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

Molecular Pharmacology

Volumn 74, Issue 5, 2008, Pages 1319-1332

  Kung, Ling Chang ^a   Chan, Samuel H H ^b   Wu, Kay L H ^b   Ou, Chen Chun ^c   Tai, Ming Hon ^c   Chan, Julie Y H ^c  

^a TIAN SHENG MEMORIAL HOSPITAL   (Taiwan)

^b NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^c KAOHSIUNG VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MANGANESE SUPEROXIDE DISMUTASE; NITRIC OXIDE; SUPEROXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE REGULATION; CARDIOVASCULAR AUTOREGULATION; CONTROLLED STUDY; GENE OVEREXPRESSION; HEART RATE; HYPERTENSION; MALE; MEDULLA OBLONGATA; MICROINJECTION; MITOCHONDRIAL RESPIRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; REBOUND; SPONTANEOUSLY HYPERTENSIVE RAT; TRANSGENE;

ANIMALS; BASE SEQUENCE; BLOOD PRESSURE; DNA PRIMERS; HEART RATE; MEDULLA OBLONGATA; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, INBRED SHR; RATS, INBRED WKY; SUPEROXIDES; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 54349105140     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.108.048793     Document Type: Article

References (47)

1. Adlam D, Bendall JK, De Bono JP, Alp NJ, Khoo J, Nicoli T, Yokoyama M, Kawashima S, and Channon KM (2007) Relationships between nitric oxide-mediated endothelial function, eNOS coupling and blood pressure revealed by eNOS-GTP cyclohydrolase 1 double transgenic mice. Exp Physiol 92:119-126.
2. Andrews ZB, Diano S, and Horvath TL (2005) Mitochondrial uncoupling proteins in the CNS: in support of function and survival. Nat Rev Neurosci 6:829-840.
3. Antoniades C, Shirodaria C, Warrick N, Cai S, de Bono J, Lee J, Leeson P, Neubauer S, Ratnatunga C, Pillai R, et al. (2006) 5-methyltetrahydrofolate rapidly improves endothelial function and decrease superoxide production in human vessels. Effects on vascular tetrahyrobiopterin availability and endothelial nitric oxide synthase coupling. Circulation 114:1193-1201.
4. Bendall JK, Alp NJ, Warrick N, Cai S, Adlam D, Rockett K, Yokoyama M, Kawashima S, and Channon KM (2005) Stoichiometric relationships between endothelial tetrahydrobiopterin, eNOS activity and eNOS coupling in vivo: insights from transgenic mice with endothelial-targeted GTP cyclohydrolase 1 and eNOS over-expression. Circ Res 97:864-871.
5. Borutaite V and Brown GC (2006) S-nitrosothiol inhibition of mitochondrial complex I causes a reversible increase in mitochondrial hydrogen peroxide production. Biochim Biophys Acta 1757:562-566.
6. Brevetti LS, Chang DS, Tang GL, Sarkar R, and Messina LM (2003) Overexpression of endothelial nitric oxide synthase increases skeletal muscle blood flow and oxygenation in severe rat hind limb ischemia. J Vasc Surg 38:820-826.
7. Brown GC and Borutaite V (2004) Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols. Biochim Biophys Acta 1658:44-49.
8. Callera GE, Tostes RC, Yogi A, Montezano AC, and Touyz RM (2006) Endothelin-1-induced oxidative stress in DOCA-salt hypertension involves NADPH-oxidase-independent mechanisms. Clin Sci 110:243-253.
9. Chan JY, Chang AY, Wang LL, Ou CC, and Chan SH (2007a) Protein kinase C-dependent mitochondrial translocation of proapoptotic protein Bax on activation of inducible nitric oxide synthase in rostral ventrolateral medulla mediates cardiovascular depression during experimental endotoxemia. Mol Pharmacol 71: 1129-1139.
10. Chan JY, Wang LL, Chao YM, and Chan SH (2003) Down-regulation of basal iNOS at rostral ventrolateral medulla is innate in SHR. Hypertension 41:563-570.
