Redox signaling in central neural regulation of cardiovascular function

Progress in Biophysics and Molecular Biology

Volumn 84, Issue 2-3, 2004, Pages 125-149

  Zimmerman, Matthew C ^a,b   Davisson, Robin L ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

CNS; Free radicals; NAD(P)H oxidase; Renin angiotensin system; Superoxide dismutase

Indexed keywords

EID: 1242321407     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2003.11.009     Document Type: Review

References (162)

1. Alisky J.M., Hughes S.M., Sauter S.L., Jolly D., Dubensky T.W. Jr., Staber P.D., Chiorini J.A., Davidson B.L. Transduction of murine cerebellar neurons with recombinant FIV and AAV5 vectors. Neuroreport. 11:2000;2669-2673.
2. 1 receptors. Am. J. Hypertens. 13:2000;31S-38S.
3. Bains J.S., Ferguson A.V. Angiotensin II neurotransmitter actions in paraventricular nucleus are potentiated by a nitric oxide synthase inhibitor. Regul. Pept. 50:1994;53-59.
4. Bains J.S., Ferguson A.V. Nitric oxide regulates NMDA-driven GABAergic inputs to type I neurones of the rat paraventricular nucleus. J. Physiol. 499:1997;733-746.
5. Bauersachs J., Bouloumie A., Fraccarollo D., Hu K., Busse R., Ertl G. Endothelial dysfunction in chronic myocardial infarction despite increased vascular endothelial nitric oxide synthase and soluble guanylate cyclase expression. role of enhanced vascular superoxide production Circulation. 100:1999;292-298.
6. Beyer W., Imlay J., Fridovich I. Superoxide dismutases. Prog. Nucleic Acid Res. Mol. Biol. 40:1991;221-253.
7. - forming NADPH oxidase in microglia, monocytes, and neutrophils. A possible inflammatory mechanism of neuronal damage in Alzheimer's disease. J. Biol. Chem. 274:1999;15493-15499.
8. Blomer U., Naldini L., Kafri T., Trono D., Verma I.M., Gage F.H. Highly efficient and sustained gene transfer in adult neurons with a lentivirus vector. J. Virol. 71:1997;6641-6649.
9. Bunnemann B., Fuxe K., Ganten D. The renin-angiotensin system in the brain. an update Regul. Pept. 46:1993;487-509.
10. Butterfield D.A., Kanski J. Brain protein oxidation in age-related neurodegenerative disorders that are associated with aggregated proteins. Mech. Ageing Dev. 122:2001;945-962.
11. Cai H., Harrison D.G. Endothelial dysfunction in cardiovascular diseases. the role of oxidant stress Circ. Res. 87:2000;840-844.
12. Carmody R.J., Cotter T.G. Signalling apoptosis. a radical approach Redox Rep. 6:2001;77-90.
13. Chabrashvili T., Tojo A., Onozato M.L., Kitiyakara C., Quinn M.T., Fujita T., Welch W.J., Wilcox C.S. Expression and cellular localization of classic NADPH oxidase subunits in the spontaneously hypertensive rat kidney. Hypertension. 39:2002;269-274.
14. Chandel N.S., Schumacker P.T., Arch R.H. Reactive oxygen species are downstream products of TRAF-mediated signal transduction. J. Biol. Chem. 276:2001;42728-42736.
15. Chapleau M.W., Abboud F.M. Neuro-cardiovascular regulation. from molecules to man Ann. N.Y. Acad. Sci. 940:2001;xiii-xxii.
16. + channel blocker 4-aminopyridine J. Physiol. 462:1993;291-306.
17. Chowdhary S., Townend J.N. Role of nitric oxide in the regulation of cardiovascular autonomic control. Clin. Sci. 97:1999;5-17.
18. Cohen G. Enzymatic/nonenzymatic sources of oxyradicals and regulation of antioxidant defenses. Ann. N.Y. Acad. Sci. 738:1994;8-14.
19. Dampney R.A. Functional organization of central pathways regulating the cardiovascular system. Physiol. Rev. 74:1994;323-364.
20. Davidson B.L., Allen E.D., Kozarsky K.F., Wilson J.M., Roessler B.J. A model system for in vivo gene transfer into the central nervous system using an adenoviral vector. Nat. Gene. 3:1993;219-223.
21. Davisson R.L., Yang G.Y., Beltz T.G., Cassell M.D., Johnson A.K., Sigmund C.D. The brain renin-angiotensin system contributes to the hypertension in mice containing both the human renin and human angiotensinogen transgenes. Circ. Res. 83:1998;1047-1058.
