Differential effects of NOX4 and NOX1 on immune cell-mediated inflammation in the aortic sinus of diabetic ApoE-/- mice

Clinical Science

Volumn 130, Issue 15, 2016, Pages 1363-1374

  Marco, Elyse Di ^a,b   Gray, Stephen P ^a,b   Chew, Phyllis ^a   Kennedy, Kit ^a   Cooper, Mark E ^a   Schmidt, Harald H H W ^c   Jandeleit Dahm, Karin A M ^a,b  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Atherosclerosis; Diabetes; Inflammation; NADPH oxidase; Oxidative stress

Indexed keywords

REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; APOLIPOPROTEIN E; AUTACOID; CYTOKINE; NOX4 PROTEIN, MOUSE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA SINUS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DIABETES MELLITUS; GENE DELETION; GENE EXPRESSION REGULATION; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; INFLAMMATION; LYMPH NODE; MACROPHAGE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; AORTIC SINUS; AORTITIS; CELLULAR IMMUNITY; DEFICIENCY; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION;

ANIMALS; AORTITIS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CD4-POSITIVE T-LYMPHOCYTES; CHEMOTAXIS, LEUKOCYTE; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; GENETIC PREDISPOSITION TO DISEASE; IMMUNITY, CELLULAR; INFLAMMATION MEDIATORS; MACROPHAGES; MICE, KNOCKOUT; NADH, NADPH OXIDOREDUCTASES; NADPH OXIDASE; OXIDATIVE STRESS; PHENOTYPE; PLAQUE, ATHEROSCLEROTIC; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SINUS OF VALSALVA;

EID: 85014330866     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20160249     Document Type: Article

References (52)

