner TA, and Reis DJ. Reticulospinal vasomotor neurons of the rat rostral ventrolateral medulla: relationship to sympathetic nerve activity and the C1 adrenergic cell group. J Neurosci 8: 1286-1301, 1988.
116. Nishihara M, Hirooka Y, Matsukawa R, Kishi T, and Sunagawa K. Oxidative stress in the rostral ventrolateral medulla modulates excitatory and inhibitory inputs in spontaneously hypertensive rats. J Hypertens 30: 97-106, 2012.
117. Nishimura Y, Ito T, Hoe K-L, and Saavedra JM. Chronic peripheral administration of the angiotensin II AT1 receptor antagonist candesartan blocks brain AT1 receptors. Brain Res 871: 29-38, 2000.
118. Nozoe M, Hirooka Y, Koga Y, Araki S, Konno S, Kishi T, Ide T, and Sunagawa K. Mitochondria-derived reactive oxygen species mediate sympathoexcitation induced by angiotensin II in the rostral ventrolateral medulla. J Hypertens 26: 2176-2184, 2008.
119. Nozoe M, Hirooka Y, Koga Y, Sagara Y, Kishi T, Engelhardt JF, and Sunagawa K. Inhibition of Rac1-derived reactive oxygen species in nucleus tractus solitarius decreases blood pressure and heart rate in stroke-prone spontaneously hypertensive rats. Hypertension 50: 62-68, 2007.
120. Ogawa K, Hirooka Y, Shinohara K, Kishi T, and Sunagawa K. Inhibition of oxidative stress in rostral ventrolateral medulla improves impaired baroreflex sensitivity in strokeprone spontaneously hypertensive rats. Int Heart J 53: 193-198, 2012.
121. Oliveira-Sales EB, Nishi EE, Carillo BA, Boim MA, Dolnikoff MS, Bergamaschi CT, and Campos RR. Oxidative stress in the sympathetic premotor neurons contributes to sympathetic activation in renovascular hypertension. Am J Hypertens 22: 484-492, 2009.
122. Pannu R and Singh I. Pharmacological strategies for the regulation of inducible nitric oxidase synthase: neurogenerative versus neuroprotective mechanisms. Neurochem Intl 49: 170-182, 2006.
123. Park JH, Kim BH, Park SJ, Jin JK, Jeon YC, Wen GY, Shin HY, Carp RI, and Kim YS. Association of endothelial nitric oxide synthase and mitochondrial dysfunction in the hippocampus of scrapie-infected mice. Hippocampus 21: 319-333, 2011.
124. Patel KP, Mayhan WG, Bidasee KR, and Zheng H. Enhanced angiotensin II-mediated central sympathoexcitation in streptozotocin-induced diabetes: role of superoxide anion. Am J Physiol Regul Integr Comp Physiol 300: R311-R320, 2011.
125. Paton JF, Deuchars J, Ahmad Z, Wong LF, Murphy D, and Kasparov S. Adenoviral vector demonstrates that angiotensin II-induced depression of the cardiac baroreflex is mediated by endothelial nitric oxide synthase in the nucleus tractus solitarii of the rat. J Physiol (Lond) 531: 2-58, 2001.
126. Paton JFR and Kasparov S. Differential effects of angiotensin II on cardiorespiratory reflexes mediated by nucleus tractus solitarii-A microinjection study in the rat. J Physiol (Lond) 521: 213-225, 1999.
127. Paton JF, Lonergan T, Deuchars J, James PE, and Kasparov S. Detection of angiotensin II mediated nitric oxide release within the nucleus of the solitary tract using electronparamagnetic resonance (EPR) spectroscopy. Auton Neurosci 126: 193-201, 2006.
128. Paton JF, Waki H, Abdala AP, Dickinson J, and Kasparov S. Vascular-brain signaling in hypertension: role of angiotensin II and nitric oxide. Curr Hypertens Rep 9: 242-247, 2007.