22. Day B.J., Shawen S., Liochev S.I., Crapo J.D. A metalloporphyrin superoxide dismutase mimetic protects against paraquat-induced endothelial cell injury, in vitro. J. Pharmacol. Exp. Therap. 275:1995;1227-1232.
23. Deng H.X., Hentati A., Tainer J.A., Iqbal Z., Cayabyab A., Hung W.Y., Getzoff E.D., Hu P., Herzfeldt B., Roos R.P. Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase. Science. 261:1993;1047-1051.
24. DiBona G.F., Jones S.Y., Brooks V.L. ANG II receptor blockade and arterial baroreflex regulation of renal nerve activity in cardiac failure. Am. J. Physiol. 269:1995;R1189-R1196.
25. DiBona G.F., Jones S.Y., Sawin L.L. Angiotensin receptor antagonist improves cardiac reflex control of renal sodium handling in heart failure. Am. J. Physiol. 274:1998;H636-H641.
26. Doctrow S.R., Huffman K., Marcus C.B., Musleh W., Bruce A., Baudry M., Malfroy B. Salen-manganese complexes. combined superoxide dismutase/catalase mimics with broad pharmacological efficacy Adv. Pharmacol. 38:1997;247-269.
27. Edgley A., Kett M., Anderson W. 'Slow pressor' hypertension from low-dose chronic angiotensin II infusion. Clin. Exp. Pharmacol. Physiol. 28:2001;1035-1039.
28. Felder R.B., Francis J., Zhang Z.H., Wei S.G., Weiss R.M., Johnson A.K. Heart failure and the brain. new perspectives Am. J. Physiol. Regul. Integrat. Comp. Physiol. 284:2003;R259-R276.
29. Francis G.S. The relationship of the sympathetic nervous system and the renin-angiotensin system in congestive heart failure. Am. Heart J. 118:1989;642-648.
30. Fukai T., Siegfried M.R., Ushio-Fukai M., Griendling K.K., Harrison D.G. Modulation of extracellular superoxide dismutase expression by angiotensin II and hypertension. Circ. Res. 85:1999;23-28.
31. Fukui T., Ishizaka N., Rajagopalan S., Laursen J.B., Capers Q., Taylor W.R., Harrison D.G., de Leon H., Wilcox J.N., Griendling K.K. p22phox mRNA expression and NADPH oxidase activity are increased in aortas from hypertensive rats. Circ. Res. 80:1997;45-51.
32. Ganong W.F. Circumventricular organs. definition and role in the regulation of endocrine and autonomic function Clin. Exp. Pharmacol. Physiol. 27:2000;422-427.
33. Geiszt M., Kopp J.B., Varnai P., Leto T.L. Identification of renox, an NAD(P)H oxidase in kidney. Proc. Natl. Acad. Sci. USA. 97:2000;8010-8014.
34. Gheorghiade M., Bonow R.O. Chronic heart failure in the United States. a manifestation of coronary artery disease Circulation. 97:1998;282-289.
35. Giasson B.I., Ischiropoulos H., Lee V.M., Trojanowski J.Q. The relationship between oxidative/nitrative stress and pathological inclusions in Alzheimer's and Parkinson's diseases. Free Radic. Biol. Med. 32:2002;1264-1275.
36. Gorlach A., Brandes R.P., Nguyen K., Amidi M., Dehghani F., Busse R. A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ. Res. 87:2000;26-32.
37. Griendling K.K., Minieri C.A., Ollerenshaw J.D., Alexander R.W. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ. Res. 74:1994;1141-1148.
38. Griendling K.K., Sorescu D., Ushio-Fukai M. NAD(P)H oxidase. role in cardiovascular biology and disease Circ. Res. 86:2000;494-501.
39. Griendling K.K., Ushio-Fukai M. Reactive oxygen species as mediators of angiotensin II signaling. Regul. Pept. 91:2000;21-27.
40. Hanna I.R., Taniyama Y., Szocs K., Rocic P., Griendling K.K. NAD(P)H oxidase-derived reactive oxygen species as mediators of angiotensin II signaling. Antioxidants Redox Signal. 4:2003;899-914.
41. Hannken T., Schroeder R., Stahl R.A., Wolf G. Angiotensin II-mediated expression of p27Kip1 and induction of cellular hypertrophy in renal tubular cells depend on the generation of oxygen radicals. Kidney Int. 54:1998;1923-1933.