1. Kannel, W.B. and McGee, D.L. (1979) Diabetes and cardiovascular disease. The Framingham study. JAMA 241, 2035-2038.
2. Beckman, J.A., Paneni, F., Cosentino, F. and Creager, M.A. (2013) Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part II. Eur. Heart J. 34, 2436-2443.
3. Guzik, T.J., Mussa, S., Gastaldi, D., Sadowski, J., Ratnatunga, C., Pillai, R. and Channon, K.M. (2002) Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 105, 1656-1662.
4. Zhang, L., Zalewski, A., Liu, Y., Mazurek, T., Cowan, S., Martin, J.L., Hofmann, S.M., Vlassara, H. and Shi, Y. (2003) Diabetes-induced oxidative stress and low-grade inflammation in porcine coronary arteries. Circulation 108, 472-478.
5. Kanter, J.E., Averill, M.M., Leboeuf, R.C. and Bornfeldt, K.E. (2008) Diabetes-accelerated atherosclerosis and inflammation. Circ. Res. 103, e116-e117.
6. Sorescu, D., Weiss, D., Lassègue, B., Clempus, R.E., Szöcs, K., Sorescu, G.P., Valppu, L., Quinn, M.T., Lambeth, J.D., Vega, J.D. et al. (2002) Superoxide production and expression of Nox family proteins in human atherosclerosis. Circulation 105, 1429-1435.
7. Lassègue, B. and Griendling, K.K. (2010) NADPH oxidases: functions and pathologies in the vasculature. Arterioscler. Thromb. Vasc. Biol. 30, 653-661.
8. 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. (2013) NADPH Oxidase 1 plays a key role in diabetes mellitus-accelerated atherosclerosis. Circulation 127, 1888-1902.
9. Sheehan, A.L., Carrell, S., Johnson, B., Stanic, B., Banfi, B. and Miller, Jr, F.J. (2011) Role for Nox1 NADPH oxidase in atherosclerosis. Atherosclerosis 216, 321-326.
10. Montezano, A.C., Burger, D., Ceravolo, G.S., Yusuf, H., Montero, M. and Touyz, R.M. (2011) Novel nox homologues in the vasculature: focusing on Nox4 and Nox5. Clin. Sci. (Lond) 120, 131-141.
11. Craige, S.M., Kant, S., Reif, M., Chen, K., Pei, Y., Angoff, R., Sugamura, K., Fitzgibbons, T. and Keaney, Jr, J.F. (2015) Endothelial NADPH oxidase 4 protects ApoE-/- mice from atherosclerotic lesions. Free Radic. Biol. Med. 89, 1-7.
12. Schurmann, C., Rezende, F., Kruse, C., Yasar, Y., Lowe, O., Fork, C., van de Sluis, B., Bremer, R., Weissmann, N., Shah, A.M. et al. (2015) The NADPH oxidase Nox4 has anti-atherosclerotic functions. Eur. Heart J. 36, 3447-3456.
13. Choy, K., Beck, K., Png, F.Y., Wu, B.J., Leichtweis, S.B., Thomas, S.R., Hou, J.Y., Croft, K.D., Mori, T.A. and Stocker, R. (2005) Processes involved in the site-specific effect of probucol on atherosclerosis in apolipoprotein E gene knockout mice. Arterioscler. Thromb. Vasc. Biol. 25, 1684-1690.
14. Goel, R., Schrank, B.R., Arora, S., Boylan, B., Fleming, B., Miura, H., Newman, P.J., Molthen, R.C. and Newman, D.K. (2008) Site-specific effects of PECAM-1 on atherosclerosis in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 28, 1996-2002.
15. Chew, P., Yuen, D.Y.C., Koh, P., Stefanovic, N., Febbraio, M.A., Kola, I., Cooper, M.E. and de Haan, J.B. (2009) Site-specific antiatherogenic effect of the antioxidant ebselen in the diabetic apolipoprotein E-deficient mouse. Arterioscler. Thromb. Vasc. Biol. 29, 823-830.
16. Libby, P. (2012) Inflammation in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 32, 2045-2051.
17. VanderLaan, P.A., Reardon, C.A. and Getz, G.S. (2004) Site specificity of atherosclerosis: site-selective responses to atherosclerotic modulators. Arterioscler. Thromb. Vasc. Biol. 24, 12-22.
18. Zhou, X., Nicoletti, A., Elhage, R. and Hansson, G.K. (2000) Transfer of CD4+ T cells aggravates atherosclerosis in immunodeficient apolipoprotein E knockout mice. Circulation 102, 2919-2922.
19. Li, Y., To, K., Kanellakis, P., Hosseini, H., Deswaerte, V., Tipping, P., Smyth, M.J., Toh, B.H., Bobik, A. and Kyaw, T. (2015) CD4+ natural killer T cells potently augment aortic root atherosclerosis by perforin- and granzyme B-dependent cytotoxicity. Circ. Res. 116, 245-254.
20. Stentz, F.B. and Kitabchi, A.E. (2005) Hyperglycemia-induced activation of human T-lymphocytes with de novo emergence of insulin receptors and generation of reactive oxygen species. Biochem. Biophys. Res. Commun. 335, 491-495.
21. Soro-Paavonen, A., Watson, A.M.D., Li, J., Paavonen, K., Koitka, A., Calkin, A.C., Barit, D., Coughlan, M.T., Drew, B.G., Lancaster, G.I. et al. (2008) Receptor for advanced glycation end products (RAGE) deficiency attenuates the development of atherosclerosis in diabetes. Diabetes 57, 2461-2469.
22. Di Marco, E., Gray, S.P., Chew, P., Koulis, C., Ziegler, A., Szyndralewiez, C., Touyz, R.M., Schmidt, H.H., Cooper, M.E., Slattery, R. and Jandeleit-Dahm, K.A. (2014) Pharmacological inhibition of NOX reduces atherosclerotic lesions, vascular ROS and immune-inflammatory responses in diabetic ApoE -/- mice. Diabetologia 57, 633-642.
23. Kleinschnitz, C., Grund, H., Wingler, K., Armitage, M.E., Jones, E., Mittal, M., Barit, D., Schwarz, T., Geis, C., Kraft, P. et al. (2010) Post-stroke inhibition of induced NADPH oxidase type 4 prevents oxidative stress and neurodegeneration. PLoS Biol 8, e1000479.
24. Gavazzi, G., Banfi, B., Deffert, C., Fiette, L., Schappi, M., Herrmann, F. and Krause, K.H. (2006) Decreased blood pressure in NOX1-deficient mice. FEBS Lett 580, 497-504.
