The neuroprotective effects of apocynin

Frontiers in Bioscience - Elite

Volumn 4 E, Issue 6, 2012, Pages 2183-2193

  Simonyi, Agnes ^a   Serfozo, Peter ^a   Lehmidi, Tareq M ^a   Cui, Jiankun ^a   Gu, Zezong ^a   Lubahn, Dennis B ^a   Sun, Albert Y ^a   Sun, Grace Y ^a  

^a University of Missouri   (United States)

Author keywords

Animal models; Apocynin; NADPH oxidase; Neurodegeneration; NOX2; Review

Indexed keywords

APOCYNIN; CYCLOOXYGENASE 2; GLYCOPROTEIN GP 91; INDUCIBLE NITRIC OXIDE SYNTHASE; MYELOPEROXIDASE; PEROXYNITRITE; PROTEIN P22; PROTEIN P47; PROTEIN P67; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SECRETORY PHOSPHOLIPASE A2; ACETOPHENONE DERIVATIVE; NEUROPROTECTIVE AGENT;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ANTIINFLAMMATORY ACTIVITY; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN ISCHEMIA; DEGENERATIVE DISEASE; DRUG EFFECT; DRUG EFFICACY; ENZYME INHIBITION; HEPATIC ENCEPHALOPATHY; HIV ASSOCIATED DEMENTIA; HUMAN; HUNTINGTON CHOREA; IN VIVO STUDY; INFLAMMATION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; REVIEW; SCHIZOPHRENIA; SLEEP DISORDERED BREATHING; SPINAL CORD INJURY; SUBARACHNOID HEMORRHAGE; TEMPORAL LOBE EPILEPSY; ENZYMOLOGY; MENTAL DISEASE; METABOLISM;

ANIMALIA; PICRORHIZA KURROOA;

ACETOPHENONES; HUMANS; MENTAL DISORDERS; NADPH OXIDASE; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS;

EID: 84860848480     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: 10.2741/e535     Document Type: Review

References (113)

1. D. E. Moerman: Native American Ethnobotany. Timber Press, Portland, Oregon (1998)
2. Q. Xiong, W. Fan, Y. Tezuka, I. K. Adnyana, P. Stampoulis, M. Hattori, T. Namba and S. Kadota: Hepatoprotective effect of Apocynum venetum and its active constituents. Planta Med, 66 (2), 127-33 (2000)) (Pubitemid 30164353)
3. Picrorhiza kurroa. Monograph. Altern Med Rev., 6, 319-321 (2001))
4. J. Yu, M. Weiwer, R. J. Linhardt and J. S. Dordick: The role of the methoxyphenol apocynin, a vascular NADPH oxidase inhibitor, as a chemopreventative agent in the potential treatment of cardiovascular diseases. Curr Vasc Pharmacol, 6 (3), 204-17 (2008))
5. Q. Wang, R. E. Smith, R. Luchtefeld, A. Y. Sun, A. Simonyi, R. Luo and G. Y. Sun: Bioavailability of apocynin through its conversion to glycoconjugate but not to diapocynin. Phytomedicine, 15 (6-7), 496-503 (2008)) (Pubitemid 351790760)
6. F. B. Gjertsen, E. Solheim and R. R. Scheline: Metabolism of aromatic plant ketones in rats: acetovanillone and paeonol. Xenobiotica, 18 (2), 225-34 (1988)) (Pubitemid 18071749)
7. J. M. Simons, B. A. Hart, T. R. Ip Vai Ching, H. Van Dijk and R. P. Labadie: Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils. Free Radic Biol Med, 8 (3), 251-8 (1990))
8. J. Stolk, T. J. Hiltermann, J. H. Dijkman and A. J. Verhoeven: Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxysubstituted catechol. Am J Respir Cell Mol Biol, 11 (1), 95-102 (1994))
9. V. F. Ximenes, M. P. Kanegae, S. R. Rissato and M. S. Galhiane: The oxidation of apocynin catalyzed by myeloperoxidase: proposal for NADPH oxidase inhibition. Arch Biochem Biophys, 457 (2), 134-41 (2007)) (Pubitemid 46048700)