42. Harrison D.G., Cai H., Landmesser U., Griendling K.K. Interactions of angiotensin II with NAD(P)H oxidase, oxidant stress and cardiovascular disease. J. Renin Angiotensin Aldosterone Syst. 4:2003;51-61.
43. Harrison D.G., Griendling K.K., Landmesser U., Hornig B., Drexler H. Role of oxidative stress in atherosclerosis. Am. J. Cardiol. 91:2003;7A-11A.
44. Hensley K., Carney J.M., Mattson M.P., Aksenova M., Harris M., Wu J.F., Floyd R.A., Butterfield D.A. A model for beta-amyloid aggregation and neurotoxicity based on free radical generation by the peptide. relevance to Alzheimer disease Proc. Natl. Acad. Sci. USA. 91:1994;3270-3274.
45. Hu L., Zhu D.N., Yu Z., Wang J.Q., Sun Z.J., Yao T. Expression of angiotensin II type 1(AT(1)) receptor in the rostral ventrolateral medulla in rats. J. Appl. Physiol. 92:2002;2153-2161.
46. Imboden H., Harding J.W., Felix D. Hypothalamic angiotensinergic fibre systems terminate in the neurohypophysis. Neurosci. Lett. 96:1989;42-46.
47. Inagaki S., Takagi H., Suzuki K., Akai F., Taniguchi N. Intense immunoreactivity for Mn-superoxide dismutase (Mn-SOD) in cholinergic and non-cholinergic neurons in the rat basal forebrain. Brain Res. 541:1991;354-357.
48. 2+ and sustained opening of the permeability transition pore. J. Cell Sci. 115:2002;1175-1188.
49. Jang J.H., Surh Y.J. Beta-amyloid induces oxidative DNA damage and cell death through activation of c-Jun N terminal kinase. Ann. N.Y. Acad. Sci. 973:2002;228-236.
50. Jenner P., Olanow C.W. Oxidative stress and the pathogenesis of Parkinson's disease. Neurology. 47:1996;S161-S170.
51. Jeremy J.Y., Yim A.P., Wan S., Angelini G.D. Oxidative stress, nitric oxide, and vascular disease. J. Cardiac Surg. 17:2002;324-327.
52. Jhamandas J.H., Lind R.W., Renaud L.P. Angiotensin II may mediate excitatory neurotransmission from the subfornical organ to the hypothalamic supraoptic nucleus. an anatomical and electrophysiological study in the rat Brain Res. 487:1989;52-61.
53. Johnson A.K., Gross P.M. Sensory circumventricular organs and brain homeostatic pathways. FASEB J. 7:1993;678-686.
54. Johnson A.K., Thunhorst R.L. The neuroendocrinology of thirst and salt appetite. visceral sensory signals and mechanisms of central integration Front. Neuroendocrinol. 18:1997;292-353.
55. Jones S.A., O'Donnell V.B., Wood J.D., Broughton J.P., Hughes E.J., Jones O.T. Expression of phagocyte NADPH oxidase components in human endothelial cells. Am. J. Physiol. 271:1996;H1626-H1634.
56. Kato H., Kogure K., Araki T., Liu X.H., Kato K., Itoyama Y. Immunohistochemical localization of superoxide dismutase in the hippocampus following ischemia in a gerbil model of ischemic tolerance. J. Cereb. Blood Flow Metab. 15:1995;60-70.
57. Kawada N., Imai E., Karber A., Welch W.J., Wilcox C.S. A mouse model of angiotensin II slow pressor response. role of oxidative stress J. Am. Soc. Nephrol. 13:2002;2860-2868.
58. Kaye D.M., Lambert G.W., Lefkovits J., Morris M., Jennings G., Esler M.D. Neurochemical evidence of cardiac sympathetic activation and increased central nervous system norepinephrine turnover in severe congestive heart failure. J. Am. College Cardiol. 23:1994;570-578.
59. Kishi T., Hirooka Y., Sakai K., Shigematsu H., Shimokawa H., Takeshita A. Overexpression of eNOS in the RVLM causes hypotension and bradycardia via GABA release. Hypertension. 38:2001;896-901.
60. 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. 39:2002;264-268.
61. Kishi T., Hirooka Y., Kimura Y., Sakai K., Ito K., Shimokawa H., 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. 41:2003;255-260.