11. Chan SH, Hsu KS, Huang CC, Wang LL, Ou CC, and Chan JY (2005a) 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.
12. Chan SH, Tai MH, Li CY, and Chan JY (2006) 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.
13. 1 receptor gene on activation of protein kinase Cβ/nicotinamide adenine dinucleotide diphosphate oxidase/ERK1/2/c-fos signaling cascade mediates long-term pressor effect of angiotensin II in rostral ventrolateral medulla. J Hypertens 25:1845-1861.
14. Chan SH, Wang LL, Wang SH, and Chan JY (2001) Differential cardiovascular responses to blockade of nNOS or iNOS in rostral ventrolateral medulla of the rat. Br J Pharmacol 133:606-614.
15. Chan SH, Wu KL, Wang LL, and Chan JY (2005b) Nitric oxide- and superoxide-dependent mitochondrial signaling in endotoxin-induced apoptosis in the rostral ventrolateral medulla of rats. Free Radic Biol Med 39:603-618.
16. Cleeter MW, Cooper JM, Darley-Usmar VM, Moncada S, and Schapira AH (1994) Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett 345:50-54.
17. Dampney RAL (1994) Functional organization of central pathways regulating the cardiovascular system. Physiol Rev 74:323-364.
18. Edwards MA, Loxley RA, Powers-Martin K, Lipski J, McKitrick DJ, Arnolda LF, and Phillips JK (2004) 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.
19. Kagiyama S, Tsuchihashi T, Abe I, and Fujishima M (1998) Enhanced depressor response to nitric oxide in the rostral ventrolateral medulla of spontaneously hypertensive rats. Hypertension 31:1030-1034.
20. Kantrow SP, Taylor DE, Carraway MS, and Piantadosi CA (1997) Oxidative metabolism in rat hepatocytes and mitochondria during sepsis. Arch Biochem Biophys 345:278-288.
21. Kimura Y, Hirooka Y, Sagara Y, Ito K, Kishi T, Shimokawa H, Takeshita A, and Sunagawa K (2005a) 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.
22. Kimura S, Zhang GX, Nishiyama A, Shokoji T, Yao L, Fan YY, Rahman M, and Abe Y (2005b) Mitochondria-derived reactive oxygen species and vascular MAP kinases: comparison of angiotensin II and diazoxide. Hypertension 45:438-444.
23. Kishi T, Hirooka Y, Ito K, Sakai K, Shimokawa H, and Takeshita A (2002) Cardiovascular effects of overexpression of endothelial nitric oxide synthase in the rostral ventrolateral medulla in stroke-prone spontaneously hypertensive rats. Hypertension 39:264-268.
24. Kishi T, Hirooka Y, Kimura Y, Ito K, Shimokawa H, and Takeshita A (2004) Increased reactive oxygen species in rostral ventrolateral medulla contribute to neural mechanisms of hypertension in stroke-prone spontaneously hypertensive rats. Circulation 109:2357-2362.
25. Kishi T, Hirooka Y, Kimura Y, Sakai K, Ito K, Shimokawa H, and Takeshita A (2003) Overexpression of eNOS in RVLM improves impaired baroreflex control of heart rate in SHRSP. Hypertension 41:255-260.
26. Korshunov SS, Skulachev VP, and Starkov AA (1997) High protonic potential actuates a mechanism o f production of reactive oxygen species in mitochondria. FEBS Lett 416:15-18.
27. Kudin AP, Bimpong-Buta NY, Vielhaber S, Elger CE, and Kunz WS (2004) Characterization of superoxide-producing sites in isolated brain mitochondria. J Biol Chem 279:4127-4135.
28. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, and Harrison DG (2003) Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 111:1201-1209.
29. Li H, Witte K, August M, Brausch I, Gödtel-Armbrust U, Habermeier A, Closs EI, Oelze M, Münzel T, and Förstermann U (2006) Reversal of endothelial nitric oxide synthase uncoupling and up-regulation of endothelial nitric oxide synthase expression lowers blood pressure in hypertensive rats. J Am Coll Cardiol 47:2536-2544.