10. M. P. Kanegae, A. Condino-Neto, L. A. Pedroza, A. C. de Almeida, J. Rehder, L. M. da Fonseca and V. F. Ximenes: Diapocynin versus apocynin as pretranscriptional inhibitors of NADPH oxidase and cytokine production by peripheral blood mononuclear cells. Biochem Biophys Res Commun, 393 (3), 551-4 (2010))
11. M. Mora-Pale, M. Weiwer, J. Yu, R. J. Linhardt and J. S. Dordick: Inhibition of human vascular NADPH oxidase by apocynin derived oligophenols. Bioorg Med Chem, 17 (14), 5146-52 (2009))
12. Y. Steffen, C. Gruber, T. Schewe and H. Sies: Mono-Omethylated flavanols and other flavonoids as inhibitors of endothelial NADPH oxidase. Arch Biochem Biophys, 469 (2), 209-19 (2008)) (Pubitemid 50008450)
13. J. Stefanska and R. Pawliczak: Apocynin: molecular aptitudes. Mediators Inflamm, 2008, 106507 (2008))
14. L. R. Castor, K. A. Locatelli and V. F. Ximenes: Prooxidant activity of apocynin radical. Free Radic Biol Med, 48 (12), 1636-43 (2010))
15. S. Sorce and K. H. Krause: NOX enzymes in the central nervous system: from signaling to disease. Antioxid Redox Signal, 11 (10), 2481-504 (2009))
16. G. Y. Sun, L. A. Horrocks and A. A. Farooqui: The roles of NADPH oxidase and phospholipases A2 in oxidative and inflammatory responses in neurodegenerative diseases. J Neurochem, 103 (1), 1-16 (2007)) (Pubitemid 47404193)
17. R. M. Adibhatla and J. F. Hatcher: Lipid oxidation and peroxidation in CNS health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal, 12 (1), 125-69 (2010))
18. T. Kahles, A. Kohnen, S. Heumueller, A. Rappert, I. Bechmann, S. Liebner, I. M. Wittko, T. Neumann-Haefelin, H. Steinmetz, K. Schroeder and R. P. Brandes: NADPH oxidase Nox1 contributes to ischemic injury in experimental stroke in mice. Neurobiol Dis, 40 (1), 185-92 (2010))
19. G. C. Brown and J. J. Neher: Inflammatory neurodegeneration and mechanisms of microglial killing of neurons. Mol Neurobiol, 41 (2-3), 242-7 (2010))
20. S. S. Barbieri, V. Cavalca, S. Eligini, M. Brambilla, A. Caiani, E. Tremoli and S. Colli: Apocynin prevents cyclooxygenase 2 expression in human monocytes through NADPH oxidase and glutathione redox-dependent mechanisms. Free Radic Biol Med, 37 (2), 156-65 (2004)) (Pubitemid 38760252)
21. M. D. Jensen, W. Sheng, A. Simonyi, G. S. Johnson, A. Y. Sun and G. Y. Sun: Involvement of oxidative pathways in cytokine-induced secretory phospholipase A2-IIA in astrocytes. Neurochem Int, 55 (6), 362-8 (2009))
22. S. Pawate, Q. Shen, F. Fan and N. R. Bhat: Redox regulation of glial inflammatory response to lipopolysaccharide and interferongamma. J Neurosci Res, 77 (4), 540-51 (2004)) (Pubitemid 39007006)
23. H. M. Gao, J. Jiang, B. Wilson, W. Zhang, J. S. Hong and B. Liu: Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J Neurochem, 81 (6), 1285-97 (2002)) (Pubitemid 34809262)
24. B. Li, Y. S. Guo, M. M. Sun, H. Dong, S. Y. Wu, D. X. Wu and C. Y. Li: The NADPH oxidase is involved in lipopolysaccharide-mediated motor neuron injury. Brain Res, 1226, 199-208 (2008))
25. H. Shibata, H. Katsuki, M. Okawara, T. Kume and A. Akaike: c-Jun N-terminal kinase inhibition and alphatocopherol protect midbrain dopaminergic neurons from interferon-gamma/lipopolysaccharide-induced injury without affecting nitric oxide production. J Neurosci Res, 83 (1), 102-9 (2006)) (Pubitemid 43062014)
26. G. C. Brown: Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase. Biochem Soc Trans, 35 (Pt 5), 1119-21 (2007)) (Pubitemid 350206442)