62. Klein J.A., Ackerman S.L. Oxidative stress, cell cycle, and neurodegeneration. J. Clin. Investig. 111:2003;785-793.
63. Kordower J.H., Bloch J., Ma S.Y., Chu Y., Palfi S., Roitberg B.Z., Emborg M., Hantraye P., Deglon N., Aebischer P. Lentiviral gene transfer to the nonhuman primate brain. Exp. 160:1999;1-16.
64. Kumanogoh H., Miyata S., Sokawa Y., Maekawa S. Biochemical and morphological analysis on the localization of Rac1 in neurons. Neurosci. Res. 39:2001;189-196.
65. La Rovere M.T., Bigger J.T. Jr., Marcus F.I., Mortara A., Schwartz P.J. Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction. ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction) Investigators. Lancet. 351:1998;478-484.
66. Landmesser U., Harrison D.G. Oxidative stress and vascular damage in hypertension. Coronary Artery Dis. 12:2001;455-461.
67. Landmesser U., Cai H., Dikalov S., McCann L., Hwang J., Jo H., Holland S.M., Harrison D.G. Role of p47(phox) in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension. 40:2002;511-515.
68. Lassegue B., Sorescu D., Szocs K., Yin Q., Akers M., Zhang Y., Grant S.L., Lambeth J.D., Griendling K.K. Novel gp91(phox) homologues in vascular smooth muscle cells. nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways Circ. Res. 88:2001;888-894.
69. Laursen J.B., Rajagopalan S., Galis Z., Tarpey M., Freeman B.A., Harrison D.G. Role of superoxide in angiotensin II-induced but not catecholamine-induced hypertension. Circulation. 95:1997;588-593.
70. Lavigne M.C., Malech H.L., Holland S.M., Leto T.L. Genetic requirement of p47phox for superoxide production by murine microglia. FASEB J. 15:2001;285-287.
71. Lazartigues E., Dunlay S.M., Loihl A.K., Sinnayah P., Lang J.A., Espelund J.J., Sigmund C.D., Davisson R.L. Brain-selective overexpression of angiotensin (AT1) receptors causes enhanced cardiovascular sensitivity in transgenic mice. Circ. Res. 90:2002;617-624.
72. Leenen F.H., Skarda V., Yuan B., White R. Changes in cardiac ANG II postmyocardial infarction in rats. effects of nephrectomy and ACE inhibitors Am. J. Physiol. 276:1999;H317-H325.
73. Lenkei Z., Corvol P., Llorens-Cortes C. The angiotensin receptor subtype AT1A predominates in rat forebrain areas involved in blood pressure, body fluid homeostasis and neuroendocrine control. Brain Res. 30:1995;53-60.
74. Lenkei Z., Palkovits M., Corvol P., Llorens-Cortes C. Expression of angiotensin type-1 (AT1) and type-2 (AT2) receptor mRNAS in the adult rat brain. a functional neuroanatomical review Front. Neuroendocrinol. 18:1997;383-439.
75. Li Z., Ferguson A.V. Angiotensin ii responsiveness of rat paraventricular and subfornical organ neurons in vitro. Neuroscience. 55:1993;197-207.
76. Li Y.F., Patel K.P. Paraventricular nucleus of the hypothalamus and elevated sympathetic activity in heart failure. the altered inhibitory mechanisms Acta Physiol. Scand. 177:2003;17-26.
77. Li Z., Mao H.Z., Abboud F.M., Chapleau M.W. Oxygen-derived free radicals contribute to baroreceptor dysfunction in atherosclerotic rabbits. Circ. Res. 79:1996;802-811.
78. Li, Z., Bates, J., Lee, H.C., Abboud, F.M., Chapleau, M.W., 1997a. Oxidation selectively inhibits tetrodotoxin-sensitive sodium currents in insolated baroreceptor neurons. Soc. Neurosci. Abstracts 23, 1519.
79. + current in aortic baroreceptor neurones of rats. J. Physiol. 501:1997;275-287.
80. Lind R.W. Bi-directional, chemically specified neural connections between the subfornical organ and the midbrain raphe system. Brain Res. 384:1986;250-261.
81. Lind R.W., Van Hoesen G.W., Johnson A.K. An HRP study of the connections of the subfornical organ of the rat. J. Comp. Neurol. 210:1982;265-277.
82. Lind R.W., Swanson L.W., Ganten D. Organization of angiotensin II immunoreactive cells and fibers in the rat central nervous system. An immunohistochemical study. Neuroendocrinology. 40:1985;2-24.