129. Peterson JR, Shrama RV, and Davisson RL. Reactive oxygen species in the neuropathogenesis of hypertension. Curr Hypertens Rep 8: 232-241, 2006.
130. Plochocka-Zulinska D, and Krukoff TL. Increased gene expression of neuronal nitric oxide synthase in brain of adult spontaneously hypertensive rats. Brain Res Mol Brain Res 48: 291-297, 1997.
131. Powers-Martin K, Barron AM, Auckland CH, McCooke JK, McKitrick DJ, Arnolda LF, and Phillips JK. Immunohistochemical assessment of cyclic guanosine monophosphate (cGMP) and soluble guanylate cyclase (sGC) within the rostral ventrolateral medulla. J Biomed Sci 15: 801-812, 2008.
132. Qadri F, Arens T, Schwarz EC, Ha?user W, Dendorfer A, and Dominiak P. Brain nitric oxide synthase activity in spontaneously hypertensive rats during the development of hypertension. J Hypertens 21: 1687-1694, 2003.
133. Qadri F, Carretero OA, and Scicli AG. Centrally produced neuronal nitric oxide in the control of baroreceptor reflex sensitivity and blood pressure in normotensive and spontaneously hypertensive rats. Jpn J Pharmacol 81: 279-285, 1999.
134. Riobo NA, Melani M, Sanjuan N, Fiszman ML, Gravielle MC, Carreras MC, Cadenas E, and Poderoso JJ. The modulation of mitochondrial nitric-oxide synthase activity in rat brain development. J Biol Chem 277: 42447-42455, 2002.
135. Roman G, Dovinova I, and Chan JYH. Approaches in gene therapy of cancer and cardiovascular diseases. In: Gene Therapy Applications, edited by Chunsheng, K. Rijeka, Croatia: InTech, 2011, pp. 59-84.
136. Rosenbaugh EG, Roat JW, Gao L, Yang RF, Manickam DS, Yin JX, Schultz HD, Bronich TK, Batrakova EV, Kabanov AV, Zucker IH, and Zimmerman MC. The attenuation of central angiotensin II-dependent pressor response and intra-neuronal signaling by intracarotid injection of nanoformulated copper/zinc superoxide dismutase. Biomaterials 31: 5218-5226, 2010.
137. Ross CA, Ruggiero DA, Park DH, Joh TH, Sved AF, Fernandez-Pardal J, Saavedra JM, and Reis DJ. Tonic vasomotor control by the rostral ventrolateral medulla: effect of electrical or chemical stimulation of the area containing C1 adrenaline neurons on arterial pressure, heart rate, and plasma catecholamines and vasopressin. J Neurosci 4: 74-94, 1984.
138. Saheki A, Terasaki T, Tamai I, and Tsuji A. In vivo and in vitro blood-brain barrier transport of 3-hydroxy-3-methylglutaryl coenzyme A (HMG-CoA) reductase inhibitors. Pharm Res 11: 305-311, 1994.
139. Sakai K, Hirooka Y, Matsuo I, Eshima K, Shigematsu H, Shimokawa H, and Takeshita A. Overexpression of eNOS in NTS causes hypotension and bradycardia in vivo. Hypertension 36: 1023-1028, 2000.
140. Santhanam AV, d?Uscio LV, Smith LA, and Katusic ZS. Uncoupling of eNOS causes superoxide anion production and impairs NO signaling in the cerebral microvessels of hph-1 mice. J Neurochem 122: 1211-1218, 2012.
141. Sapru HN. Carotid chemoreflex. Neural pathways and transmitters. Adv Exp Med Biol 410: 357-364, 1996.
142. Seltzer A, Bregonzio C, Armando I, Baiardi G, and Saavedra JM. Oral administration of an AT1 receptor antagonist prevents the central effects of angiotensin II in spontaneously hypertensive rats. Brain Res 1028: 9-18, 2004.
143. Shi P, Diez-Freire C, Jun JY, Qi Y, Katovich MJ, Li Q, Sriramula S, Francis J, Sumners C, and Raizada MK. Brain microglial cytokines in neurogenic hypertension. Hypertension 56: 297-303, 2010.
