Inhibition of NADPH oxidase by apocynin attenuates progression of atherosclerosis

International Journal of Molecular Sciences

Volumn 14, Issue 8, 2013, Pages 17017-17028

  Kinkade, Kara ^a   Streeter, Jennifer ^a   Miller Jr , Francis J ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Apocynin; Atherosclerosis; NADPH oxidase; Superoxide

Indexed keywords

APOCYNIN; APOLIPOPROTEIN E; CHOLESTEROL; DRINKING WATER; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ABDOMINAL AORTA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ARCH; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; DISEASE COURSE; DISEASE MODEL; ENZYME INHIBITION; FEMALE; FLOW CYTOMETRY; GRANULOCYTE; HYPERCHOLESTEROLEMIA; MALE; MOUSE; NONHUMAN; RESPIRATORY BURST; THORACIC AORTA;

ACETOPHENONES; ANIMALS; AORTA, ABDOMINAL; ATHEROSCLEROSIS; FEMALE; HYPERCHOLESTEROLEMIA; LEUKOCYTES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NADPH OXIDASE; PROTEIN TRANSPORT; RESPIRATORY BURST; SUPEROXIDES;

EID: 84883170266     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140817017     Document Type: Article

References (34)

1. Lassegue, B.; Griendling, K.K. NADPH oxidases: Functions and pathologies in the vasculature. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 653-661.
2. Azumi, H.; Inoue, N.; Takeshita, S.; Rikitake, Y.; Kawashima, S.; Hayashi, Y.; Itoh, H.; Yokoyama, M. Expression of NADH/NADPH oxidase p22phox in human coronary arteries. Circulation 1999, 100, 1494-1498.
3. Sorescu, D.; Weiss, D.; Lassegue, B.; Clempus, R.E.; Szocs, K.; Sorescu, G.P.; Valppu, L.; Quinn, M.T.; Lambeth, J.D.; Vega, J.D.; et al. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 2002, 105, 1429-1435.
4. Guzik, T.J.; Sadowski, J.; Guzik, B.; Jopek, A.; Kapelak, B.; Przybylowski, P.; Wierzbicki, K.; Korbut, R.; Harrison, D.G.; Channon, K.M. Coronary artery superoxide production and nox isoform expression in human coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 2006, 26, 333-339.
5. Guzik, T.J.; Chen, W.; Gongora, M.C.; Guzik, B.; Lob, H.E.; Mangalat, D.; Hoch, N.; Dikalov, S.; Rudzinski, P.; Kapelak, B.; Sadowski, J.; Harrison, D.G. Calcium-dependent NOX5 nicotinamide adenine dinucleotide phosphate oxidase contributes to vascular oxidative stress in human coronary artery disease. J. Am. Coll. Cardiol. 2008, 52, 1803-1809.
6. Madrigal-Matute, J.; Fernandez-Garcia, C.E.; Gomez-Guerrero, C.; Lopez-Franco, O.; Munoz-Garcia, B.; Egido, J.; Blanco-Colio, L.M.; Martin-Ventura, J.L. HSP90 inhibition by 17-DMAG attenuates oxidative stress in experimental atherosclerosis. Cardiovasc. Res. 2012, 95, 116-123.
7. Kirk, E.A.; Dinauer, M.C.; Rosen, H.; Chait, A.; Heinecke, J.W.; LeBoeuf, R.C. Impaired superoxide production due to a deficiency in phagocyte NADPH oxidase fails to inhibit atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 2000, 20, 1529-1535.
8. Barry-Lane, P.A.; Patterson, C.; van der Merwe, M.; Hu, Z.Y.; Holland, S.M.; Yeh, E.T.H.; Runge, M.S. p47phox is required for atherosclerotic lesion progression in ApoE(-/-) mice. J. Clin. Invest. 2001, 108, 1513-1522.
9. Vendrov, A.E.; Hakim, Z.S.; Madamanchi, N.R.; Rojas, M.; Madamanchi, C.; Runge, M.S. Atherosclerosis is attenuated by limiting superoxide generation in both macrophages and vessel wall cells. Arterioscler. Thromb. Vasc. Biol. 2007, 27, 2714-2721.
10. Judkins, C.P.; Diep, H.; Broughton, B.R.; Mast, A.E.; Hooker, E.U.; Miller, A.A.; Selemidis, S.; Dusting, G.J.; Sobey, C.G.; Drummond, G.R. Direct evidence of a role for Nox2 in superoxide production, reduced nitric oxide bioavailability, and early atherosclerotic plaque formation in ApoE-/-mice. Am. J. Physiol. Heart Circ. Physiol. 2010, 298, H24-H32.
11. Sheehan, A.L.; Carrell, S.; Johnson, B.; Stanic, B.; Banfi, B.; Miller, F.J., Jr. Role for Nox1 NADPH oxidase in atherosclerosis. Atherosclerosis 2011, 216, 321-326.
12. Douglas, G.; Bendall, J.K.; Crabtree, M.J.; Tatham, A.L.; Carter, E.E.; Hale, A.B.; Channon, K.M. Endothelial-specific Nox2 overexpression increases vascular superoxide and macrophage recruitment in ApoE(-)/(-) mice. Cardiovasc. Res. 2012, 94, 20-29.
13. Thomas, M.; Gavrila, D.; McCormick, M.L.; Miller, F.J., Jr.; Daugherty, A.; Cassis, L.A.; Dellsperger, K.C.; Weintraub, N.L. Deletion of p47phox attenuates angiotensin II-induced abdominal aortic aneurysm formation in apolipoprotein E-deficient mice. Circulation 2006, 114, 404-413.
