NOX activation by subunit interaction and underlying mechanisms in disease

Frontiers in Cellular Neuroscience

Volumn 10, Issue , 2017, Pages

  Rastogi, Radhika ^a   Geng, Xiaokun ^a,b   Li, Fengwu ^b   Ding, Yuchuan ^a,b  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Ischemia reperfusion; NAPDH oxidase; Neurodegenerative disease; NOX inhibitors; PKC; Reactive oxygen species; Stroke; TBI

Indexed keywords

2 (2 CHLOROPHENYL) 4 [3 (DIMETHYLAMINO)PHENYL] 5 METHYL 1H PYRAZOLO[4,3 C]PYRIDINE 3,6(2H,5H) DIONE; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR ANTAGONIST; APOCYNIN; CALPHOSTIN C; CHELERYTHRINE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DIPHENYLIODONIUM SALT; GSK2795039; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE FLAVOCYTOCHROME; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE P22 PHOX; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE P40 PHOX; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE P47 PHOX; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE P67 PHOX; OXIDOREDUCTASE INHIBITOR; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C DELTA; PROTEIN KINASE C THETA; RAC PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; RUBOXISTAURIN; SALIVANOLIC ACID; UNCLASSIFIED DRUG; UNINDEXED DRUG; VAS2870;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL DAMAGE; CEREBROVASCULAR ACCIDENT; CLINICAL TRIAL (TOPIC); CYTOSOL; DEGENERATIVE DISEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SYNTHESIS; HUMAN; NEUROLOGIC DISEASE; NONHUMAN; OXIDATIVE STRESS; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TRAUMATIC BRAIN INJURY;

EID: 85012042860     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2016.00301     Document Type: Article

References (106)

1. Abramov, A. Y., Canevari, L., and Duchen, M. R. (2004). β-amyloid peptides induce mitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase. J. Neurosci. 24, 565-575. doi:10.1523/jneurosci.4042-03.2004
2. Ago, T., Kuribayashi, F., Hiroaki, H., Takeya, R., Ito, T., Kohda, D., et al. (2003). Phosphorylation of p47phox directs phox homology domain from SH3 domain toward phosphoinositides, leading to phagocyte NADPH oxidase activation. Proc. Natl. Acad. Sci. U S A 100, 4474-4479. doi:10.1073/pnas.0735712100
3. Ago, T., Nunoi, H., Ito, T., and Sumimoto, H. (1999). Mechanism for phosphorylation-induced activation of the phagocyte NADPH oxidase protein p47phox. Triple replacement of serines 303, 304, and 328 with aspartates disrupts the SH3 domain-mediated intramolecular interaction in p47phox, thereby activating the oxidase. J. Biol. Chem. 274, 33644-33653. doi:10.1074/jbc.274.47.33644
4. Aoyama, T., Paik, Y.-H., Watanabe, S., Laleu, B., Gaggini, F., Fioraso-Cartier, L., et al. (2012). Nicotinamide adenine dinucleotide phosphate oxidase (NOX) in experimental liver fibrosis: GKT137831 as a novel potential therapeutic agent. Hepatology 56, 2316-2327. doi:10.1002/hep.25938
5. Arenillas, J. F. (2015). Intracranial atherosclerosis and inflammation: lessons from the East and the West. Brain Circ. 1, 47-52. doi:10.4103/2394-8108.162531
6. Ay, H., Furie, K. L., Singhal, A., Smith, W. S., Sorensen, A. G., and Koroshetz, W. S. J. (2005). An evidence-based causative classification system for acute ischemic stroke. Ann. Neurol. 58, 688-697. doi:10.1002/ana.20617
7. Bánfi, B., Malgrange, B., Knisz, J., Steger, K., Dubois-Dauphin, M., and Krause, K. H. (2004). NOX3, a superoxide-generating NADPH oxidase of the inner ear. J. Biol. Chem. 279,46065-46072. doi:10.1074/jbc.m403046200