30. Mason MG, Nicholls P, Wilson MT, and Cooper CE (2006) Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase. Proc Natl Acad Sci U S A 103:708-713.
31. Mayorov DN (2005) Selective sensitization by nitric oxide of sympathetic baroreflex in rostral ventrolateral medulla of conscious rabbits. Hypertension 45:901-906.
32. Merial C, Bouloumie A, Trocheris V, Lafontan M, and Galitzky J (2000) Nitric oxide-dependent downregulation of adipocyte UCP-2 expression by tumor necrosis factor-α. Am J Physiol Cell Physiol 279:C1100- C1106.
33. Morten KJ, Ackrell BA, and Melov S (2006) Mitochondrial reactive oxygen species in mice lacking superoxide dismutase 2. Attenuation via antioxidant treatment. J Biol Chem 281:3354-3359.
34. Murray J, Taylor SW, Zhang B, Ghosh SS, and Capaldi RA (2003) Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry. J Biol Chem 278:37223- 37230.
35. Naithani S, Saracco SA, Butler CA, and Fox TD (2003) Interactions among COX1, COX2, and COX3 mRNA-specific translational activator proteins on the inner surface of the mitochondrial inner membrane of Saccharomyces cerevisiae. Mol Biol Cell 14:324-333.
36. Nègre-Salvayre A, Hirtz C, Carrera G, Cazenave R, Troly M, Salvayre R, Pénicaud L, and Casteilla L (1997) A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J 11:809-815.
37. Nolte RT, Wisely GB, Westin S, Cobb JE, Lambert MH, Kurokawa R, Rosenfeld MG, Willson TM, Glass CK, and Milburn MV (1998) Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. Nature 395: 137-143.
38. Reiter CD, Teng RJ, and Beckman JS (2000) Superoxide reacts with nitric oxide to nitrate tyrosine at physiological pH via peroxynitrite. J Biol Chem 275:32460-32466.
39. Ross CA, Ruggiero DA, Park DH, Joh TH, Sved AF, Fernandez-Pardal J, Saavedra JM, and Reis DJ (1984) Tonic vasomotor control by the rostral ventrolateral medulla: effect of electrical and chemical stimulation of the area containing C1 adrenaline neurons on arterial pressure, heart rate and plasma catecholamine and vasopressin. J Neurosci 4:474-494.
40. a3 couple in cytochrome c oxidase as revealed by nitric oxide binding studies. Proc Natl Acad Sci U S A 76:3320-3324.
41. Tai MH, Wang LL, Wu KL, and Chan JY (2005) 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.
42. Tandai-Hiruma M, Horiuchi J, Sakamoto H, Kemuriyama T, Hirakawa H, and Nishida Y (2005) Brain neuronal nitric oxide synthase neuron-mediated sympathoinhibition is enhanced in hypertensive Dahl rats. J Hypertens 23:825-834.
43. Waki H, Murphy D, Yao ST, Kasparov S, and Paton JF (2006) Endothelial NO synthase activity in nucleus tractus solitarii contributes to hypertension in spontaneously hypertensive rats. Hypertension 48:644-650.
44. Wu KL, Hsu C, and Chan JY (2007) Impairment of the mitochondrial respiratory enzyme activity triggers sequential activation of apoptosis-inducing factor-dependent and caspase-dependent signaling pathways to induce apoptosis after spinal cord injury. J Neurochem 101:1552-1566.
45. 2+/calmodulin-dependent and tetrahydrobiopterin regulatory process. J Biol Chem 273:25804- 25808.
46. Zanzinger J (1999) Role of nitric oxide in the neural control of cardiovascular function. Cardiovasc Res 43:639-649.
47. Zanzinger J, Czachurski J, and Seller H (1995) Inhibition of basal and reflex-mediated sympathetic activity in the RVLM by nitric oxide. Am J Physiol 268:R958-R962.