27. H. Chen, Y. S. Song and P. H. Chan: Inhibition of NADPH oxidase is neuroprotective after ischemiareperfusion. J Cereb Blood Flow Metab, 29 (7), 1262-72 (2009))
28. T. Kahles, P. Luedike, M. Endres, H. J. Galla, H. Steinmetz, R. Busse, T. Neumann-Haefelin and R. P. Brandes: NADPH oxidase plays a central role in bloodbrain barrier damage in experimental stroke. Stroke, 38 (11), 3000-6 (2007))
29. C. E. Walder, S. P. Green, W. C. Darbonne, J. Mathias, J. Rae, M. C. Dinauer, J. T. Curnutte and G. R. Thomas: Ischemic stroke injury is reduced in mice lacking a functional NADPH oxidase. Stroke, 28 (11), 2252-8 (1997))
30. D. K. Choi, S. Koppula, M. Choi and K. Suk: Recent developments in the inhibitors of neuroinflammation and neurodegeneration: inflammatory oxidative enzymes as a drug target. Expert Opin Ther Pat, 20 (11), 1531-46 (2010))
31. J. D. Lambeth, K. H. Krause and R. A. Clark: NOX enzymes as novel targets for drug development. Semin Immunopathol, 30 (3), 339-63 (2008))
32. H. Chen, G. S. Kim, N. Okami, P. Narasimhan and P. H. Chan: NADPH oxidase is involved in post-ischemic brain inflammation. Neurobiol Dis, 42 (3), 341-8 (2011))
33. A. Y. Sun, Q. Wang, A. Simonyi and G. Y. Sun: Botanical phenolics and brain health. Neuromolecular Med, 10 (4), 259-74 (2008))
34. W. Xia, J. Han, G. Huang and W. Ying: Inflammation in ischaemic brain injury: current advances and future perspectives. Clin Exp Pharmacol Physiol, 37 (2), 253-8 (2010))
35. K. A. Jackman, A. A. Miller, T. M. De Silva, P. J. Crack, G. R. Drummond and C. G. Sobey: Reduction of cerebral infarct volume by apocynin requires pretreatment and is absent in Nox2-deficient mice. Br J Pharmacol, 156 (4), 680-8 (2009))
36. K. A. Kelly, X. Li, Z. Tan, R. L. VanGilder, C. L. Rosen and J. D. Huber: NOX2 inhibition with apocynin worsens stroke outcome in aged rats. Brain Res, 1292, 165-72 (2009))
37. Z. Gu, J. Cui, S. Brown, R. Fridman, S. Mobashery, A. Y. Strongin and S. A. Lipton: A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J Neurosci, 25 (27), 6401-8 (2005))
38. H. Yoshioka, K. Niizuma, M. Katsu, N. Okami, H. Sakata, G. S. Kim, P. Narasimhan and P. H. Chan: NADPH oxidase mediates striatal neuronal injury after transient global cerebral ischemia. J Cereb Blood Flow Metab, 31 (3), 868-80 (2011))
39. J. Shen, X. Y. Bai, Y. Qin, W. W. Jin, J. Y. Zhou, J. P. Zhou, Y. G. Yan, Q. Wang, I. C. Bruce, J. H. Chen and Q. Xia: Interrupted reperfusion reduces the activation of NADPH oxidase after cerebral I/R injury. Free Radic Biol Med, 50 (12), 1780-6 (2011))
40. H. Hong, J. S. Zeng, D. L. Kreulen, D. I. Kaufman and A. F. Chen: Atorvastatin protects against cerebral infarction via inhibition of NADPH oxidase-derived superoxide in ischemic stroke. Am J Physiol Heart Circ Physiol, 291 (5), H2210-5 (2006))
41. L. L. Tang, K. Ye, X. F. Yang and J. S. Zheng: Apocynin attenuates cerebral infarction after transient focal ischaemia in rats. J Int Med Res, 35 (4), 517-22 (2007)) (Pubitemid 47261114)
42. M. Iwai, H. W. Liu, R. Chen, A. Ide, S. Okamoto, R. Hata, M. Sakanaka, T. Shiuchi and M. Horiuchi: Possible inhibition of focal cerebral ischemia by angiotensin II type 2 receptor stimulation. Circulation, 110 (7), 843-8 (2004)) (Pubitemid 39096013)
