NADPH oxidase-2 and atherothrombosis: Insight from chronic granulomatous disease

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 37, Issue 2, 2017, Pages 218-225

  Violi, Francesco ^a   Carnevale, Roberto ^a   Loffredo, Lorenzo ^a   Pignatelli, Pasquale ^a   Gallin, John I ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

atherosclerosis; eicosanoids; foam cells; monocytes; oxidative stress

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; ANTITHROMBOCYTIC AGENT; CYBB PROTEIN, HUMAN; CYBB PROTEIN, MOUSE; ENZYME INHIBITOR; MEMBRANE PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ATHEROSCLEROSIS; CHRONIC GRANULOMATOUS DISEASE; EXPERIMENTAL STUDY; HUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; THROMBOCYTE AGGREGATION; THROMBOSIS; VASCULAR SMOOTH MUSCLE CELL; VASOCONSTRICTION; VASODILATATION; ANIMAL; ANTAGONISTS AND INHIBITORS; ARTERY; ATHEROSCLEROTIC PLAQUE; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; SIGNAL TRANSDUCTION; THROMBOCYTE;

ANIMALS; ARTERIES; ATHEROSCLEROSIS; BLOOD PLATELETS; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; GRANULOMATOUS DISEASE, CHRONIC; HUMANS; MEMBRANE GLYCOPROTEINS; MICE, KNOCKOUT; NADPH OXIDASE; OXIDATIVE STRESS; PLAQUE, ATHEROSCLEROTIC; PLATELET AGGREGATION INHIBITORS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; THROMBOSIS;

EID: 85004125679     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.116.308351     Document Type: Review

References (55)