14. Hsich, E.; Segal, B.H.; Pagano, P.J.; Rey, F.E.; Paigen, B.; Deleonardis, J.; Hoyt, R.F.; Holland, S.M.; Finkel, T. Vascular effects following homozygous disruption of p47(phox): An essential component of NADPH oxidase. Circulation 2000, 101, 1234-1236.
15. Gray, S.P.; di Marco, E.; Okabe, J.; Szyndralewiez, C.; Heitz, F.; Montezano, A.C.; de Haan, J.B.; Koulis, C.; El-Osta, A.; Andrews, K.L.; et al. NADPH oxidase 1 plays a key role in diabetes mellitus-accelerated atherosclerosis. Circulation 2013, 127, 1888-1902.
16. Miller, F.J., Jr.; Sharp, W.J.; Fang, X.; Oberley, L.W.; Oberley, T.D.; Weintraub, N.L. Oxidative stress in human abdominal aortic aneurysms: A potential mediator of aneurysmal remodeling. Arterioscler. Thromb. Vasc. Biol. 2002, 22, 560-565.
17. Stolk, J.; Hiltermann, T.J.; Dijkman, J.H.; Verhoeven, A.J. Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol. Am. J. Respir. Cell Mol. Biol. 1994, 11, 95-102.
18. Barbieri, S.S.; Cavalca, V.; Eligini, S.; Brambilla, M.; Caiani, A.; Tremoli, E.; Colli, S. Apocynin prevents cyclooxygenase 2 expression in human monocytes through NADPH oxidase and glutathione redox-dependent mechanisms. Free Radic. Biol. Med. 2004, 37, 156-165.
19. Hathaway, C.A.; Heistad, D.D.; Piegors, D.J.; Miller, F.J., Jr. Regression of atherosclerosis in monkeys reduces vascular superoxide levels. Circ. Res. 2002, 90, 277-283.
20. Miller, F.J., Jr.; Gutterman, D.D.; Rios, C.D.; Heistad, D.D.; Davidson, B.L. Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis. Circ. Res. 1998, 82, 1298-1305.
21. Heumuller, S.; Wind, S.; Barbosa-Sicard, E.; Schmidt, H.H.; Busse, R.; Schroder, K.; Brandes, R.P. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 2008, 51, 211-217.
22. Lassegue, B.; San Martin, A.; Griendling, K.K. Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ. Res. 2012, 110, 1364-1390.
23. Drummond, G.R.; Selemidis, S.; Griendling, K.K.; Sobey, C.G. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat. Rev. Drug Discov. 2011, 10, 453-471.
24. Johnson, D.K.; Schillinger, K.J.; Kwait, D.M.; Hughes, C.V.; McNamara, E.J.; Ishmael, F.; O'Donnell, R.W.; Chang, M.M.; Hogg, M.G.; Dordick, J.S.; et al. Inhibition of NADPH oxidase activation in endothelial cells by ortho-methoxy-substituted catechols. Endothelium 2002, 9, 191-203.
25. Cheret, C.; Gervais, A.; Lelli, A.; Colin, C.; Amar, L.; Ravassard, P.; Mallet, J.; Cumano, A.; Krause, K.H.; Mallat, M. Neurotoxic activation of microglia is promoted by a nox1-dependent NADPH oxidase. J. Neurosci. 2008, 28, 12039-12051.
26. Banfi, B.; Clark, R.A.; Steger, K.; Krause, K.H. Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J. Biol. Chem. 2003, 278, 3510-3513.
27. Wu, M.C.; Ho, H.I.; Lee, T.W.; Wu, H.L.; Lo, J.M. In vivo examination of 111In-bis-5HT-DTPA to target myeloperoxidase in atherosclerotic ApoE knockout mice. J. Drug Target. 2012, 20, 605-614.
28. Liu, C.; Desikan, R.; Ying, Z.; Gushchina, L.; Kampfrath, T.; Deiuliis, J.; Wang, A.; Xu, X.; Zhong, J.; Rao, X.; et al. Effects of a novel pharmacologic inhibitor of myeloperoxidase in a mouse atherosclerosis model. PLoS One 2012, 7, e50767.
29. Castor, L.R.; Locatelli, K.A.; Ximenes, V.F. Pro-oxidant activity of apocynin radical. Free Radic. Biol. Med. 2010, 48, 1636-1643.
30. Kinoshita, H.; Matsumura, T.; Ishii, N.; Fukuda, K.; Senokuchi, T.; Motoshima, H.; Kondo, T.; Taketa, K.; Kawasaki, S.; Hanatani, S.; et al. Apocynin suppresses the progression of atherosclerosis in apoE-deficient mice by inactivation of macrophages. Biochem. Biophys. Res. Commun. 2013, 431, 124-130.
31. Streeter, J.; Thiel, W.; Brieger, K.; Miller, F.J., Jr. Opportunity Nox: The future of NADPH oxidases as therapeutic targets in cardiovascular disease. Cardiovasc. Ther. 2013, 31, 125-137.
32. Xu, S.; Shriver, A.S.; Jagadeesha, D.K.; Chamseddine, A.; Szocs, K.; Weintraub, N.L.; Griendling, K.K.; Bhalla, R.; Miller, F.J., Jr. Increased expression of Nox1 in neointimal smooth muscle cells promotes activation of matrix metalloproteinase-9. J. Vasc. Res. 2012, 49, 242-248.
33. Vuorte, J.; Jansson, S.E.; Repo, H. Standardization of a flow cytometric assay for phagocyte respiratory burst activity. Scand. J. Immunol. 1996, 43, 329-334.
34. Ochs, H.D.; Igo, R.P. The NBT slide test: A simple screening method for detecting chronic granulomatous disease and female carriers. J. Pediatr. 1973, 83, 77-82.