Mitochondria-derived reactive oxygen species mediate sympathoexcitation induced by angiotensin II in the rostral ventrolateral medulla

Journal of Hypertension

Volumn 26, Issue 11, 2008, Pages 2176-2184

  Nozoe, Masatsugu ^a   Hirooka, Yoshitaka ^a   Koga, Yasuaki ^a   Araki, Shuichiro ^a   Konno, Satomi ^a   Kishi, Takuya ^a   Ide, Tomomi ^a   Sunagawa, Kenji ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Blood pressure; Brain; Hypertension; Mitochondria; Sympathetic nervous system

Indexed keywords

ADENOVIRUS VECTOR; ANGIOTENSIN II; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; EGTAZIC ACID; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; ROTENONE; CALCIUM; SUPEROXIDE DISMUTASE; VASOCONSTRICTOR AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CELL STRAIN; CONTROLLED STUDY; DRUG INHIBITION; EXTRACELLULAR CALCIUM; GENE OVEREXPRESSION; GENE TRANSFER; IN VITRO STUDY; IN VIVO STUDY; MALE; MEDULLA OBLONGATA; MITOCHONDRION; NONHUMAN; PRESSOR RESPONSE; PRIORITY JOURNAL; RAT; SYMPATHETIC INNERVATION; SYMPATHETIC TONE; ADENOVIRUS; ADRENERGIC SYSTEM; ANIMAL; DRUG EFFECT; GENE VECTOR; GENETICS; METABOLISM; WISTAR KYOTO RAT;

ADENOVIRIDAE; ANGIOTENSIN II; ANIMALS; CALCIUM; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; MALE; MEDULLA OBLONGATA; MITOCHONDRIA; RATS; RATS, INBRED WKY; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; SYMPATHETIC NERVOUS SYSTEM; VASOCONSTRICTOR AGENTS;

EID: 56049119631     PISSN: 02636352     EISSN: None     Source Type: Journal    
DOI: 10.1097/HJH.0b013e32830dd5d3     Document Type: Article

References (44)