83. Lindenau J., Noack H., Asayama K., Wolf G. Enhanced cellular glutathione peroxidase immunoreactivity in activated astrocytes and in microglia during excitotoxin induced neurodegeneration. GLIA. 24:1998;252-256.
84. Lindenau J., Noack H., Possel H., Asayama K., Wolf G. Cellular distribution of superoxide dismutases in the rat CNS. GLIA. 29:2000;25-34.
85. Lindley T.E., Doobay M.F., Davisson R.L. Redox signaling is involved in central activation and sympathoexcitation during heart failure. FASEB J. 17:2003;A401.
86. Lindley, T.E., Doobay, M.F., Sharma, R.V., Davisson, R.L., 2003b. Superoxide is involved in the central nervous system activation and sympatho-excitation of myocardial infarction-induced heart failure. Circ. Res. (in press).
87. Lindley T.E., Sharma R.V., Davisson R.L. Increased superoxide scavenging in the brain improves survival and cardiac performance following myocardial infarction. Hypertension. 42:2003;390.
88. Liu J.L., Zucker I.H. Regulation of sympathetic nerve activity in heart failure. a role for nitric oxide and angiotensin II Circ. Res. 84:1999;417-423.
89. Liu X.H., Kato H., Nakata N., Kogure K., Kato K. An immunohistochemical study of copper/zinc superoxide dismutase and manganese superoxide dismutase in rat hippocampus after transient cerebral ischemia. Brain Res. 625:1993;29-37.
90. Liu J.L., Murakami H., Sanderford M., Bishop V.S., Zucker I.H. ANG II and baroreflex function in rabbits with CHF and lesions of the area postrema. Am. J. Physiol. 277:1999;H342-H350.
91. Ma S., Abboud F.M., Felder R.B. Effects of L-arginine-derived nitric oxide synthesis on neuronal activity in nucleus tractus solitarius. Am. J. Physiol. 268:1995;R487-R491.
92. Mangiapane M.L., Simpson J.B. Subfornical organ. forebrain site of pressor and dipsogenic action of angiotensin II Am. J. Physiol. 239:1980;R382-R389.
93. Matsuura T., Kumagai H., Kawai A., Onimaru H., Imai M., Oshima N., Sakata K., Saruta T. Rostral ventrolateral medulla neurons of neonatal Wistar-Kyoto and spontaneously hypertensive rats. Hypertension. 40:2002;560-565.
94. McKinley M.J., Badoer E., Vivas L., Oldfield B.J. Comparison of c-fos expression in the lamina terminalis of conscious rats after intravenous or intracerebroventricular angiotensin. Brain Res. Bull. 37:1995;131-137.
95. Melaragno M.G., Fink G.D. Enhanced slow pressor effect of angiotensin II in two-kidney, one clip rats. Hypertension. 25:1995;288-293.
96. Melov S., Schneider J.A., Day B.J., Hinerfeld D., Coskun P., Mirra S.S., Crapo J.D., Wallace D.C. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat. Genet. 18:1998;159-163.
97. Melov S., Coskun P., Patel M., Tuinstra R., Cottrell B., Jun A.S., Zastawny T.H., Dizdaroglu M., Goodman S.I., Huang T.T., Miziorko H., Epstein C.J., Wallace D.C. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc. Natl. Acad. Sci. USA. 96:1999;846-851.
98. Melov S., Ravenscroft J., Malik S., Gill M.S., Walker D.W., Clayton P.E., Wallace D.C., Malfroy B., Doctrow S.R., Lithgow G.J. Extension of life-span with superoxide dismutase/catalase mimetics. Science. 289:2000;1567-1569.
99. Meyrelles S.S., Sharma R.V., Whiteis C.A., Davidson B.L., Chapleau M.W. Adenovirus-mediated gene transfer to cultured nodose sensory neurons. Brain research. Mol. Brain Res. 51:1997;33-41.
100. Miller L.W., Missov E.D. Epidemiology of heart failure. Cardiol. Clin. 19:2001;547-555.
101. Miselis R.R. The efferent projections of the subfornical organ of the rat. a circumventricular organ within a neural network subserving water balance Brain Res. 230:1981;1-23.
102. Moreno S., Nardacci R., Ceru M.P. Regional and ultrastructural immunolocalization of copper-zinc superoxide dismutase in rat central nervous system. J. Histochem. Cytochem. 45:1997;1611-1622.