1. Badimon L, Vilahur G. Thrombosis formation on atherosclerotic lesions and plaque rupture. J Intern Med. 2014;276:618-632. doi: 10.1111/ joim.12296.
2. Violi F, Pignatelli P, Basili S. Nutrition, supplements, and vitamins in platelet function and bleeding. Circulation. 2010;121:1033-1044. doi: 10.1161/CIRCULATIONAHA.109.880211.
3. Violi F, Pignatelli P. Clinical application of NOX activity and other oxidative biomarkers in cardiovascular disease: a critical review. Antioxid Redox Signal. 2015;23:514-532. doi: 10.1089/ars.2013.5790.
4. Roos D. Chronic granulomatous disease. Br Med Bull. 2016;118:50-63. doi: 10.1093/bmb/ldw009.
5. Lekstrom-Himes JA, Gallin JI. Immunodeficiency diseases caused by defects in phagocytes. N Engl J Med. 2000;343:1703-1714. doi: 10.1056/ NEJM200012073432307.
6. Dayal S, Wilson KM, Motto DG, Miller FJ Jr, Chauhan AK, Lentz SR. Hydrogen peroxide promotes aging-related platelet hyperactivation and thrombosis. Circulation. 2013;127:1308-1316. doi: 10.1161/ CIRCULATIONAHA.112.000966.
7. Kuhns DB, Alvord WG, Heller T, Feld JJ, Pike KM, Marciano BE, Uzel G, DeRavin SS, Priel DA, Soule BP, Zarember KA, Malech HL, Holland SM, Gallin JI. Residual NADPH oxidase and survival in chronic granulomatous disease. N Engl J Med. 2010;363:2600-2610. doi: 10.1056/ NEJMoa1007097.
8. Violi F, Sanguigni V, Carnevale R, et al. Hereditary deficiency of gp91(phox) is associated with enhanced arterial dilatation: results of a multicenter study. Circulation. 2009;120:1616-1622. doi: 10.1161/ CIRCULATIONAHA.109.877191.
9. Pignatelli P, Carnevale R, Di Santo S, Bartimoccia S, Sanguigni V, Lenti L, Finocchi A, Mendolicchio L, Soresina AR, Plebani A, Violi F. Inherited human gp91phox deficiency is associated with impaired isoprostane formation and platelet dysfunction. Arterioscler Thromb Vasc Biol. 2011;31:423-434. doi: 10.1161/ATVBAHA.110.217885.
10. Sibley CT, Estwick T, Zavodni A, et al. Assessment of atherosclerosis in chronic granulomatous disease. Circulation. 2014;130:2031-2039. doi: 10.1161/CIRCULATIONAHA.113.006824.
11. Judkins CP, Diep H, Broughton BR, Mast AE, Hooker EU, Miller AA, Selemidis S, Dusting GJ, Sobey CG, Drummond GR. 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. doi: 10.1152/ ajpheart.00799.2009.
12. Walsh TG, Berndt MC, Carrim N, Cowman J, Kenny D, Metharom P. The role of Nox1 and Nox2 in GPVI-dependent platelet activation and thrombus formation. Redox Biol. 2014;2:178-186. doi: 10.1016/j. redox.2013.12.023.
13. Matsuno K, Yamada H, Iwata K, Jin D, Katsuyama M, Matsuki M, Takai S, Yamanishi K, Miyazaki M, Matsubara H, Yabe-Nishimura C. Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation. 2005;112:2677-2685. doi: 10.1161/ CIRCULATIONAHA.105.573709.
14. Cathcart MK. Regulation of superoxide anion production by NADPH oxidase in monocytes/macrophages: contributions to atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:23-28. doi: 10.1161/01. ATV.0000097769.47306.12.
15. Violi F, Sanguigni V, Loffredo L, Carnevale R, Buchetti B, Finocchi A, Tesauro M, Rossi P, Pignatelli P. Nox2 is determinant for ischemiainduced oxidative stress and arterial vasodilatation: a pilot study in patients with hereditary Nox2 deficiency. Arterioscler Thromb Vasc Biol. 2006;26:e131-e132. doi: 10.1161/01.ATV.0000229710.13054.2d.
16. Loffredo L, Carnevale R, Sanguigni V, et al. Does NADPH oxidase deficiency cause artery dilatation in humans? Antioxid Redox Signal. 2013;18:1491-1496. doi: 10.1089/ars.2012.4987.
17. Loukogeorgakis SP, van den Berg MJ, Sofat R, Nitsch D, Charakida M, Haiyee B, de Groot E, MacAllister RJ, Kuijpers TW, Deanfield JE. Role of NADPH oxidase in endothelial ischemia/reperfusion injury in humans. Circulation. 2010;121:2310-2316. doi: 10.1161/ CIRCULATIONAHA.108.814731.
18. Brown DI, Griendling KK. Nox proteins in signal transduction. Free Radic Biol Med. 2009;47:1239-1253. doi: 10.1016/j.freeradbiomed.2009.07.023.
19. Schürmann C, Rezende F, Kruse C, Yasar Y, Löwe O, Fork C, van de Sluis B, Bremer R, Weissmann N, Shah AM, Jo H, Brandes RP, Schröder K. The NADPH oxidase Nox4 has anti-atherosclerotic functions. Eur Heart J. 2015;36:3447-3456. doi: 10.1093/eurheartj/ehv460.