8. Bey, E. A., Xu, B., Bhattacharjee, A., Oldfield, C. M., Zhao, X., Li, Q., et al. (2004). Protein kinase CS is required for p47phox phosphorylation and translocation in activated human monocytes. J. Immunol. 173, 5730-5738. doi:10.4049/jimmunol.173.9.5730
9. Bianca, V. D., Dusi, S., Bianchini, E., Dal Prà, I., and Rossi, F. (1999). β-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, 15493-15499. doi:10.1074/jbc.274.22.15493
10. Block, M. L., and Hong, J.-S. (2005). Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 76, 77-98. doi:10.1016/j.pneurobio.2005.06.004
11. Boillée, S., and Cleveland, D. W. (2008). Revisiting oxidative damage in ALS: microglia, Nox and mutant SOD1. J. Clin. Invest. 118, 474-478. doi:10.1172/JCI34613
12. Brennan, A. M., Suh, S. W., Won, S. J., Narasimhan, P., Kauppinen, T. M., Lee, H., et al. (2009). NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat. Neurosci. 12, 857-863. doi:10.1038/nn.2334
13. Brieger, K., Schiavone, S., Miller, F. J. Jr., and Krause, K. H. (2012). Reactive oxygen species: from health to disease. Swiss Med. Wkly. 142:w13659. doi:10.4414/smw.2012.13659
14. Bright, R., and Mochly-Rosen, D. (2005). The role of protein kinase C in cerebral ischemic and reperfusion injury. Stroke 36, 2781-2790. doi:10.1161/01.STR.0000189996.71237.f7
15. Cai, L., Stevenson, J., Geng, X., Peng, C., Ji, X., Xin, R., et al. (2016). Combining normobaric oxygen with ethanol or hypothermia prevents brain damage from thromboembolic stroke via PKC-Akt-NOX modulation. Mol. Neurobiol. doi:10.1007/s12035-016-9695-7[Epubaheadofprint].
16. Chen, H., Kim, G. S., Okami, N., Narasimhan, P., and Chan, P. H. (2011). NADPH oxidase is involved in post-ischemic brain inflammation. Neurobiol. Dis. 42, 341-348. doi:10.1016/j.nbd.2011.01.027
17. Choi, D. H., Cristóvão, A. C., Guhathakurta, S., Lee, J., Joh, T. H., Beal, M. F., et al. (2012). NADPH oxidase 1-mediated oxidative stress leads to dopamine neuron death in Parkinson’s disease. Antioxid. Redox Signal. 16, 1033-1045. doi:10.1089/ars.2011.3960
18. Chrissobolis, S., Banfi, B., Sobey, C. G., and Faraci, F. M. (2012). Role of Nox isoforms in angiotensin II-induced oxidative stress and endothelial dysfunction in brain. J. Appl. Physiol. (1985) 113,184-191. doi:10.1152/japplphysiol.00455.2012
19. Cooney, S. J., Bermudez-Sabogal, S. L., and Byrnes, K. R. (2013). Cellular and temporal expression of NADPH oxidase (NOX) isotypes after brain injury. J. Neuroinflammation 10:155. doi:10.1186/1742-2094-10-155
20. Costa, A., Scholer-Dahirel, A., and Mechta-Grigoriou, F. (2014). The role of reactive oxygen species and metabolism on cancer cells and their microenvironment. Semin. Cancer Biol. 25, 23-32. doi:10.1016/j.semcancer.2013.12.007
21. Cox, J. A., Jeng, A. Y., Sharkey, N. A., Blumberg, P. M., and Tauber, A. I. (1985). Activation of the human neutrophil nicotinamide adenine dinucleotide phosphate (NADPH)-oxidase by protein kinase C. J. Clin. Invest. 76, 1932-1938. doi:10.1172/jci112190
22. D’Autréaux, B., and Toledano, M. B. (2007). ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8, 813-824. doi:10.1038/nrm2256
23. DeLeo, F. R., Yu, L., Burritt, J. B., Loetterle, L. R., Bond, C. W., Jesaitis, A. J., et al. (1995). Mapping sites of interaction of p47-phox and flavocytochrome b with random-sequence peptide phage display libraries. Proc. Natl. Acad. Sci. U S A 92, 7110-7114. doi:10.1073/pnas.92.15.7110
24. Deliyanti, D., and Wilkinson-Berka, J. L. (2015). Inhibition of NOX1/4 with GKT137831: a potential novel treatment to attenuate neuroglial cell inflammation in the retina. J. Neuroinflammation 12:136. doi:10.1186/s12974-015-0363-z