103. Morimoto S., Cassell M.D., Beltz T.G., Johnson A.K., Davisson R.L., Sigmund C.D. Elevated blood pressure in transgenic mice with brain-specific expression of human angiotensinogen driven by the glial fibrillary acidic protein promoter. Circ. Res. 89:2001;365-372.
104. Murakami H., Liu J.L., Zucker I.H. Angiotensin II blockade enhances baroreflex control of sympathetic outflow in heart failure. Hypertension. 29:1997;564-569.
105. Muratani H., Ferrario C.M., Averill D.B. Ventrolateral medulla in spontaneously hypertensive rats. role of angiotensin II Am. J. Physiol. 264:1993;R388-R395.
106. Nakagami H., Takemoto M., Liao J.K. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced cardiac hypertrophy. J. Mol. Cell. Cardiol. 35:2003;851-859.
107. Nakamura K., Fushimi K., Kouchi H., Mihara K., Miyazaki M., Ohe T., Namba M. Inhibitory effects of antioxidants on neonatal rat cardiac myocyte hypertrophy induced by tumor necrosis factor-alpha and angiotensin II. Circulation. 98:1998;794-799.
108. Noh, K.M., Koh, J.Y., 2000. Induction and activation by zinc of NADPH oxidase in cultured cortical neurons and astrocytes. J. Neurosci. 20, RC111(1-5).
109. Oury T.D., Card J.P., Klann E. Localization of extracellular superoxide dismutase in adult mouse brain. Brain Res. 850:1999;96-103.
110. 2+ and Ca(2+)-induced increase in oxidative stress. an experimental model using dissociated rat brain neurons Jpn. J. Pharmacol. 72:1996;381-385.
111. + current. role of protein kinase C-alpha Am. J. Physiol. Cell Physiol. 281:2001;C17-C23.
112. Pardo C.A., Xu Z., Borchelt D.R., Price D.L., Sisodia S.S., Cleveland D.W. Superoxide dismutase is an abundant component in cell bodies, dendrites, and axons of motor neurons and in a subset of other neurons. Proc. Natl. Acad. Sci. USA. 92:1995;954-958.
113. Patel K.P., Zhang K., Zucker I.H., Krukoff T.L. Decreased gene expression of neuronal nitric oxide synthase in hypothalamus and brainstem of rats in heart failure. Brain Res. 734:1996;109-115.
114. Paton, J.F., Kasparov, S., 1999. Differential effects of angiotensin II on cardiorespiratory reflexes mediated by nucleus tractus solitarii - a microinjection study in the rat. J. Physiol. 521 Pt 1, 213-225.
115. Paton J.F., Deuchars J., Ahmad Z., Wong L.F., Murphy D., 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. 531:2001;445-458.
116. Paton J.F.R., Kasparov S., Paterson D.J. Nitric oxide and autonomic control of heart rate. a question of specificity Trends in Neurosci. 25:2002;626-631.
117. Phillips M.I., Sumners C. Angiotensin II in central nervous system physiology. Regul. Pept. 78:1998;1-11.
118. Piccirillo G., Nocco M., Moise A., Lionetti M., Naso C., di Carlo S., Marigliano V. Influence of vitamin C on baroreflex sensitivity in chronic heart failure. Hypertension. 41:2003;1240-1245.
119. Piomelli D. Arachidonic acid in cell signaling. Curr. Opin. Cell Biol. 5:1993;274-280.
120. Poeschla E.M., Wong-Staal F., Looney D.J. Efficient transduction of nondividing human cells by feline immunodeficiency virus lentiviral vectors. Nat. Med. 4:1998;354-357.
121. Richards E.M., Raizada M.K., Gelband C.H., Sumners C. Angiotensin II type 1 receptor-modulated signaling pathways in neurons. Mol. Neurobio. 19:1999;25-41.
122. Rinckel L.A., Faris S.L., Hitt N.D., Kleinberg M.E. Rac1 disrupts p67phox/p40phox binding. a novel role for Rac in NADPH oxidase activation Biochem. Biophys. Res. Commun. 263:1999;118-122.
123. Rogers R.J., Monnier J.M., Nick H.S. Tumor necrosis factor-alpha selectively induces MnSOD expression via mitochondria-to-nucleus signaling, whereas interleukin-1 beta utilizes an alternative pathway. J. Biol. Chem. 276:2001;20419-20427.
124. Ronson R.S., Nakamura M., Vinten-Johansen J. The cardiovascular effects and implications of peroxynitrite. Cardiovasc. Res. 44:1999;47-59.