43. C. F. Xia, H. Yin, C. V. Borlongan, L. Chao and J. Chao: Kallikrein gene transfer protects against ischemic stroke by promoting glial cell migration and inhibiting apoptosis. Hypertension, 43 (2), 452-9 (2004)) (Pubitemid 38174153)
44. H. Zhao, W. G. Mayhan, D. M. Arrick, W. Xiong and H. Sun: Alcohol-induced exacerbation of ischemic brain injury: role of NAD (P)H oxidase. Alcohol Clin Exp Res, 34 (11), 1948-55 (2010))
45. E. M. Park, S. Cho, K. Frys, G. Racchumi, P. Zhou, J. Anrather and C. Iadecola: Interaction between inducible nitric oxide synthase and poly (ADP-ribose) polymerase in focal ischemic brain injury. Stroke, 35 (12), 2896-901 (2004)) (Pubitemid 39565191)
46. I. Kusaka, G. Kusaka, C. Zhou, M. Ishikawa, A. Nanda, D. N. Granger, J. H. Zhang and J. Tang: Role of AT1 receptors and NAD (P)H oxidase in diabetes-aggravated ischemic brain injury. Am J Physiol Heart Circ Physiol, 286 (6), H2442-51 (2004)) (Pubitemid 38685263)
47. K. Murotomi, N. Takagi, S. Takeo and K. Tanonaka: NADPH oxidase-mediated oxidative damage to proteins in the postsynaptic density after transient cerebral ischemia and reperfusion. Mol Cell Neurosci, 46 (3), 681-8 (2011))
48. S. P. Green, B. Cairns, J. Rae, C. Errett-Baroncini, J. A. Hongo, R. W. Erickson and J. T. Curnutte: Induction of gp91-phox, a component of the phagocyte NADPH oxidase, in microglial cells during central nervous system inflammation. J Cereb Blood Flow Metab, 21 (4), 374-84 (2001)) (Pubitemid 32298884)
49. J. S. Zheng, R. Y. Zhan, S. S. Zheng, Y. Q. Zhou, Y. Tong and S. Wan: Inhibition of NADPH oxidase attenuates vasospasm after experimental subarachnoid hemorrhage in rats. Stroke, 36 (5), 1059-64 (2005))
50. E. Titova, R. P. Ostrowski, L. C. Sowers, J. H. Zhang and J. Tang: Effects of apocynin and ethanol on intracerebral haemorrhage-induced brain injury in rats. Clin Exp Pharmacol Physiol, 34 (9), 845-50 (2007)) (Pubitemid 47083966)
51. J. C. Fleming, M. D. Norenberg, D. A. Ramsay, G. A. Dekaban, A. E. Marcillo, A. D. Saenz, M. Pasquale-Styles, W. D. Dietrich and L. C. Weaver: The cellular inflammatory response in human spinal cords after injury. Brain, 129 (Pt 12), 3249-69 (2006)) (Pubitemid 44871440)
52. D. Impellizzeri, E. Mazzon, E. Esposito, I. Paterniti, P. Bramanti and S. Cuzzocrea: Effect of Apocynin, an inhibitor of NADPH oxidase, in the inflammatory process induced by an experimental model of spinal cord injury. Free Radic Res, 45 (2), 221-36 (2011))
53. Y. Jinnouchi, S. Yamagishi, T. Matsui, K. Takenaka, Y. Yoshida, K. Nakamura, S. Ueda and T. Imaizumi: Administration of pigment epithelium-derived factor (PEDF) inhibits cold injury-induced brain edema in mice. Brain Res, 1167, 92-100 (2007)) (Pubitemid 47302429)
54. K. Dohi, H. Ohtaki, T. Nakamachi, S. Yofu, K. Satoh, K. Miyamoto, D. Song, S. Tsunawaki, S. Shioda and T. Aruga: Gp91phox (NOX2) in classically activated microglia exacerbates traumatic brain injury. J Neuroinflammation, 7, 41 (2010))
55. M. A. Ansari and S. W. Scheff: NADPH-oxidase activation and cognition in Alzheimer disease progression. Free Radic Biol Med, 51 (1), 171-8 (2011))
56. A. J. Bruce-Keller, S. Gupta, T. E. Parrino, A. G. Knight, P. J. Ebenezer, A. M. Weidner, H. LeVine, 3rd, J. N. Keller and W. R. Markesbery: NOX activity is increased in mild cognitive impairment. Antioxid Redox Signal, 12 (12), 1371-82 (2010))
