The neuroprotective action of candesartan is related to interference with the early stages of 6-hydroxydopamine-induced dopaminergic cell death

European Journal of Neuroscience

Volumn 34, Issue 7, 2011, Pages 1141-1148

  Mertens, Birgit ^a   Varcin, Mustafa ^a   Michotte, Yvette ^a   Sarre, Sophie ^a,b  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b Wetenschappelijk Instituut voor Volksgezondheid   (Belgium)

Author keywords

Antagonist of the angiotensin II type 1 receptor; Nicotinamide adenine dinucleotide phosphate oxidase; Oxidative stress; Protein kinase C; Rat; Renin angiotensin system

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; APOCYNIN; CANDESARTAN; CHELERYTHRINE; OXIDOREDUCTASE; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC SYSTEM; DRUG ACTIVITY; DRUG EFFICACY; IN VIVO STUDY; MALE; MICRODIALYSIS; NEUROPROTECTION; NEUROTOXICITY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; STEREOTAXIS;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; BENZIMIDAZOLES; CELL COUNT; CELL DEATH; CORPUS STRIATUM; DOPAMINE; DOPAMINERGIC NEURONS; MALE; MICRODIALYSIS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; OXIDOPAMINE; RATS; RATS, WISTAR; SUBSTANTIA NIGRA; TETRAZOLES;

EID: 80053563928     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07840.x     Document Type: Article

References (58)