125. Rowland L.P. Amyotrophic lateral sclerosis. human challenge for neuroscience Proc. Natl. Acad. Sci. USA. 92:1995;1251-1253.
126. Saavedra J.M., Correa F.M., Kurihara M., Shigematsu K. Increased number of angiotensin II receptors in the subfornical organ of spontaneously hypertensive rats. J. Hypertens. Suppl. 4:1986;S27-S30.
127. Sakuma I., Togashi H., Yoshioka M., Saito H., Yanagida M., Tamura M., Kobayashi T., Yasuda H., Gross S.S., Levi R. NG-methyl-L-arginine, an inhibitor of L-arginine-derived nitric oxide synthesis, stimulates renal sympathetic nerve activity in vivo. A role for nitric oxide in the central regulation of sympathetic tone? Circ. Res. 70:1992;607-611.
128. Satriano J.A., Shuldiner M., Hora K., Xing Y., Shan Z., Schlondorff D. Oxygen radicals as second messengers for expression of the monocyte chemoattractant protein, JE/MCP-1, and the monocyte colony-stimulating factor, CSF-1, in response to tumor necrosis factor-alpha and immunoglobulin G. Evidence for involvement of reduced nicotinamide adenine dinucleotide phosphate (NADPH)-dependent oxidase. J. Clin. Investig. 92:1993;1564-1571.
129. Sayre L.M., Smith M.A., Perry G. Chemistry and biochemistry of oxidative stress in neurodegenerative disease. Curr. Med. Chem. 8:2001;721-738.
130. Schmid H.A., Schafer F., Simon E. Opposite effects of angiotensin II and nitric oxide on neurons in the duck subfornical organ. Neurosci. Lett. 187:1995;149-152.
131. Schnackenberg C.G., Welch W.J., Wilcox C.S. Normalization of blood pressure and renal vascular resistance in SHR with a membrane-permeable superoxide dismutase mimetic. role of nitric oxide Hypertension. 32:1998;59-64.
132. Schrier R.W., Abraham W.T. Hormones and hemodynamics in heart failure. N. Engl. J. Med. 341:1999;577-585.
133. Schulze-Osthoff K., Bakker A.C., Vanhaesebroeck B., Beyaert R., Jacob W.A., Fiers W. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J. Biol. Chem. 267:1992;5317-5323.
134. Schumacker P.T. Angiotensin II signaling in the brain. compartmentalization of redox signaling? Circ. Res. 91:2002;982-984.
135. Shimohama S., Tanino H., Kawakami N., Okamura N., Kodama H., Yamaguchi T., Hayakawa T., Nunomura A., Chiba S., Perry G., Smith M.A., Fujimoto S. Activation of NADPH oxidase in Alzheimer's disease brains. Biochem. Biophys. Res. Commun. 273:2000;5-9.
136. Simpson J.B. The circumventricular organs and the central actions of angiotensin. Neuroendocrinology. 32:1981;248-256.
137. Sinnayah P., Lindley T.E., Staber P.D., Cassell M.D., Davidson B.L., Davisson R.L. Selective gene transfer to key cardiovascular regions of the brain. comparison of two viral vector systems Hypertension. 39:2002;603-608.
138. Sorescu D., Griendling K.K. Reactive oxygen species, mitochondria, and NAD(P)H oxidases in the development and progression of heart failure. Congest. Heart Failure. 8:2002;132-140.
139. Suh Y.A., Arnold R.S., Lassegue B., Shi J., Xu X., Sorescu D., Chung A.B., Griendling K.K., Lambeth J.D. Cell transformation by the superoxide-generating oxidase Mox1. Nature. 401:1999;79-82.
140. Suzukawa K., Miura K., Mitsushita J., Resau J., Hirose K., Crystal R., Kamata T. Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. J. Biol. Chem. 275:2000;13175-13178.
141. Swanson L.W., Lind R.W. Neural projections subserving the initiation of a specific motivated behavior in the rat. new projections from the subfornical organ Brain Res. 379:1986;399-403.
142. Tammariello, S.P., Quinn, M.T., Estus, S., 2000. NADPH oxidase contributes directly to oxidative stress and apoptosis in nerve growth factor-deprived sympathetic neurons. J. Neurosci. 20, RC53, 1-5.
143. Thannickal V.J., Fanburg B.L. Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 279:2000;L1005-L1028.
144. Toda N., Kitamura Y., Okamura T. Neural mechanism of hypertension by nitric oxide synthase inhibitor in dogs. Hypertension. 21:1993;3-8.