57. S. Shimohama, H. Tanino, N. Kawakami, N. Okamura, H. Kodama, T. Yamaguchi, T. Hayakawa, A. Nunomura, S. Chiba, G. Perry, M. A. Smith and S. Fujimoto: Activation of NADPH oxidase in Alzheimer's disease brains. Biochem Biophys Res Commun, 273 (1), 5-9 (2000)) (Pubitemid 30426853)
58. A. Y. Abramov, J. Jacobson, F. Wientjes, J. Hothersall, L. Canevari and M. R. Duchen: Expression and modulation of an NADPH oxidase in mammalian astrocytes. J Neurosci, 25 (40), 9176-84 (2005)) (Pubitemid 41500826)
59. V. D. Bianca, S. Dusi, E. Bianchini, I. Dal Pra and F. Rossi: Beta-amyloid activates the O-2 forming NADPH oxidase in microglia, monocytes, and neutrophils. A possible inflammatory mechanism of neuronal damage in Alzheimer's disease. J Biol Chem, 274 (22), 15493-9 (1999))
60. A. Jana and K. Pahan: Fibrillar amyloid-beta peptides kill human primary neurons via NADPH oxidase-mediated activation of neutral sphingomyelinase. Implications for Alzheimer's disease. J Biol Chem, 279 (49), 51451-9 (2004))
61. P. B. Shelat, M. Chalimoniuk, J. H. Wang, J. B. Strosznajder, J. C. Lee, A. Y. Sun, A. Simonyi and G. Y. Sun: Amyloid beta peptide and NMDA induce ROS from NADPH oxidase and AA release from cytosolic phospholipase A2 in cortical neurons. J Neurochem, 106 (1), 45-55 (2008)) (Pubitemid 351840199)
62. A. Jekabsone, P. K. Mander, A. Tickler, M. Sharpe and G. C. Brown: Fibrillar beta-amyloid peptide Abeta1-40 activates microglial proliferation via stimulating TNF-alpha release and H2O2 derived from NADPH oxidase: a cell culture study. J Neuroinflammation, 3, 24 (2006))
63. M. Li, K. Pisalyaput, M. Galvan and A. J. Tenner: Macrophage colony stimulatory factor and interferongamma trigger distinct mechanisms for augmentation of beta-amyloid-induced microglia-mediated neurotoxicity. J Neurochem, 91 (3), 623-33 (2004)) (Pubitemid 39431157)
64. A. Y. Abramov and M. R. Duchen: The role of an astrocytic NADPH oxidase in the neurotoxicity of amyloid beta peptides. Philos Trans R Soc Lond B Biol Sci, 360 (1464), 2309-14 (2005)) (Pubitemid 46682150)
65. M. L. Block: NADPH oxidase as a therapeutic target in Alzheimer's disease. BMC Neurosci, 9 Suppl 2, S8 (2008))
66. A. Simonyi, Y. He, W. Sheng, A. Y. Sun, W. G. Wood, G. A. Weisman and G. Y. Sun: Targeting NADPH oxidase and phospholipases A2 in Alzheimer's disease. Mol Neurobiol, 41 (2-3), 73-86 (2010))
67. B. L. Wilkinson and G. E. Landreth: The microglial NADPH oxidase complex as a source of oxidative stress in Alzheimer's disease. J Neuroinflammation, 3, 30 (2006))
68. Y. Abe, Y. Hashimoto, Y. Tomita, K. Terashita, S. Aiso, H. Tajima, T. Niikura, M. Matsuoka and I. Nishimoto: Cytotoxic mechanisms by M239V presenilin 2, a little-analyzed Alzheimer's disease-causative mutant. J Neurosci Res, 77 (4), 583-95 (2004)) (Pubitemid 39007010)
69. T. Niikura, M. Yamada, T. Chiba, S. Aiso, M. Matsuoka and I. Nishimoto: Characterization of V642IAbetaPP- induced cytotoxicity in primary neurons. J Neurosci Res, 77 (1), 54-62 (2004)) (Pubitemid 38850055)
70. M. Dumont, C. Stack, C. Elipenhali, N. Y. Calingasan, E. Wille and M. F. Beal: Apocynin administration does not improve behavioral and neuropathological deficits in a transgenic mouse model of Alzheimer's disease. Neurosci Lett, 492 (3), 150-4 (2011))