144. Shih CD, Chan SHH, and Chan JYH. Participation of Fos protein at the nucleus tractus solitarius in inhibitory modulation of baroreceptor reflex response in the rat. Brain Res 738: 39-47, 1996.
145. Shih CD and Chuang YC. Nitric oxide and GABA mediate bi-directional cardiovascular effects of orexin in the nucleus tractus solitarii of rats. Neuroscience 149: 625-635, 2007.
146. Shinohara K, Hirooka Y, Kishi T, and Sunagawa K. Reduction of nitric oxide-mediated c-Amino butyric acid release in rostral ventrolateral medulla is involved in superoxide-induced sympathoexcitation of hypertensive rats. Circ J 76: 2814-2821, 2012.
147. SumbalovaZ, KucharskaJ, and Kristek F. Losartan improved respiratory function and coenzyme Q content in brain mitochondria of young spontaneously hypertensive rats. Cell Mol Neurobiol 30: 751-758, 2010.
148. Sun C, Sumners C, and Raizada MK. Chronotropic action of angiotensin II in neurons via protein kinase C and CaMKII. Hypertension 39: 562-566, 2002.
149. Sun C, Sellers KW, Sumners C, and Raizada MK. NADPH oxidase inhibition attenuates neuronal chronotropic actions of angiotensin II. Circ Res 96: 659-666, 2005.
150. Sun J, Druhan LJ, and Zweier JL. Reactive oxygen and nitrogen species regulate inducible nitric oxide synthase function shifting the balance of nitric oxide and superoxide production. Arch Biochem Biophys 494: 130-137, 2010.
151. Tagawa T, Horiuchi J, Potts PD, and Dampney RA. Sympathoinhibition after angiotensin receptor blockade in the rostral ventrolateral medulla is independent of glutamate and gamma-Aminobutyric acid receptors J Auton Nerv Syst 77: 21-30, 1999.
152. Tai MH, Hsiao M, Chan JYH, Lo WC, Wang FS, Liu GS, Howng SL, and Tseng CJ. Gene delivery of endothelial nitric oxide synthase into nucleus tractus solitarii induces biphasic response in cardiovascular functions of hypertensive rats. Am J Hypertens 17: 63-70, 2004.
153. Tai MH, Wang LL, Wu KL, and Chan JYH. Increased superoxide anion in rostral ventrolateral medulla contributes to hypertension in spontaneously hypertensive rats via interactions with nitric oxide. Free Radic Biol Med 38: 450-462, 2005.
154. Talman WT and Dragon DN. Transmission of arterial baroreflex signals depends on neuronal nitric oxide synthase. Hypertension 43: 820-824, 2004.
155. Topel I, Stanarius A, and Wolf G. Distribution of the endothelial constitutive nitric oxide synthase in the developing rat brain: an immunohistochemical study. Brain Res 788: 43-48, 1998.
156. Touyz RM and Briones AM. Reactive oxygen species and vascular biology: implications in human hypertension. Hypertens Res 34: 5-14, 2011.
157. Tsujimoto I, Hikoso S, Yamaguchi O, Kashiwase K, Nakai A, Takeda T, Watanabe T, Taniike M, Matsumura Y, Nishida K, Hori M, Kogo M, and Otsu K. The antioxidant edaravone attenuates pressure overload-induced left ventricular hypertrophy. Hypertension 45: 921-926, 2005.
158. Veerasingham SJ, Yamazato M, Berecek KH, Wyss JM, and Raizada MK. Increased PI3-kinase in presympathetic brain areas of the spontaneously hypertensive rat. Circ Res 96: 277-279, 2005.
159. Vickers C, Hales P, Kaushik V, Dick L, Gavin J, Tang J, Godbout K, Parsons T, Baronas E, Hsieh F, Acton S, Patane M, Nichols A, and Tummino P. Hydrolysis of biological peptides by human angiotensin-converting enzyme-related carboxypeptidase. J Biol Chem 277: 148381-14843, 2002.