25. Dohi, K., Ohtaki, H., Nakamachi, T., Yofu, S., Satoh, K., Miyamoto, K., et al. (2010). Gp91phox (NOX2) in classically activated microglia exacerbates traumatic brain injury. J. Neuroinflammation 7:41. doi:10.1186/1742-2094-7-41
26. Faust, L. R., el Benna, J., Babior, B. M., and Chanock, S. J. (1995). The phosphorylation targets of p47phox, a subunit of the respiratory burst oxidase. Functions of the individual target serines as evaluated by site-directed mutagenesis. J. Clin. Invest. 96,1499-1505. doi:10.1172/jci118187
27. Forreider, B., Pozivilko, D., Kawaji, Q., Geng, X., and Ding, Y. (2016). Hibernation-like neuroprotection in stroke by attenuating brain metabolic dysfunction. Prog. Neurobiol. doi:10.1016/j.pneurobio.2016.03.002[Epubaheadofprint].
28. Gandhi, S., Wood-Kaczmar, A., Yao, Z., Plun-Favreau, H., Deas, E., Klupsch, K., et al. (2009). PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death. Mol. Cell 33, 627-638. doi:10.1016/j.molcel.2009.02.013
29. Goldstein, L. B., Bushnell, C. D., Adams, R. J., Appel, L. J., Braun, L. T., Chaturvedi, S., et al. (2011). Guidelines for the primary prevention of stroke: a guideline for healthcare professionals from the American heart Association/American stroke association. Stroke 42, 517-584. doi:10.1161/STR.0b013e3181fcb238
30. Gray, S. P., and Jandeleit-Dahm, K. A. (2015). The role of NADPH oxidase in vascular disease—hypertension, atherosclerosis and stroke. Curr. Pharm. Des. 21, 5933-5944. doi:10.2174/1381612821666151029112302
31. Groemping, Y., and Rittinger, K. (2005). Activation and assembly of the NADPH oxidase: a structural perspective. Biochem. J. 386, 401-416. doi:10.1042/bj20041835
32. Hampton, M. B., and Orrenius, S. (1997). Dual regulation of caspase activity by hydrogen peroxide: implications for apoptosis. FEBS Lett. 414, 552-556. doi:10.1016/s0014-5793(97)01068-5
33. Harraz, M. M., Marden, J. J., Zhou, W., Zhang, Y., Williams, A., Sharov, V. S., et al. (2008). SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model. J. Clin. Invest. 118, 659-670. doi:10.1172/JCI34060
34. Heumüller, S., Wind, S., Barbosa-Sicard, E., Schmidt, H. H., Busse, R., Schroder, K., et al. (2008). Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51, 211-217. doi:10.1161/HYPERTENSIONAHA.107.100214
35. Hirano, K., Chen, W. S., Chueng, A. L., Dunne, A. A., Seredenina, T., Filippova, A., et al. (2015). Discovery of GSK2795039, a novel small molecule NADPH oxidase 2 inhibitor. Antioxid. Redox Signal. 23, 358-374. doi:10.1089/ars.2014.6202
36. Hirsch, E. C., and Hunot, S. (2009). Neuroinflammation in Parkinson’s disease: a target for neuroprotection? Lancet Neurol. 8, 382-397. doi:10.1016/S1474-4422(09)70062-6
37. Huang, J., and Kleinberg, M. E. (1999). Activation of the phagocyte NADPH oxidase protein p47phox. Phosphorylation controls SH3 domain-dependent binding to p22phox. J. Biol. Chem. 274, 19731-19737. doi:10.1074/jbc.274.28.19731
38. Jiang, F., Zhang, Y., and Dusting, G. J. (2011). NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance and tissue repair. Pharmacol. Rev. 63, 218-242. doi:10.1124/pr.110.002980
39. Johnson, J. L., Park, J.-W., Benna, J. E., Faust, L. P., Inanami, O., and Babior, B. M. (1998). Activation of p47phox, a cytosolic subunit of the leukocyte NADPH oxidase. Phosphorylation of ser-359 or ser-370 precedes phosphorylation at other sites and is required for activity. J. Biol. Chem. 273, 35147-35152. doi:10.1074/jbc.273.52.35147