1. Andersen, J.K. (2004) Oxidative stress in neurodegeneration: cause or consequence? Nat. Med., 10(Suppl), S18-S25.
2. Babior, B.M. (1999) NADPH oxidase: an update. Blood, 93, 1464-1476.
3. Babior, B.M. (2004) NADPH oxidase. Curr. Opin. Immunol., 16, 42-47.
4. Babior, B.M., Lambeth, J.D. & Nauseef, W. (2002) The neutrophil NADPH oxidase. Arch. Biochem. Biophys., 397, 342-344.
5. Block, M.L. & Hong, J.S. (2005) Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol., 76, 77-98.
6. Chabrashvili, T., Kitiyakara, C., Blau, J., Karber, A., Aslam, S., Welch, W.J. & Wilcox, C.S. (2003) Effects of ANG II type 1 and 2 receptors on oxidative stress, renal NADPH oxidase, and SOD expression. Am. J. Physiol. Regul. Integr. Comp. Physiol., 285, R117-R124.
7. Culman, J., Blume, A., Gohlke, P. & Unger, T. (2002) The renin-angiotensin system in the brain: possible therapeutic implications for AT(1)-receptor blockers. J. Hum. Hypertens., 16(Suppl 3), S64-S70.
8. Dunnett, S.B. & Bjorklund, A. (1999) Prospects for new restorative and neuroprotective treatments in Parkinson's disease. Nature, 399, A32-A39.
9. Fischer-Ferraro, C., Nahmod, V.E., Goldstein, D.J. & Finkielman, S. (1971) Angiotensin and renin in rat and dog brain. J. Exp. Med., 133, 353-361.
10. Gao, H.M., Hong, J.S., Zhang, W. & Liu, B. (2002) Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci., 22, 782-790.
11. Gao, H.M., Liu, B. & Hong, J.S. (2003) Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci., 23, 6181-6187.
12. Garrido, A.M. & Griendling, K.K. (2009) NADPH oxidases and angiotensin II receptor signaling. Mol. Cell. Endocrinol., 302, 148-158.
13. Gohlke, P., Von Kugelgen, S., Jurgensen, T., Kox, T., Rascher, W., Culman, J. & Unger, T. (2002) Effects of orally applied candesartan cilexetil on central responses to angiotensin II in conscious rats. J. Hypertension, 20, 909-918.
14. Grammatopoulos, T.N., Ahmadi, F., Jones, S.M., Fariss, M.W., Weyhenmeyer, J.A. & Zawada, W.M. (2005) Angiotensin II protects cultured midbrain dopaminergic neurons against rotenone-induced cell death. Brain Res., 1045, 64-71.
15. Grammatopoulos, T.N., Jones, S.M., Ahmadi, F.A., Hoover, B.R., Snell, L.D., Skoch, J., Jhaveri, V.V., Poczobutt, A.M., Weyhenmeyer, J.A. & Zawada, W.M. (2007) Angiotensin type 1 receptor antagonist losartan, reduces MPTP-induced degeneration of dopaminergic neurons in substantia nigra. Mol. Neurodegener., 2, 1.
16. Griendling, K.K. & Ushio-Fukai, M. (2000) Reactive oxygen species as mediators of angiotensin II signaling. Regul. Pept., 91, 21-27.
17. Griendling, K.K., Sorescu, D. & Ushio-Fukai, M. (2000) NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res., 86, 494-501.
18. Izurieta-Sanchez, P., Sarre, S., Ebinger, G. & Michotte, Y. (1998) Effect of trihexyphenidyl, a non-selective antimuscarinic drug, on decarboxylation of L-dopa in hemi-Parkinson rats. Eur. J. Pharmacol., 353, 33-42.
19. Jenner, P. & Olanow, C.W. (1998) Understanding cell death in Parkinson's disease. Ann. Neurol., 44, S72-S84.
20. Joglar, B., Rodriguez-Pallares, J., Rodriguez-Perez, A.I., Rey, P., Guerra, M.J. & Labandeira-Garcia, J.L. (2009) The inflammatory response in the MPTP model of Parkinson's disease is mediated by brain angiotensin: relevance to progression of the disease. J. Neurochem., 109, 656-669.
21. Johnston, T.H. & Brotchie, J.M. (2004) Drugs in development for Parkinson's disease. Curr. Opin. Investig. Drugs, 5, 720-726.
22. Laursen, J.B., Rajagopalan, S., Galis, Z., Tarpey, M., Freeman, B.A. & Harrison, D.G. (1997) Role of superoxide in angiotensin II-induced but not catecholamine-induced hypertension. Circulation, 95, 588-593.
23. Mertens, B., Massie, A., Michotte, Y. & Sarre, S. (2009) Effect of nigrostriatal damage induced by 6-hydroxydopamine on the expression of glial cell line-derived neurotrophic factor in the striatum of the rat. Neuroscience, 162, 148-154.
24. Mertens, B., Vanderheyden, P., Michotte, Y. & Sarre, S. (2010a) Direct angiotensin II type 2 receptor stimulation decreases dopamine synthesis in the rat striatum. Neuropharmacology, 58, 1038-1044.
25. Mertens, B., Vanderheyden, P., Michotte, Y. & Sarre, S. (2010b) The role of the central renin-angiotensin system in Parkinson's disease. J. Renin Angiotensin Aldosterone Syst., 11, 49-56.
26. van Muiswinkel, F.L., de Vos, R.A., Bol, J.G., Andringa, G., Jansen Steur, E.N., Ross, D., Siegel, D. & Drukarch, B. (2004) Expression of NAD(P)H:quinone oxidoreductase in the normal and Parkinsonian substantia nigra. Neurobiol. Aging, 25, 1253-1262.
27. Obata, T. (2006) Activation of protein kinase C enhances 1-methyl-4-phenylpyridinium ion (MPP+)-induced hydroxylradical generation in rat striatum. Neurosci. Lett., 398, 50-52.
28. O'Neill, M.J., Messenger, M.J., Lakics, V., Murray, T.K., Karran, E.H., Szekeres, P.G., Nisenbaum, E.S. & Merchant, K.M. (2007) Neuroreplacement, growth factor, and small molecule neurotrophic approaches for treating Parkinson's disease. Int. Rev. Neurobiol., 77, 179-217.
29. Oudit, G.Y., Kassiri, Z., Patel, M.P., Chappell, M., Butany, J., Backx, P.H., Tsushima, R.G., Scholey, J.W., Khokha, R. & Penninger, J.M. (2007) Angiotensin II-mediated oxidative stress and inflammation mediate the age-dependent cardiomyopathy in ACE2 null mice. Cardiovasc. Res., 75, 29-39.
30. Paxinos, G. & Watson, C. (1986). The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego.
31. Phillips, M.I. & de Oliveira, E.M. (2008) Brain renin angiotensin in disease. J. Mol. Med., 86, 715-722.