20. Langbein H, Brunssen C, Hofmann A, Cimalla P, Brux M, Bornstein SR, Deussen A, Koch E, Morawietz H. NADPH oxidase 4 protects against development of endothelial dysfunction and atherosclerosis in LDL receptor deficient mice. Eur Heart J. 2016;37:1753-1761. doi: 10.1093/ eurheartj/ehv564.
21. Mancini GB, Dahlöf B, Díez J. Surrogate markers for cardiovascular disease: structural markers. Circulation. 2004;109(25 suppl 1):IV22-IV30. doi: 10.1161/01.CIR.0000133443.77237.2f.
22. Violi F, Pignatelli P, Pignata C, Plebani A, Rossi P, Sanguigni V, Carnevale R, Soresina A, Finocchi A, Cirillo E, Catasca E, Angelico F, Loffredo L. Reduced atherosclerotic burden in subjects with genetically determined low oxidative stress. Arterioscler Thromb Vasc Biol. 2013;33:406-412. doi: 10.1161/ATVBAHA.112.300438.
23. Leiding JW, Marciano BE, Zerbe CS, Deravin SS, Malech HL, Holland SM. Diabetes, renal and cardiovascular disease in p47 phox-/-chronic granulomatous disease. J Clin Immunol. 2013;33:725-730. doi: 10.1007/ s10875-013-9871-8.
24. Khatri JJ, Johnson C, Magid R, Lessner SM, Laude KM, Dikalov SI, Harrison DG, Sung HJ, Rong Y, Galis ZS. Vascular oxidant stress enhances progression and angiogenesis of experimental atheroma. Circulation. 2004;109:520-525. doi: 10.1161/01.CIR.0000109698.70638.2B.
25. 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.
26. Guzik TJ, Sadowski J, Guzik B, Jopek A, Kapelak B, Przybylowski P, Wierzbicki K, Korbut R, Harrison DG, Channon KM. Coronary artery superoxide production and nox isoform expression in human coronary artery disease. Arterioscler Thromb Vasc Biol. 2006;26:333-339. doi: 10.1161/01.ATV.0000196651.64776.51.
27. Kirk EA, Dinauer MC, Rosen H, Chait A, Heinecke JW, LeBoeuf RC. 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.
28. Barry-Lane PA, Patterson C, van der Merwe M, Hu Z, Holland SM, Yeh ET, Runge MS. p47phox is required for atherosclerotic lesion progression in ApoE(-/-) mice. J Clin Invest. 2001;108:1513-1522. doi: 10.1172/ JCI11927.
29. Xu F, Liu Y, Shi L, Liu W, Zhang L, Cai H, Qi J, Cui Y, Wang W, Hu Y. NADPH oxidase p47phox siRNA attenuates adventitial fibroblasts proliferation and migration in apoE(-/-) mouse. J Transl Med. 2015;13:38. doi: 10.1186/s12967-015-0407-2.
30. Hsich E, Segal BH, Pagano PJ, Rey FE, Paigen B, Deleonardis J, Hoyt RF, Holland SM, Finkel T. Vascular effects following homozygous disruption of p47(phox): an essential component of NADPH oxidase. Circulation. 2000;101:1234-1236.
31. Quesada IM, Lucero A, Amaya C, Meijles DN, Cifuentes ME, Pagano PJ, Castro C. Selective inactivation of NADPH oxidase 2 causes regression of vascularization and the size and stability of atherosclerotic plaques. Atherosclerosis. 2015;242:469-475. doi: 10.1016/j. atherosclerosis.2015.08.011.
32. Liu Y, Davidson BP, Yue Q, Belcik T, Xie A, Inaba Y, McCarty OJ, Tormoen GW, Zhao Y, Ruggeri ZM, Kaufmann BA, Lindner JR. Molecular imaging of inflammation and platelet adhesion in advanced atherosclerosis effects of antioxidant therapy with NADPH oxidase inhibition. Circ Cardiovasc Imaging. 2013;6:74-82. doi: 10.1161/CIRCIMAGING.112.975193.
33. Csányi G, Taylor WR, Pagano PJ. NOX and inflammation in the vascular adventitia. Free Radic Biol Med. 2009;47:1254-1266. doi: 10.1016/j. freeradbiomed.2009.07.022.
34. Konior A, Schramm A, Czesnikiewicz-Guzik M, Guzik TJ. NADPH oxidases in vascular pathology. Antioxid Redox Signal. 2014;20:2794-2814. doi: 10.1089/ars.2013.5607.
35. -/- mice. Cardiovasc Res. 2012;94:20-29. doi: 10.1093/cvr/cvs026.
36. Meijles DN, Fan LM, Ghazaly MM, Howlin B, Krönke M, Brooks G, Li JM. p22phox C242T single-nucleotide polymorphism inhibits inflammatory oxidative damage to endothelial cells and vessels. Circulation. 2016;133:2391-2403. doi: 10.1161/CIRCULATIONAHA.116.021993.
37. Guzik TJ, West NE, Black E, McDonald D, Ratnatunga C, Pillai R, Channon KM. Functional effect of the C242T polymorphism in the NAD(P)H oxidase p22phox gene on vascular superoxide production in atherosclerosis. Circulation. 2000;102:1744-1747.