71. M. E. Lull, S. Levesque, M. J. Surace and M. L. Block: Chronic apocynin treatment attenuates beta amyloid plaque size and microglial number in hAPP (751) (SL) mice. PLoS One, 6 (5), e20153 (2011))
72. C. J. Barnum and M. G. Tansey: Modeling neuroinflammatory pathogenesis of Parkinson's disease. Prog Brain Res, 184, 113-32 (2010))
73. R. L. Miller, M. James-Kracke, G. Y. Sun and A. Y. Sun: Oxidative and inflammatory pathways in Parkinson's disease. Neurochem Res, 34 (1), 55-65 (2009))
74. D. C. Wu, P. Teismann, K. Tieu, M. Vila, V. Jackson-Lewis, H. Ischiropoulos and S. Przedborski: 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 U S A, 100 (10), 6145-50 (2003)) (Pubitemid 36576945)
75. H. M. Gao, B. Liu, W. Zhang and J. S. Hong: Critical role of microglial NADPH oxidase-derived free radicals in the in vitro MPTP model of Parkinson's disease. FASEB J, 17 (13), 1954-6 (2003))
76. Y. S. Kim, D. H. Choi, M. L. Block, S. Lorenzl, L. Yang, Y. J. Kim, S. Sugama, B. P. Cho, O. Hwang, S. E. Browne, S. Y. Kim, J. S. Hong, M. F. Beal and T. H. Joh: A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. FASEB J, 21 (1), 179-87 (2007)) (Pubitemid 46052555)
77. J. Rodriguez-Pallares, J. A. Parga, A. Munoz, P. Rey, M. J. Guerra and J. L. Labandeira-Garcia: Mechanism of 6- hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6-hydroxydopamineinduced degeneration of dopaminergic neurons. J Neurochem, 103 (1), 145-56 (2007)) (Pubitemid 47404195)
78. V. Anantharam, S. Kaul, C. Song, A. Kanthasamy and A. G. Kanthasamy: Pharmacological inhibition of neuronal NADPH oxidase protects against 1-methyl-4- phenylpyridinium (MPP+)-induced oxidative stress and apoptosis in mesencephalic dopaminergic neuronal cells. Neurotoxicology, 28 (5), 988-97 (2007)) (Pubitemid 47519806)
79. W. Zhang, K. Phillips, A. R. Wielgus, J. Liu, A. Albertini, F. A. Zucca, R. Faust, S. Y. Qian, D. S. Miller, C. F. Chignell, B. Wilson, V. Jackson-Lewis, S. Przedborski, D. Joset, J. Loike, J. S. Hong, D. Sulzer and L. Zecca: Neuromelanin activates microglia and induces degeneration of dopaminergic neurons: implications for progression of Parkinson's disease. Neurotox Res, 19 (1), 63-72 (2011))
80. A. C. Cristovao, D. H. Choi, G. Baltazar, M. F. Beal and Y. S. Kim: The role of NADPH oxidase 1-derived reactive oxygen species in paraquat-mediated dopaminergic cell death. Antioxid Redox Signal, 11 (9), 2105-18 (2009))
81. J. Peng, F. F. Stevenson, M. L. Oo and J. K. Andersen: Iron-enhanced paraquat-mediated dopaminergic cell death due to increased oxidative stress as a consequence of microglial activation. Free Radic Biol Med, 46 (2), 312-20 (2009))
82. H. M. Gao, B. Liu and J. S. Hong: Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J Neurosci, 23 (15), 6181-7 (2003))
83. X. Gao, X. Hu, L. Qian, S. Yang, W. Zhang, D. Zhang, X. Wu, A. Fraser, B. Wilson, P. M. Flood, M. Block and J. S. Hong: Formyl-methionyl-leucyl- phenylalanine-induced dopaminergic neurotoxicity via microglial activation: a mediator between peripheral infection and neurodegeneration? Environ Health Perspect, 116 (5), 593-8 (2008)) (Pubitemid 351864273)