32. Rajagopalan, S., Kurz, S., Munzel, T., Tarpey, M., Freeman, B.A., Griendling, K.K. & Harrison, D.G. (1996) Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J. Clin. Invest., 97, 1916-1923.
33. Rey, F.E., Cifuentes, M.E., Kiarash, A., Quinn, M.T. & Pagano, P.J. (2001) Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O(2)(-) and systolic blood pressure in mice. Circ. Res., 89, 408-414.
34. Rey, P., Lopez-Real, A., Sanchez-Iglesias, S., Munoz, A., Soto-Otero, R. & Labandeira-Garcia, J.L. (2007) Angiotensin type-1-receptor antagonists reduce 6-hydroxydopamine toxicity for dopaminergic neurons. Neurobiol. Aging, 28, 555-567.
35. Rodriguez-Pallares, J., Parga, J.A., Munoz, A., Rey, P., Guerra, M.J. & Labandeira-Garcia, J.L. (2007) Mechanism of 6-hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6-hydroxydopamine-induced degeneration of dopaminergic neurons. J. Neurochem., 103, 145-156.
36. Rodriguez-Pallares, J., Rey, P., Parga, J.A., Munoz, A., Guerra, M.J. & Labandeira-Garcia, J.L. (2008) Brain angiotensin enhances dopaminergic cell death via microglial activation and NADPH-derived ROS. Neurobiol. Dis., 31, 58-73.
37. Ruiz-Ortega, M., Lorenzo, O., Ruperez, M., Esteban, V., Suzuki, Y., Mezzano, S., Plaza, J.J. & Egido, J. (2001) Role of the renin-angiotensin system in vascular diseases: expanding the field. Hypertension, 38, 1382-1387.
38. Sanchez-Iglesias, S., Rey, P., Mendez-Alvarez, E., Labandeira-Garcia, J.L. & Soto-Otero, R. (2007) Time-course of brain oxidative damage caused by intrastriatal administration of 6-hydroxydopamine in a rat model of Parkinson's disease. Neurochem. Res., 32, 99-105.
39. Serrano, F., Kolluri, N.S., Wientjes, F.B., Card, J.P. & Klann, E. (2003) NADPH oxidase immunoreactivity in the mouse brain. Brain Res., 988, 193-198.
40. Seshiah, P.N., Weber, D.S., Rocic, P., Valppu, L., Taniyama, Y. & Griendling, K.K. (2002) Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ. Res., 91, 406-413.
41. Shu, S.Y, Ju, G & Fan, L.Z. (1988) The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. J. Neurosci. Methods, 85, 169-171.
42. Soto-Otero, R., Mendez-Alvarez, E., Hermida-Ameijeiras, A., Munoz-Patino, A.M. & Labandeira-Garcia, J.L. (2000) Autoxidation and neurotoxicity of 6-hydroxydopamine in the presence of some antioxidants: potential implication in relation to the pathogenesis of Parkinson's disease. J. Neurochem., 74, 1605-1612.
43. Steckelings, U.M., Kaschina, E. & Unger, T. (2005) The AT2 receptor - a matter of love and hate. Peptides, 26, 1401-1409.
44. Stefanska, J. & Pawliczak, R. (2008) Apocynin: molecular aptitudes. Mediators Inflamm., 2008, 106507.
45. Stragier, B., Sarre, S., Vanderheyden, P., Vauquelin, G., Fournie-Zaluski, M.C., Ebinger, G. & Michotte, Y. (2004) Metabolism of angiotensin II is required for its in vivo effect on dopamine release in the striatum of the rat. J. Neurochem., 90, 1251-1257.
46. Sun, C., Sellers, K.W., Sumners, C. & Raizada, M.K. (2005) NAD(P)H oxidase inhibition attenuates neuronal chronotropic actions of angiotensin II. Circ. Res., 96, 659-666.
47. Suzuki, Y., Ruiz-Ortega, M., Lorenzo, O., Ruperez, M., Esteban, V. & Egido, J. (2003) Inflammation and angiotensin II. Int. J. Biochem. Cell Biol., 35, 881-900.
48. Touyz, R.M. (2004) Reactive oxygen species and angiotensin II signaling in vascular cells - implications in cardiovascular disease. Braz. J. Med. Biol. Res., 37, 1263-1273.
49. Touyz, R.M., Chen, X., Tabet, F., Yao, G., He, G., Quinn, M.T., Pagano, P.J. & Schiffrin, E.L. (2002) Expression of a functionally active gp91phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ. Res., 90, 1205-1213.
50. Veerasingham, S.J. & Raizada, M.K. (2003) Brain renin-angiotensin system dysfunction in hypertension: recent advances and perspectives. Br. J. Pharmacol., 139, 191-202.
51. Wang, Q.D. & Sjoquist, P.O. (1999) Effects of the insurmountable angiotensin AT1 receptor antagonist candesartan and the surmountable antagonist losartan on ischemia/reperfusion injury in rat hearts. Eur. J. Pharmacol., 380, 13-21.
52. Wang, G., Anrather, J., Huang, J., Speth, R.C., Pickel, V.M. & Iadecola, C. (2004) NADPH oxidase contributes to angiotensin II signaling in the nucleus tractus solitarius. J. Neurosci., 24, 5516-5524.
53. Wang, G., Anrather, J., Glass, M.J., Tarsitano, M.J., Zhou, P., Frys, K.A., Pickel, V.M. & Iadecola, C. (2006) Nox2, Ca2+, and protein kinase C play a role in angiotensin II-induced free radical production in nucleus tractus solitarius. Hypertension, 48, 482-489.
54. Wu, D.C., Teismann, P., Tieu, K., Vila, M., Jackson-Lewis, V., Ischiropoulos, H. & Przedborski, S. (2003) NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine model of Parkinson's disease. Proc. Natl. Acad. Sci. USA, 100, 6145-6150.
55. Yuan, H., Sarre, S., Ebinger, G. & Michotte, Y. (2004) Neuroprotective and neurotrophic effect of apomorphine in the striatal 6-OHDA-lesion rat model of Parkinson's disease. Brain Res., 1026, 95-107.
56. Yuan, H., Sarre, S., Ebinger, G. & Michotte, Y. (2005) Histological, behavioural and neurochemical evaluation of medial forebrain bundle and striatal 6-OHDA lesions as rat models of Parkinson's disease. J. Neurosci. Methods, 144, 35-45.
57. Zimmerman, M.C., Dunlay, R.P., Lazartigues, E., Zhang, Y., Sharma, R.V., Engelhardt, J.F. & Davisson, R.L. (2004a) Requirement for Rac1-dependent NADPH oxidase in the cardiovascular and dipsogenic actions of angiotensin II in the brain. Circ. Res., 95, 532-539.
58. Zimmerman, M.C., Lazartigues, E., Sharma, R.V. & Davisson, R.L. (2004b) Hypertension caused by angiotensin II infusion involves increased superoxide production in the central nervous system. Circ. Res., 95, 210-216.