38. Arca M, Conti B, Montali A, Pignatelli P, Campagna F, Barillà F, Tanzilli G, Verna R, Vestri A, Gaudio C, Violi F. C242T polymorphism of NADPH oxidase p22phox and recurrence of cardiovascular events in coronary artery disease. Arterioscler Thromb Vasc Biol. 2008;28:752-757. doi: 10.1161/ATVBAHA.107.154823.
39. Li JM, Fan LM, Christie MR, Shah AM. Acute tumor necrosis factor alpha signaling via NADPH oxidase in microvascular endothelial cells: role of p47phox phosphorylation and binding to TRAF4. Mol Cell Biol. 2005;25:2320-2330. doi: 10.1128/MCB.25.6.2320-2330.2005.
40. Cook-Mills JM, Marchese ME, Abdala-Valencia H. Vascular cell adhesion molecule-1 expression and signaling during disease: regulation by reactive oxygen species and antioxidants. Antioxid Redox Signal. 2011;15:1607-1638. doi: 10.1089/ars.2010.3522.
41. Li H, Förstermann U. Nitric oxide in the pathogenesis of vascular disease. J Pathol. 2000;190:244-254.
42. Pratic D. Prostanoid and isoprostanoid pathways in atherogenesis. Atherosclerosis. 2008;201:8-16. doi: 10.1016/j. atherosclerosis.2008.04.037.
43. Cyrus T, Yao Y, Ding T, Dogné JM, Pratic D. Thromboxane receptor blockade improves the antiatherogenic effect of thromboxane A2 suppression in LDLR KO mice. Blood. 2007;109:3291-3296. doi: 10.1182/ blood-2006-08-044990.
44. Violi F, Pignatelli P. Platelet oxidative stress and thrombosis. Thromb Res. 2012;129:378-381. doi: 10.1016/j.thromres.2011.12.002.
45. Freedman JE. Oxidative stress and platelets. Arterioscler Thromb Vasc Biol. 2008;28:s11-s16. doi: 10.1161/ATVBAHA.107.159178.
46. Pignatelli P, Pulcinelli FM, Lenti L, Gazzaniga PP, Violi F. Hydrogen peroxide is involved in collagen-induced platelet activation. Blood. 1998;91:484-490.
47. Cadenas E. Basic mechanisms of antioxidant activity. Biofactors. 1997;6:391-397.
48. Carnevale R, Bartimoccia S, Nocella C, Di Santo S, Loffredo L, Illuminati G, Lombardi E, Boz V, Del Ben M, De Marco L, Pignatelli P, Violi F. LDL oxidation by platelets propagates platelet activation via an oxidative stress-mediated mechanism. Atherosclerosis. 2014;237:108-116. doi: 10.1016/j.atherosclerosis.2014.08.041.
49. Delaney MK, Kim K, Estevez B, Xu Z, Stojanovic-Terpo A, Shen B, Ushio-Fukai M, Cho J, Du X. Differential roles of the NADPH-oxidase 1 and 2 in platelet activation and thrombosis. Arterioscler Thromb Vasc Biol. 2016;36:846-854. doi: 10.1161/ATVBAHA.116.307308.
50. Kim K, Li J, Tseng A, Andrews RK, Cho J. NOX2 is critical for heterotypic neutrophil-platelet interactions during vascular inflammation. Blood. 2015;126:1952-1964. doi: 10.1182/blood-2014-10-605261.
51. Pignatelli P, Carnevale R, Cangemi R, Loffredo L, Sanguigni V, Stefanutti C, Basili S, Violi F. Atorvastatin inhibits gp91phox circulating levels in patients with hypercholesterolemia. Arterioscler Thromb Vasc Biol. 2010;30:360-367. doi: 10.1161/ATVBAHA.109.198622.
52. Pignatelli P, Pastori D, Carnevale R, Farcomeni A, Cangemi R, Nocella C, Bartimoccia S, Vicario T, Saliola M, Lip GY, Violi F. Serum NOX2 and urinary isoprostanes predict vascular events in patients with atrial fibrillation. Thromb Haemost. 2015;113:617-624. doi: 10.1160/ TH14-07-0571.
53. Carnevale R, Pignatelli P, Lenti L, Buchetti B, Sanguigni V, Di Santo S, Violi F. LDL are oxidatively modified by platelets via GP91(phox) and accumulate in human monocytes. FASEB J. 2007;21:927-934. doi: 10.1096/fj.06-6908com.
54. Rösen-Wolff A, Soldan W, Heyne K, Bickhardt J, Gahr M, Roesler J. Increased susceptibility of a carrier of X-linked chronic granulomatous disease (CGD) to Aspergillus fumigatus infection associated with agerelated skewing of lyonization. Ann Hematol. 2001;80:113-115.
55. Pignatelli P, Carnevale R, Pastori D, Cangemi R, Napoleone L, Bartimoccia S, Nocella C, Basili S, Violi F. Immediate antioxidant and antiplatelet effect of atorvastatin via inhibition of Nox2. Circulation. 2012;126:92-103. doi: 10.1161/CIRCULATIONAHA.112.095554.