160. Waki H, Kasparov S, Wong LF, Murphy D, Shimizu T, and Paton JF. Chronic inhibition of endothelial nitric oxide synthase activity in nucleus tractus solitarii enhances baroreceptor reflex in conscious rats. J Physiol (Lond.) 546: 1-42, 2003.
161. Waki H, Murphy D, Yao ST, Kasparov S, and Paton JF. Endothelial NO synthase activity in nucleus tractus solitarii contributes to hypertension in spontaneously hypertensive rats. Hypertension 48: 644-650, 2006.
162. Wang G, Anrather J, Huang J, Speth RC, Pickel VM, and Iadecola C. NADPH oxidase contributes to angiotensin II signaling in the nucleus tractus solitarius. J Neurosci 24: 5516-5524, 2004.
163. Wang G, Anrather J, Glass MJ, Tarsitano MJ, Zhou P, Frys KA, Pickel VM, and Iadecola C. Nox2, Ca2 + , and protein kinase C play a role in angiotensin II-induced free radical production in nucleus tractus solitarius. Hypertension 48: 482-489, 2006.
164. Wang G, Coleman CG, Glass MJ, Zhou P, Yu Q, Park L, Anrather J, Pickel VM, and Iadecola C. Angiotensin II type 2 receptor-coupled nitric oxide production modulates free radical availability and voltage-gated Ca2 + currents in NTS neurons. Am J Physiol Regul Integr Comp Physiol 302: R1076-R1083, 2012.
165. Wang LL, Chan SHH, and Chan JYH. Fos protein is required for the re-expression of angiotensin subtype 1 receptors in the nucleus tractus solitarii after baroreceptor activation in the rat. Neuroscience 103: 143-151, 2001.
166. Wang S, Paton JF, and Kasparov S. Differential sensitivity of excitatory and inhibitory synaptic transmission to modulation by nitric oxide in rat nucleus tractus solitarii. Exp Physiol 92: 371-382, 2007.
167. Wang S, Teschemacher AG, Paton JF, and Kasparov S. Mechanism of nitric oxide action on inhibitory GABAergic signaling within the nucleus tractus solitarii. FASEB J 20: 1537-1739, 2006.
168. Wang Y, Patel KP, Cornish KG, Channon KM, and Zucker IH. nNOS gene transfer to RVLM improves baroreflex function in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 285: H1660-H1667, 2003.
169. Wei SG, Zhang ZH, Yu Y, and Felder RB. Systemically administered tempol reduces neuronal activity in paraventricular nucleus of hypothalamus and rostral ventrolateral medulla in rats. J Hypertens 27: 543-550, 2009.
170. Wu KLH, Chan SHH, and Chan JYH. Neuroinflammation and oxidative stress in rostral ventrolateral medulla contribute to neurogenic hypertension induced by systemic inflammation. J Neuroinflam 9: 212, 2012.
171. Wu KLH, Wu CA, Wu CW, Chan SHH, Chang AYH, and Chan JYH. Redox-sensitive oxidation and phosphorylation of PTEN contribute to enhanced activation of PI3K/Akt signaling in rostral ventrolateral medulla and neurogenic hypertension in spontaneously hypertensive rats. Antioxid Redox Signal 18: 36-50, 2013.
172. Xia H and Lazartigues E. Angiotensin-converting enzyme 2: central regulator for cardiovascular function. Curr Hypertens Rep 12: 170-175, 2010.
173. Xia H, Suda S, Bindom S, Feng Y, Gurley SB, Seth D, Navar LG, and Lazartigues E. ACE2-mediated reduction of oxidative stress in the central nervous system is associated with improvement of autonomic function. PLoS One 6: e22682, 2011.
174. Yamazato M, Yamazato Y, Sun C, Diez-Freire C, and Raizada MK. Overexpression of angiotensin-converting enzyme 2 in the rostral ventrolateral medulla causes longterm decrease in blood pressure in the spontaneously hypertensive rats. Hypertension 49: 926-931, 2007.