40. Kahles, T., and Brandes, R. P. (2013). Which NADPH oxidase isoform is relevant for ischemic stroke? The case for NOX 2. Antioxid. Redox Signal. 18, 1400-1417. doi:10.1089/ars.2012.4721
41. Kamata, T. (2009). Roles of Nox1 and other Nox isoforms in cancer development. Cancer Sci. 100, 1382-1388. doi:10.1111/j.1349-7006.2009.01207.x
42. Kim, J., and Yenari, M. (2015). Hypothermia for treatment of stroke. Brain Circ. 1, 14-25. doi:10.4103/2394-8108.164997
43. Kinkade, K., Streeter, J., and Miller, F. J. (2013). Inhibition of NADPH oxidase by apocynin attenuates progression of atherosclerosis. Int. J. Mol. Sci. 14, 17017-17028. doi:10.3390/ijms140817017
44. Kleinschnitz, C., Grund, H., Wingler, K., Armitage, M. E., Jones, E., Mittal, M., et al. (2010). Post-stroke inhibition of induced NADPH oxidase type 4 prevents oxidative stress and neurodegeneration. PLoS Biol. 8:e1000479. doi:10.1371/journal.pbio.1000479
45. Kochanski, R., Peng, C., Higashida, T., Geng, X., Hüttemann, M., Guthikonda, M., et al. (2013). Neuroprotection conferred by post-ischemia ethanol therapy in experimental stroke: an inhibitory effect on hyperglycolysis and NADPH oxidase activation. J. Neurochem. 126, 113-121. doi:10.1111/jnc.12169
46. Kramer, I. M., Verhoeven, A. J., van der Bend, R. L., Weening, R. S., and Roos, D. (1988). Purified protein kinase C phosphorylates a 47-kDa protein in control neutrophil cytoplasts but not in neutrophil cytoplasts from patients with the autosomal form of chronic granulomatous disease. J. Biol. Chem. 263, 2352-2357.
47. Lambeth, J. D. (2007). Nox enzymes, ROS and chronic disease: an example of antagonistic pleiotropy. Free Radic. Biol. Med. 43, 332-347. doi:10.1016/j.freeradbiomed.2007.03.027
48. Landmesser, U., Cai, H., Dikalov, S., McCann, L., Hwang, J., Jo, H., et al. (2002). Role of p47phox in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension 40, 511-515. doi:10.1161/01.hyp.0000032100.23772.98
49. phox. J. Biol. Chem. 277, 10121-10128. doi:10.1074/jbc.M112065200
50. phox. J. Exp. Med. 180, 2329-2334. doi:10.1084/jem.180.6.2329
51. Leusen, J. H., de Boer, M., Bolscher, B. G., Hilarius, P. M., Weening, R. S., Ochs, H. D., et al. (1994b). A point mutation in gp91-phox of cytochrome b558 of the human NADPH oxidase leading to defective translocation of the cytosolic proteins p47-phox and p67-phox. J. Clin. Invest. 93, 2120-2126. doi:10.1172/jci117207
52. Leusen, J. H., Verhoeven, A. J., and Roos, D. (1996). Interactions between the components of the human NADPH oxidase: intrigues in the phox family. J. Lab. Clin. Med. 128,461-476. doi:10.2741/a117
53. Lewis, E. M., Sergeant, S., Ledford, B., Stull, N., Dinauer, M. C., and McPhail, L. C. (2010). Phosphorylation of p22phox on threonine 147 enhances NADPH oxidase activity by promoting p47phox binding. J. Biol. Chem. 285, 2959-2967. doi:10.1074/jbc.M109.030643
54. Li, J. M., and Shah, A. M. (2003). Mechanism of endothelial cell NADPH oxidase activation by angiotensin II. Role of the p47phox subunit. J. Biol. Chem. 278, 12094-12100. doi:10.1074/jbc.M209793200
55. Liu, W., Chen, Q., Liu, J., and Liu, K. J. (2011). Normobaric hyperoxia protects the blood brain barrier through inhibiting Nox2 containing NADPH oxidase in ischemic stroke. Med. Gas Res. 1:22. doi:10.1186/2045-9912-1-22
56. Liu, Z., Tuo, Y. H., Chen, J. W., Wang, Q. Y., Li, S., Li, M. C., et al. (2016). NADPH oxidase inhibitor regulates microRNAs with improved outcome after mechanical reperfusion. J. Neurointerv. Surg. doi:10.1136/neurintsurg-2016-012463[Epubaheadofprint].