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, Lazartigues E, Lang JA, Sinnayah P, Ahmad IM, Spitz DR, Davisson RL. Superoxide mediates the actions of angiotensin II in the central nervous system. Circ Res 2002; 91:1038-1045.
3. Kimura Y, Hirooka Y, Sagara Y, Ito K, Kishi T, Shimokawa H, et al. 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. 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.
5. 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.
6. Zimmerman MC, Sharma RV, Davisson RL. Superoxide mediates angiotensin II-induced infux of extracellular calcium in neural cells. Hypertension2005; 45:717-723.
7. 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 thebrain. Circ Res 2004; 95:532-539.
8. 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.
9. 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.
10. Gao L, Wang W, Li YL, Schultz HD, Liu D, Cornish KG, 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 2005; 288:H2271-H2279.
11. Gao XY, Zhang F, Han Y, Wang HJ, Zhang Y, Guo R, Zhu GQ. AT1receptor in rostral ventrolateral medulla mediating blunted baroreceptor refex in spontaneously hypertensive rats. Acta Pharmacol Sin 2004; 25:1433-1438.
12. Sun C, Sellers KW, Sumners C, Raizada MK. NAD(P)H oxidase inhibition attenuates neuronal chronotropic actions of angiotensin II. Circ Res 2005; 96:659-666.
13. Chan SH, Hsu KS, Huang CC, Wang LL, Ou CC, Chan JY. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced pressoreffect via activation of p38 mitogen-activated protein kinase in the rostral ventrolateral medulla. Circ Res 2005; 97:772-780.
14. Hongpaisan J, Winters CA, Andrews SB. Strong calcium entry activates mitochondrial superoxide generation, upregulating kinase signaling in hippocampal neurons. J Neurosci 2004; 24:10878-10887.
15. Jenner P. Parkinson's disease, pesticides and mitochondrial dysfunction. Trends Neurosci 2001; 24:245-247.
16. Yan SD, Stern DM.Mitochondrial dysfunction and Alzheimer's disease: role of amyloid-beta peptide alcohol dehydrogenase (ABAD). Int J Exp Pathol 2005; 86:161-171.
17. Sciamanna MA, Zinkel J, Fabi AY, Lee CP. Ischemic injury to rat forebrain mitochondria and cellular calcium homeostasis. Biochim Biophys Acta 1992; 1134:223-232.
18. Hancock JT, Desikan R, Neill SJ. Role of reactive oxygen species in cell signalling pathways. Biochem Soc Trans 2001; 29:345-350.
19. Dai X, Cao X, Kreulen DL. Superoxide anion is elevated in sympathetic neurons in DOCA-salt hypertension via activation of NADPH oxidase. Am JPhysiol Heart Circ Physiol 2006; 290:H1019-H1026.
20. Greene LA, Tischler AS. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 1976; 73:2424-2428.
21. Brini M. Ca(2+) signalling in mitochondria: mechanism and role in physiology and pathology. Cell Calcium 2003; 34:399-405.
22. Starkov AA, Polster BM, Fiskum G. Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J Neurochem 2002; 83:220-228.
23. Colegrove SL, AlbrechtMA, Friel DD.Quantitative analysis ofmitochondrial Ca2 uptake and release pathways in sympathetic neurons.Reconstruction of the recovery after depolarization-evoked [Ca2]ielevations. J Gen Physiol 2000; 115:371-388.
24. Zwacka RM, Zhou W, Zhang Y, Darby CJ, Dudus L, Halldorson J, et al.Redox gene therapy for ischemia/reperfusion injury of the liver reduces AP1and NF-kappaB activation. Nat Med 1998; 4:698-704.
25. Nozoe M, Hirooka Y, Koga Y, Sagara Y, Kishi T, Engelhardt JF, 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 2007; 50:62-68.
26. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. New York, NY, USA: Academic Press; 1998.
27. Yang CY, Lin MT. Oxidative stress in rats with heatstroke-induced cerebral ischemia. Stroke 2002; 33:790-794.
28. Obata T, Yamanaka Y. Protective effect of imidaprilat, an angiotensin- converting enzyme inhibitor on -OH generation in ratmyocardium. Biochim Biophys Acta 1999; 1472:62-70.
29. Obermeier A, Bradshaw RA, Seedorf K, Choidas A, Schlessinger J, Ullrich A. definition of signals for neuronal differentiation. Ann N Y Acad Sc 1995; 766:1-17.
30. Furuya H, Shinnoh N, Ohyagi Y, Ikezoe K, Kikuchi H, Osoegawa M, et al. Some avonoids and DHEA-S prevent the cis-effect of expanded CTG repeats in a stable PC12 cell transformant. Biochem Pharmacol 2005; 69:503-516.
31. 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.
32. Ono H, Ichiki T, Ohtsubo H, Fukuyama K, Imayama I, Iino N, et al. CAMP- response element-binding protein mediates tumor necrosis factor-alpha-induced vascular cell adhesion molecule-1 expression in endothelial cells. Hypertens Res 2006; 29:39-47.
33. Imoto K, Kukidome D, Nishikawa T, Matsuhisa T, Sonoda K, Fujisawa K, et al. Impact of mitochondrial reactive oxygen species and apoptosis signal-regulating kinase 1 on insulin signaling. Diabetes 2006; 55:1197-1204.
34. Philipp S, Cui L, Ludolph B, Kelm M, Schulz R, Cohen MV, Downey JM. Desferoxamine and ethyl-3,4-dihydroxybenzoate protect myocardium by activating NOS and generating mitochondrial ROS. Am J Physiol Heart Circ Physiol 2006; 290:H450-H457.
35. Ide T, Tsutsui H, Hayashidani S, Kang D, Suematsu N, Nakamura K, et al.Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res 2001; 88 :529-535.
36. Okado-Matsumoto A, Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem 2001; 276 :38388-38393.
37. Wang G, Anrather J, Glass MJ, Tarsitano MJ, Zhou P, Frys KA, et al. Nox2, Ca2, and protein kinase C play a role in angiotensin II-induced free radical production in nucleus tractus solitarius. Hypertension 2006; 48 :482-489.
38. Feng Z,Wei C, Chen X,Wang J, Cheng H, Zhang X, et al. Essential role of Ca2 release channels in angiotensin II-induced Ca2+ oscillations and mesangial cell contraction. Kidney Int 2006; 70 :130-138.
39. De Koninck P, Schulman H. Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 1998; 279 :227-230.
40. Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI. Differential activation of transcription factors induced by Ca2 response amplitude and duration. Nature 1997; 386 :855-858.
41. Tse A, Tse FW, Almers W, Hille B. Rhythmic exocytosis stimulated by GnRH-induced calcium oscillations in rat gonadotropes. Science 1993; 260 :82-84.
42. Camello-Almaraz C, Gomez-Pinilla PJ, Pozo MJ, Camello PJ. Mitochondrial reactive oxygen species and Ca2+ signaling. Am J Physiol Cell Physiol 2006; 291 :C1082-C1088.
43. Chan SH, Wu KL, Wang LL, Chan JY. Nitric oxide- and superoxide-dependent mitochondrial signaling in endotoxin-induced apoptosis in the rostral ventrolateral medulla of rats. Free Radic Biol Med 2005; 39 :603-618.
44. Nozoe M, Hirooka Y, Koga Y, Sagara Y, Ide T, Sunagawa K. Mitochondrial respiratory chain dysfunction in the brain is not a major component of increased reactive oxygen species in neural mechanisms of hypertension[abstract]. FASEB J 2006; 20 :A358.