84. P. Rey, A. Lopez-Real, S. Sanchez-Iglesias, A. Munoz, R. Soto-Otero and J. L. Labandeira-Garcia: Angiotensin type-1-receptor antagonists reduce 6-hydroxydopamine toxicity for dopaminergic neurons. Neurobiol Aging, 28 (4), 555-67 (2007)) (Pubitemid 46282209)
85. D. C. Wu, D. B. Re, M. Nagai, H. Ischiropoulos and S. Przedborski: The inflammatory NADPH oxidase enzyme modulates motor neuron degeneration in amyotrophic lateral sclerosis mice. Proc Natl Acad Sci U S A, 103 (32), 12132-7 (2006))
86. J. J. Marden, M. M. Harraz, A. J. Williams, K. Nelson, M. Luo, H. Paulson and J. F. Engelhardt: Redox modifier genes in amyotrophic lateral sclerosis in mice. J Clin Invest, 117 (10), 2913-9 (2007))
87. M. M. Harraz, J. J. Marden, W. Zhou, Y. Zhang, A. Williams, V. S. Sharov, K. Nelson, M. Luo, H. Paulson, C. Schoneich and J. F. Engelhardt: SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model. J Clin Invest, 118 (2), 659-70 (2008)) (Pubitemid 351206555)
88. M. C. Marchetto, A. R. Muotri, Y. Mu, A. M. Smith, G. G. Cezar and F. H. Gage: Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell, 3 (6), 649-57 (2008))
89. M. F. Beal, N. W. Kowall, D. W. Ellison, M. F. Mazurek, K. J. Swartz and J. B. Martin: Replication of the neurochemical characteristics of Huntington's disease by quinolinic acid. Nature, 321 (6066), 168-71 (1986)) (Pubitemid 16022019)
90. P. D. Maldonado, E. Molina-Jijon, J. Villeda-Hernandez, S. Galvan-Arzate, A. Santamaria and J. Pedraza-Chaverri: NAD (P)H oxidase contributes to neurotoxicity in an excitotoxic/prooxidant model of Huntington's disease in rats: protective role of apocynin. J Neurosci Res, 88 (3), 620-9 (2010))
91. A. Pitkanen and K. Lukasiuk: Molecular and cellular basis of epileptogenesis in symptomatic epilepsy. Epilepsy Behav, 14 Suppl 1, 16-25 (2009))
92. R. R. Pestana, E. R. Kinjo, M. S. Hernandes and L. R. Britto: Reactive oxygen species generated by NADPH oxidase are involved in neurodegeneration in the pilocarpine model of temporal lobe epilepsy. Neurosci Lett, 484 (3), 187-91 (2010))
93. F. Gonzalez-Scarano and J. Martin-Garcia: The neuropathogenesis of AIDS. Nat Rev Immunol, 5 (1), 69-81 (2005)) (Pubitemid 40070332)
94. R. Williams, H. Yao, F. Peng, Y. Yang, C. Bethel-Brown and S. Buch: Cooperative induction of CXCL10 involves NADPH oxidase: Implications for HIV dementia. Glia, 58 (5), 611-21 (2010))
95. H. Yao, J. E. Allen, X. Zhu, S. Callen and S. Buch: Cocaine and human immunodeficiency virus type 1 gp120 mediate neurotoxicity through overlapping signaling pathways. J Neurovirol, 15 (2), 164-75 (2009))
96. M. M. Behrens and T. J. Sejnowski: Does schizophrenia arise from oxidative dysregulation of parvalbumin-interneurons in the developing cortex? Neuropharmacology, 57 (3), 193-200 (2009))
97. M. M. Behrens, S. S. Ali, D. N. Dao, J. Lucero, G. Shekhtman, K. L. Quick and L. L. Dugan: Ketamineinduced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science, 318 (5856), 1645-7 (2007))
98. D. C. Lim and S. C. Veasey: Neural injury in sleep apnea. Curr Neurol Neurosci Rep, 10 (1), 47-52 (2010))
99. L. Hui-guo, L. Kui, Z. Yan-ning and X. Yong-jian: Apocynin attenuate spatial learning deficits and oxidative responses to intermittent hypoxia. Sleep Med, 11 (2), 205-12 (2010))