57. Lu, X. Y., Wang, H. D., Xu, J. G., Ding, K., and Li, T. (2014). NADPH oxidase inhibition improves neurological outcome in experimental traumatic brain injury. Neurochem. Int. 69, 14-19. doi:10.1016/j.neuint.2014.02.006
58. Lv, P., Miao, S. B., Shu, Y. N., Dong, L. H., Liu, G., Xie, X. L., et al. (2012). Phosphorylation of smooth muscle 22a facilitates angiotensin II-induced ROS production via activation of the PKCd-P47phox axis through release of PKCd and actin dynamics and is associated with hypertrophy and hyperplasia of vascular smooth muscle cells in vitro and in vivo. Circ. Res. 111, 697-707. doi:10.1161/CIRCRESAHA.112.272013
59. Nagel, S., Genius, J., Heiland, S., Horstmann, S., Gardner, H., and Wagner, S. (2007). Diphenyleneiodonium and dimethylsulfoxide for treatment of reperfusion injury in cerebral ischemia of the rat. Brain Res. 1132, 210-217. doi:10.1016/j.brainres.2006.11.023
60. Nauseef, W. M., Volpp, B. D., McCormick, S., Leidal, K. G., and Clark, R. A. (1991). Assembly of the neutrophil respiratory burst oxidase. Protein kinase C promotes cytoskeletal and membrane association of cytosolic oxidase components. J. Biol. Chem. 266, 5911-5917.
61. Niesman, I. R., Schilling, J. M., Shapiro, L. A., Kellerhals, S. E., Bonds, J. A., Kleschevnikov, A. M., et al. (2014). Traumatic brain injury enhances neuroinflammation and lesion volume in caveolin deficient mice. J. Neuroinjlammation 11:39. doi:10.1186/1742-2094-11-39
62. O’Donnell, B. V., Tew, D. G., Jones, O. T., and England, P. J. (1993). Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem. J. 290, 41-49. doi:10.1042/bj2900041
63. Ostrowski, R. P., Tang, J., and Zhang, J. H. (2006). Hyperbaric oxygen suppresses NADPH oxidase in a rat subarachnoid hemorrhage model. Stroke 37, 1314-1318. doi:10.1161/01.STR.0000217310.88450.c3
64. Park, L., Zhou, P., Pitstick, R., Capone, C., Anrather, J., Norris, E. H., et al. (2008). Nox2-derived radicals contribute to neurovascular and behavioral dysfunction in mice overexpressing the amyloid precursor protein. Proc. Natl. Acad. Sci. USA 105,1347-1352. doi:10.1073/pnas.0711568105
65. Qin, B., Cartier, L., Dubois-Dauphin, M., Li, B., Serrander, L., and Krause, K.-H. (2006). Akey role for the microglial NADPH oxidase in APP-dependent killing of neurons. Neurobiol. Aging 27, 1577-1587. doi:10.1016/j.neurobiolaging.2005.09.036
66. phox in neutrophils. Biochem. J. 344, 859-866. doi:10.1042/0264-6021:3440859
67. 2-and systolic blood pressure in mice. Circ. Res. 89, 408-414. doi:10.1161/hh1701.096037