175. Yen DH, Chen LC, Shen YC, Chiu YC, Ho IC, Lou YJ, Chen IC, and Yen JC. Protein kinase A-dependent neuronal nitric oxide synthase activation mediates the enhancement of baroreflex response by adrenomedullin in the nucleus tractus solitarii of rats. J Biomed Sci 18: 32, 2011.
176. Yi X, Zimmerman MC, Yang R, Tong J, Vinogradov S, and Kabanov AV. Pluronic-modified superoxide dismutase 1 attenuates angiotensin II-induced increase in intracellular superoxide in neurons. Free Radic Biol Med 49: 548-558, 2010.
177. Yu Y, Zhang ZH, Wei SG, Serrats J, Weiss RM, and Felder RB. Brain perivascular macrophages and the sympathetic response to inflammation in rats after myocardial infarction. Hypertension 55: 652-659, 2010.
178. Zada?k Z, Hyspler R, TichaA, Hronek M, FikrovaP, RathouskaJ, HrnciarikovaD, and Stetina R. Antioxidants and vitamins in clinical conditions. Physiol Res 58: 13-17, 2009.
179. Zalba G, Fortuno A, San JoseG, Moreno MU, Beloqui O, and Dez J. Oxidative stress, endothelial dysfunction and cerebrovascular disease. Cerebrovasc Dis 24: 24-29, 2007.
180. Zanzinger J. Mechanisms of action of nitric oxide in the brain stem: role of oxidative stress. Auton Neurosci 98: 24-27, 2002.
181. Zanzinger J and Czachurski J. Chronic oxidative stress in the RVLM modulates sympathetic control of circulation in pigs. Pflugers Arch 439: 489-494, 2000.
182. Zhang ZH, Yu Y, Wei SG, and Felder FB. Centrally administered lipopolysaccharide elicits sympathetic excitation via NAD(P)H oxidase-dependent mitogen-Activated protein kinase signaling. J Hypertens 28: 806-846, 2010.
183. Zhong MK, Gao J, Zhang F, Xu B, Fan ZD, Wang W, and Zhu GQ. Reactive oxygen species in rostral ventrolateral medulla modulate cardiac sympathetic afferent reflex in rats. Acta Physiol (Oxf ) 197: 297-304, 2009.
184. Zimmerman MC and Davisson RL. Redox signaling in central neural regulation of cardiovascular function. Prog Biophys Mol Biol 84: 125-149, 2004.
185. Zimmerman MC, Dunlay RP, Lazartigues E, Zhang Y, Sharma RV, Engelhardt JF, and Davisson RL. Requirement for rac1-dependent NADPH oxidase in the cardiovascular and dipsogenic actions of angiotensin II in the brain. Circ Res 95: 532-539, 2004.
186. Zimmerman MC, Lazartigues E, Lang JA, Sinnayah P, Ahmad IM, Spitz DR, and Davission RL. Superoxide mediates the action of angiotensin II in the central nervous system. Circ Res 91: 1038-1045, 2002.
187. Zimmerman MC, Sharma RV, and Davisson RL. Superoxide mediates angiotensin II-induced influx of extracellular calcium in neural cells. Hypertension 45: 717-723, 2005.
188. Zimmerman MC and Zucker IH. Mitochondrial dysfunction and mitochondrial-produced reactive oxygen species: new targets for neurogenic hypertension? Hypertension 53: 112-114, 2009.
189. Zubcevic J, Waki H, Raizada MK, and Paton JF. Autonomic-immune-vascular interaction: an emerging concept for neurogenic hypertension. Hypertension 57: 1026-1033, 2011.
190. Zucker IH, Schultz HD, Patel KP, Wang W, and Gao L. Regulation of central angiotensin type 1 receptors and sympathetic outflow in heart failure. Am J Physiol Heart Circ Physiol 297: H1557-H1566, 2009.