100. G. Zhan, F. Serrano, P. Fenik, R. Hsu, L. Kong, D. Pratico, E. Klann and S. C. Veasey: NADPH oxidase mediates hypersomnolence and brain oxidative injury in a murine model of sleep apnea. Am J Respir Crit Care Med, 172 (7), 921-9 (2005)) (Pubitemid 41369078)
101. Y. Zhu, P. Fenik, G. Zhan, E. Mazza, M. Kelz, G. Aston-Jones and S. C. Veasey: Selective loss of catecholaminergic wake active neurons in a murine sleep apnea model. J Neurosci, 27 (37), 10060-71 (2007))
102. J. Haorah, S. H. Ramirez, N. Floreani, S. Gorantla, B. Morsey and Y. Persidsky: Mechanism of alcohol-induced oxidative stress and neuronal injury. Free Radic Biol Med, 45 (11), 1542-50 (2008))
103. T. Doyle, L. Bryant, C. Muscoli, S. Cuzzocrea, E. Esposito, Z. Chen and D. Salvemini: Spinal NADPH oxidase is a source of superoxide in the development of morphine-induced hyperalgesia and antinociceptive tolerance. Neurosci Lett, 483 (2), 85-9 (2010))
104. B. Gorg, N. Qvartskhava, V. Keitel, H. J. Bidmon, O. Selbach, F. Schliess and D. Haussinger: Ammonia induces RNA oxidation in cultured astrocytes and brain in vivo. Hepatology, 48 (2), 567-79 (2008))
105. R. Reinehr, B. Gorg, S. Becker, N. Qvartskhava, H. J. Bidmon, O. Selbach, H. L. Haas, F. Schliess and D. Haussinger: Hypoosmotic swelling and ammonia increase oxidative stress by NADPH oxidase in cultured astrocytes and vital brain slices. Glia, 55 (7), 758-71 (2007) doi:10.1002/glia.205044 (Pubitemid 46663028)
106. Y. J. Jang, J. Kim, J. Shim, S. Byun, M. H. Oak, K. W. Lee and H. J. Lee: Kaempferol attenuates 4-hydroxynonenalinduced apoptosis in PC12 cells by directly inhibiting NADPH oxidase. J Pharmacol Exp Ther, 337 (3), 747-54 (2011))
107. V. Jaquet, J. Marcoux, E. Forest, K. G. Leidal, S. McCormick, Y. Westermaier, R. Perozzo, O. Plastre, L. Fioraso-Cartier, B. Diebold, L. Scapozza, W. M. Nauseef, F. Fieschi, K. H. Krause and K. Bedard: NOX NADPH oxidase isoforms are inhibited by celastrol with a dual mode of action. Br J Pharmacol (2011))
108. K. Decorde, P. L. Teissedre, T. Sutra, E. Ventura, J. P. Cristol and J. M. Rouanet: Chardonnay grape seed procyanidin extract supplementation prevents high-fat dietinduced obesity in hamsters by improving adipokine imbalance and oxidative stress markers. Mol Nutr Food Res, 53 (5), 659-66 (2009))
109. T. Genovese, E. Mazzon, I. Paterniti, E. Esposito, P. Bramanti and S. Cuzzocrea: Modulation of NADPH oxidase activation in cerebral ischemia/reperfusion injury in rats. Brain Res, 1372, 92-102 (2011))
110. W. Liu, R. Sood, Q. Chen, U. Sakoglu, J. Hendren, O. Cetin, M. Miyake and K. J. Liu: Normobaric hyperoxia inhibits NADPH oxidase-mediated matrix metalloproteinase-9 induction in cerebral microvessels in experimental stroke. J Neurochem, 107 (5), 1196-205 (2008))
111. X. N. Tang, B. Cairns, N. Cairns and M. A. Yenari: Apocynin improves outcome in experimental stroke with a narrow dose range. Neuroscience, 154 (2), 556-62 (2008))
112. Q. Wang, K. D. Tompkins, A. Simonyi, R. J. Korthuis, A. Y. Sun and G. Y. Sun: Apocynin protects against global cerebral ischemia-reperfusion-induced oxidative stress and injury in the gerbil hippocampus. Brain Res, 1090 (1), 182-9 (2006)) (Pubitemid 43817927)
113. S. W. Suh, E. T. Gum, A. M. Hamby, P. H. Chan and R. A. Swanson: Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase. J Clin Invest, 117 (4), 910-8 (2007)) (Pubitemid 46556747)