68. Schäbitz, W. R., Schade, H., Heiland, S., Kollmar, R., Bardutzky, J., Henninger, N., et al. (2004). Neuroprotection by hyperbaric oxygenation after experimental focal cerebral ischemia monitored by MRI. Stroke 35, 1175-1179. doi:10.1161/01.STR.0000125868.86298.8e
69. Scherz-Shouval, R., and Elazar, Z. (2007). ROS, mitochondria and the regulation of autophagy. Trends Cell Biol. 17, 422-427. doi:10.1016/j.tcb.2007.07.009
70. Shao, B., and Bayraktutan, U. (2013). Hyperglycaemia promotes cerebral barrier dysfunction through activation of protein kinase C-ß. Diabetes Obes. Metab. 15,993-999. doi:10.1111/dom.12120
71. Shao, B., and Bayraktutan, U. (2014). Hyperglycaemia promotes human brain microvascular endothelial cell apoptosis via induction of protein kinase C-ßI and prooxidant enzyme NADPH oxidase. Redox Biol. 2, 694-701. doi:10.1016/j.redox.2014.05.005
72. Sharma, N., Kapoor, M., and Nehru, B. (2016). Apocyanin, NADPH oxidase inhibitor prevents lipopolysaccharide induced a-synuclein aggregation and ameliorates motor function deficits in rats: possible role of biochemical and inflammatory alterations. Behav. Brain Res. 296, 177-190. doi:10.1016/j.bbr.2015.09.012
73. Sharma, N., and Nehru, B. (2016). Apocyanin, a microglial NADPH oxidase inhibitor prevents dopaminergic neuronal degeneration in lipopolysaccharide-induced Parkinson’s disease model. Mol. Neurobiol. 53, 3326-3337. doi:10.1007/s12035-015-9267-2
74. Shen, J., Huber, M., Zhao, E. Y., Peng, C., Li, F., Li, X., et al. (2016). Early rehabilitation aggravates brain damage after stroke via enhanced activation of nicotinamide adenine dinucleotide phosphate oxidase (NOX). Brain Res. 1648, 266-276. doi:10.1016/j.brainres.2016.08.001
75. Shimohama, S., Tanino, H., Kawakami, N., Okamura, N., Kodama, H., Yamaguchi, T., et al. (2000). Activation of NADPH oxidase in Alzheimer’s disease brains. Biochem. Biophys. Res. Commun. 273, 5-9. doi:10.1006/bbrc.2000.2897
76. Shiose, A., and Sumimoto, H. (2000). Arachidonic acid and phosphorylation synergistically induce a conformational change of p47phox to activate the phagocyte NADPH oxidase. J. Biol. Chem. 275,13793-13801. doi:10.1074/jbc.275.18.13793
77. Simpson, E. P., Yen, A. A., and Appel, S. H. (2003). Oxidative Stress: a common denominator in the pathogenesis of amyotrophic lateral sclerosis. Curr. Opin. Rheumatol. 15, 730-736. doi:10.1097/00002281-200311000-00008
78. Singhal, A. B., Wang, X., Sumii, T., Mori, T., and Lo, E. H. (2002). Effects of normobaric hyperoxia in a rat model of focal cerebral ischemia-reperfusion. J. Cereb. Blood Flow Metab. 22, 861-868. doi:10.1097/00004647-200207000-00011