145. Turini G.A., Brunner H.R., Gribic M., Waeber B., Gavras H. Improvement of chronic congestive heart-failure by oral captopril. Lancet. 1:1979;1213-1215.
146. Ueda S., Masutani H., Nakamura H., Tanaka T., Ueno M., Yodoi J. Redox control of cell death. Antioxidants Redox Signal. 4:2002;405-414.
147. Ushio-Fukai M., Zafari A.M., Fukui T., Ishizaka N., Griendling K.K. p22phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J. Biol. Chem. 271:1996;23317-23321.
148. Wada A., Ueda S., Masumori-Maemoto S., Kuji N., Sugimoto K., Umemura S. Angiotensin attenuates the vasodilating effect of a nitric oxide donor, glyceryl trinitrate. roles of superoxide and angiotensin II type 1 receptors Clin. Pharmacol. Therap. 71:2002;440-447.
149. Wang Y., Patel K.P., Cornish K.G., Channon K.M., Zucker I.H. nNOS gene transfer to RVLM improves baroreflex function in rats with chronic heart failure. Am. J. Physiol. (Heart Circul. Physiol.). 285:2003;H1660-H1667.
150. Wilcox C.S. Reactive oxygen species. roles in blood pressure and kidney function Curr. Hypertens. Rep. 4:2002;160-166.
151. Xiao L., Pimentel D.R., Wang J., Singh K., Colucci W.S., Sawyer D.B. Role of reactive oxygen species and NAD(P)H oxidase in alpha(1)-adrenoceptor signaling in adult rat cardiac myocytes. Am. J. Physiol. Cell Physiol. 282:2002;C926-C934.
152. Xu H., Fink G.D., Chen A., Watts S., Galligan J.J. Nitric oxide-independent effects of tempol on sympathetic nerve activity and blood pressure in normotensive rats. Am. J. Physiol. Heart Circul. Physiol. 281:2001;H975-H980.
153. Yermolaieva O., Brot N., Weissbach H., Heinemann S.H., Hoshi T. Reactive oxygen species and nitric oxide mediate plasticity of neuronal calcium signaling. Proc. Natl. Acad. Sci. USA. 97:2000;448-453.
154. Yokota T., Igarashi K., Uchihara T., Jishage K., Tomita H., Inaba A., Li Y., Arita M., Suzuki H., Mizusawa H., Arai H. Delayed-onset ataxia in mice lacking alpha-tocopherol transfer protein. model for neuronal degeneration caused by chronic oxidative stress Proc. Natl. Acad. Sci. USA. 98:2001;15185-15190.
155. 2 in angiotensin II-induced vascular hypertrophy. Hypertension. 32:1998;488-495.
156. Zanzinger J., Czachurski J. Chronic oxidative stress in the RVLM modulates sympathetic control of circulation in pigs. Pflugers Archiv Eur. J. Physiol. 439:2000;489-494.
157. Zhang K., Mayhan W.G., Patel K.P. Nitric oxide within the paraventricular nucleus mediates changes in renal sympathetic nerve activity. Am. J. Physiol. 273:1997;R864-R872.
158. Zhang K., Zucker I.H., Patel K.P. Altered number of diaphorase (NOS) positive neurons in the hypothalamus of rats with heart failure. Brain Res. 786:1998;219-225.
159. Zhu M., Gelband C.H., Moore J.M., Posner P., Sumners C. Angiotensin II type 2 receptor stimulation of neuronal delayed-rectifier potassium current involves phospholipase A2 and arachidonic acid. J. Neurosci. 18:1998;679-686.
160. Zimmerman M.C., Lazartigues E., Lang J.A., Sinnayah P., Ahmad I.M., Spitz D.R., Davisson R.L. Superoxide mediates the actions of angiotensin II in the central nervous system. Circ. Res. 91:2002;1038-1045.
161. Zimmerman M.C., Dunlay R.P., Zhang Y., Yan Z., Engelhardt J.F., Sharma R.V., Davisson R.L. Central angiotensin II (AngII)-induced cardiovascular responses are mediated by NADPH oxidase-derived superoxide radicals. FASEB J. 17:2003;A885.
162. Zimmerman M.C., Lazartigues E., Sharma R.V., Davisson R.L. Superoxide in the brain mediates the slow-pressor effects of peripheral angiotensin II infusion in mice. Hypertension. 42:2003;398.