79. Sorce, S., and Krause, K. H. (2009). NOX enzymes in the central nervous system: from signaling to disease. Antioxid. Redox Signal. 11, 2481-2504. doi:10.1089/ARS.2009.2578
80. Stielow, C., Catar, R. A., Muller, G., Wingler, K., Scheurer, P., Schmidt, H. H. H. W., et al. (2006). Novel Nox inhibitor of oxLDL-induced reactive oxygen species formation in human endothelial cells. Biochem. Biophys. Res. Commun. 344, 200-205. doi:10.1016/j.bbrc.2006.03.114
81. Sumimoto, H. (2008). Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 275, 3249-3277. doi:10.1111/j.1742-4658.2008.06488.x
82. Sumimoto, H., Miyano, K., and Takeya, R. (2005). Molecular composition and regulation of the Nox family NAD(P)H oxidases. Biochem. Biophys. Res. Commun. 338,677-686. doi:10.1016/j.bbrc.2005.08.210
83. Sun, Q.-A., Hess, D. T., Wang, B., Miyagi, M., and Stamler, J. S. (2012). Off-target thiol alkylation by the NADPH oxidase inhibitor 3-benzyl-7-(2-benzoxazolyl)thio-1,2,3-triazolo[4,5-d]pyrimidine (VAS2870). Free Radic. Biol. Med. 52, 1897-1902. doi:10.1016/j.freeradbiomed.2012.02.046
84. Takac, I., Schröder, K., and Brandes, R. P. (2012). The nox family of NADPH oxidases: friend or foe of the vascular system? Curr. Hypertens. Rep. 14, 70-78. doi:10.1007/s11906-011-0238-3
85. phox participate in activation of superoxide-producing NADPH oxidases. J. Biol. Chem. 278, 25234-25246. doi:10.1074/jbc.M212856200
86. Tang, X. N., Cairns, B., Cairns, N., and Yenari, M. A. (2008). Apocynin improves outcome in experimental stroke with a narrow dose range. Neuroscience 154, 556-562. doi:10.1016/j.neuroscience.2008.03.090
87. Tang, X. N., Cairns, B., Kim, J. Y., and Yenari, M. A. (2012). NADPH oxidase in stroke and cerebrovascular disease. Neurol. Res. 34, 338-345. doi:10.1179/1743132812Y.0000000021
88. Tang, H., Pan, C. S., Mao, X. W., Liu, Y. Y., Yan, L., Zhou, C. M., et al. (2014). Role of NADPH oxidase in total salvianolic acid injection attenuating ischemia-reperfusion impaired cerebral microcirculation and neurons: implication of AMPK/Akt/PKC. Microcirculation 21, 615-627. doi:10.1111/micc.12140
89. Tang, X. N., Zheng, Z., Giffard, R. G., and Yenari, M. A. (2011). Significance of marrow-derived nicotinamide adenine dinucleotide phosphate oxidase in experimental ischemic stroke. Ann. Neurol. 70, 606-615. doi:10.1002/ana.22476
90. Teixeira, G., Szyndralewiez, C., Molango, S., Carnesecchi, S., Heitz, F., Wiesel, P., et al. (2016). Therapeutic potential of NOX1/4 inhibitors. Br. J. Pharmacol. doi:10.1111/bph.13532[Epubaheadofprint].
91. Thallas-Bonke, V., Thorpe, S. R., Coughlan, M. T., Fukami, K., Yap, F. Y., Sourris, K. C., et al. (2008). Inhibition of NADPH oxidase prevents advanced glycation end product-mediated damage in diabetic nephropathy through a protein kinase C-a-dependent pathway. Diabetes 57, 460-469. doi:10.2337/db08-0406
92. Tsunawaki, S., and Yoshikawa, K. (2000). Relationships of p40phox with p67phox in the activation and expression of the human respiratory burst NADPH oxidase. J. Biochem. 128, 777-783. doi:10.1093/oxfordjournals.jbchem.a022815
93. Ushio-Fukai, M., and Nakamura, Y. (2008). Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett. 266, 37-52. doi:10.1016/j.canlet.2008.02.044
94. Wang, Y.-Y., Chen, C.-J., Lin, S.-Y., Chuang, Y.-H., Sheu, W. H.-H., and Tung, K.-C. (2013). Hyperglycemia is associated with enhanced gluconeogenesis in a rat model of permanent cerebral ischemia. Mol. Cell. Endocrinol. 367, 50-56. doi:10.1016/j.mce.2012.12.016
95. Wang, Q., Tompkins, K. D., Simonyi, A., Korthuis, R. J., Sun, A. Y., and Sun, G. Y. (2006). Apocynin protects against global cerebral ischemia-reperfusion-induced oxidative stress and injury in the gerbil hippocampus. Brain Res. 1090,182-189. doi:10.1016/j.brainres.2006.03.060
96. Wassmann, S., Laufs, U., Muller, K., Konkol, C., Ahlbory, K., Baumer, A. T., et al. (2002). Cellular antioxidant effects of atorvastatin in vitro and in vivo. Arterioscler. Thromb. Vasc. Biol. 22, 300-305. doi:10.1161/hq0202.104081
97. Wei, X. F., Zhou, Q. G., Hou, F. F., Liu, B. Y., and Liang, M. (2009). Advanced oxidation protein products induce mesangial cell perturbation through PKC-dependent activation of NADPH oxidase. Am. J. Physiol. Renal. Physiol. 296, F427-F437. doi:10.1152/ajprenal.90536.2008
98. Williams, H. C. (2007). NADPH oxidase inhibitors: new antihypertensive agents? J. Cardiovasc. Pharmacol. 50, 9-16. doi:10.1097/fjc.0b013e318063e820
99. Won, S. J., Tang, X. N., Suh, S. W., Yenari, M. A., and Swanson, R. A. (2011). Hyperglycemia promotes tissue plasminogen activator-induced hemorrhage by Increasing superoxide production. Ann. Neurol. 70, 583-590. doi:10.1002/ana.22538
100. Woodfin, A., Hu, D. E., Sarker, M., Kurokawa, T., and Fraser, P. (2011). Acute NADPH oxidase activation potentiates cerebrovascular permeability response to bradykinin in ischemia-reperfusion. Free Radic. Biol. Med. 50, 518-524. doi:10.1016/j.freeradbiomed.2010.12.010
101. Wu, D.-C., Ré, D. B., Nagai, M., Ischiropoulos, H., and Przedborski, S. (2006). The inflammatory NADPH oxidase enzyme modulates motor neuron degeneration in amyotrophic lateral sclerosis mice. Proc. Natl. Acad. Sci. U S A 103, 12132-12137. doi:10.1073/pnas.0603670103
102. Xia, C., Meng, Q., Liu, L. Z., Rojanasakul, Y., Wang, X. R., and Jiang, B. H. (2007). Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res. 67, 10823-10830. doi:10.1158/0008-5472.can-07-0783
103. Yan, S., Liu, G., Pei, C., Chen, W., Li, P., Wang, Q., et al. (2015). Inhibition of NADPH oxidase protects against metastasis of human lung cancer by decreasing microRNA-21. Anticancer Drugs 26, 388-398. doi:10.1097/CAD.0000000000000198
104. Yu, L., Quinn, M. T., Cross, A. R., and Dinauer, M. C. (1998). Gp91phox is the heme binding subunit of the superoxide-generating NADPH oxidase. Proc. Natl. Acad. Sci. USA 95,7993-7998. doi:10.1073/pnas.95.14.7993
105. Zawada, W. M., Banninger, G. P., Thornton, J., Marriott, B., Cantu, D., Rachubinski, A. L., et al. (2011). Generation of reactive oxygen species in 1-methyl-4-phenylpyridinium (MPP+) treated dopaminergic neurons occurs as an NADPH oxidase-dependent two-wave cascade. J. Neuroinflammation 8:129. doi:10.1186/1742-2094-8-129
106. Zawada, W. M., Mrak, R. E., Biedermann, J., Palmer, Q. D., Gentleman, S. M., Aboud, O., et al. (2015). Loss of angiotensin II receptor expression in dopamine neurons in Parkinson’s disease correlates with pathological progression and is accompanied by increases in Nox4-and 8-OH guanosine-related nucleic acid oxidation and caspase-3 activation. Acta Neuropathol. Commun. 3:9. doi:10.1186/s40478-015-0189-z