25. Hsueh, W., Abel, E.D., Breslow, J.L., Maeda, N., Davis, R.C., Fisher, E.A., Dansky, H., McClain, D.A., McIndoe, R., Wassef, M.K. et al. (2007) Recipes for creating animal models of diabetic cardiovascular disease. Circ. Res. 100, 1415-1427.
26. Paigen, B., Morrow, A., Holmes, P.A., Mitchell, D. and Williams, R.A. (1987) Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis 68, 231-240.
27. Akbarshahi, H., Menzel, M., Posaric Bauden, M., Rosendahl, A. and Andersson, R. (2012) Enrichment of murine CD68+ CCR2+ and CD68+ CD206+ lung macrophages in acute pancreatitis-associated acute lung injury. PLoS One 7, e42654.
28. Barry-Lane, P.A., Patterson, C., van der Merwe, M., Hu, Z., Holland, S.M., Yeh, E.T.H. and Runge, M.S. (2001) p47phox is required for atherosclerotic lesion progression in ApoE-/- mice. J. Clin. Invest. 108, 1513-1522.
29. Ma, Y., Wang, W., Zhang, J., Lu, Y., Wu, W., Yan, H. and Wang, Y. (2012) Hyperlipidemia and atherosclerotic lesion development in Ldlr-deficient mice on a long-term high-fat diet. PLoS One 7, e35835.
30. Silacci, P., Desgeorges, A., Mazzolai, L., Chambaz, C. and Hayoz, D. (2001) Flow pulsatility is a critical determinant of oxidative stress in endothelial cells. Hypertension 38, 1162-1166.
31. Chiu, J.-J. and Chien, S. (2011) Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol. Rev. 91, 327-387.
32. Ago, T., Kitazono, T., Ooboshi, H., Iyama, T., Han, Y.H., Takada, J., Wakisaka, M., Ibayashi, S., Utsumi, H. and Iida, M. (2004) Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase. Circulation 109, 227-233.
33. Hwang, J., Ing, M.H., Salazar, A., Lassegue, B., Griendling, K., Navab, M., Sevanian, A. and Hsiai, T.K. (2003) Pulsatile versus oscillatory shear stress regulates NADPH oxidase subunit expression: implication for native LDL oxidation. Circ. Res. 93, 1225-1232.
34. Bayat, H., Schröder, K., Pimentel, D.R., Brandes, R.P., Verbeuren, T.J., Cohen, R.A. and Jiang, B. (2012) Activation of thromboxane receptor modulates interleukin-1ß-induced monocyte adhesion-A novel role of Nox1. Free Radic. Biol. Med. 52, 1760-1766.
35. Teupser, D., Pavlides, S., Tan, M., Gutierrez-Ramos, J.-C., Kolbeck, R. and Breslow, J.L. (2004) Major reduction of atherosclerosis in fractalkine (CX3CL1)-deficient mice is at the brachiocephalic artery, not the aortic root. Proc. Natl. Acad. Sci. U.S.A. 101, 17795-17800.
36. Potteaux, S., Gautier, E.L., Hutchison, S.B., van Rooijen, N., Rader, D.J., Thomas, M.J., Sorci-Thomas, M.G. and Randolph, G.J. (2011) Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of ApoE-/- mice during disease regression. J. Clin. Invest. 121, 2025-2036.
37. Tong, X., Khandelwal, A.R., Wu, X., Xu, Z., Yu, W., Chen, C., Zhao, W., Yang, J., Qin, Z., Weisbrod, R.M. et al. (2016) Pro-atherogenic role of smooth muscle Nox4-based NADPH oxidase. J. Mol. Cell. Cardiol. 92, 30-40.
38. Lee, J.H., Joo, J.H., Kim, J., Lim, H.J., Kim, S., Curtiss, L., Seong, J.K., Cui, W., Yabe-Nishimura, C. and Bae, Y.S. (2013) Interaction of NADPH oxidase 1 with Toll-like receptor 2 induces migration of smooth muscle cells. Cardiovasc. Res. 99, 483-493.
39. Ross, R. (1999) Atherosclerosis - an inflammatory disease. N. Engl. J. Med. 340, 115-126.
40. Kanter, J.E., Kramer, F., Barnhart, S., Averill, M.M., Vivekanandan-Giri, A., Vickery, T., Li, L.O., Becker, L., Yuan, W., Chait, A. et al. (2012) Diabetes promotes an inflammatory macrophage phenotype and atherosclerosis through acyl-CoA synthetase 1. Proc. Natl. Acad. Sci. 109, E715-E724.
41. Mohanty, P., Hamouda, W., Garg, R., Aljada, A., Ghanim, H. and Dandona, P. (2000) Glucose challenge stimulates reactive oxygen species (ROS) generation by leucocytes. J. Clin. Endocrinol. Metab. 85, 2970-2973.
42. Frostegard, J., Ulfgren, A.K., Nyberg, P., Hedin, U., Swedenborg, J., Andersson, U. and Hansson, G.K. (1999) Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Th1) and macrophage-stimulating cytokines. Atherosclerosis 145, 33-43.
43. Guzik, T.J., Hoch, N.E., Brown, K.A., McCann, L.A., Rahman, A., Dikalov, S., Goronzy, J., Weyand, C. and Harrison, D.G. (2007) Role of the T cell in the genesis of angiotensin II-induced hypertension and vascular dysfunction. J. Exp. Med. 204, 2449-2460.
44. Rincón, M., Anguita, J., Nakamura, T., Fikrig, E. and Flavell, R.A. (1997) Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells. J. Exp. Med. 185, 461-470.
45. Sharma, P., Chakraborty, R., Wang, L., Min, B., Tremblay, M.L., Kawahara, T., Lambeth, J.D. and Haque, S.J. (2008) Redox regulation of interleukin-4 signaling. Immunity 29, 551-564.
46. Wu, J., Saleh, M.A., Kirabo, A., Itani, H.A., Montaniel, K.R., Xiao, L., Chen, W., Mernaugh, R.L., Cai, H., Bernstein, K.E. et al. (2015) Immune activation caused by vascular oxidation promotes fibrosis and hypertension. J. Clin. Invest. 126, 50-67.
47. Cuff, C.A., Kothapalli, D., Azonobi, I., Chun, S., Zhang, Y., Belkin, R., Yeh, C., Secreto, A., Assoian, R.K., Rader, D.J. and Puré, E. (2001) The adhesion receptor CD44 promotes atherosclerosis by mediating inflammatory cell recruitment and vascular cell activation. J. Clin. Invest. 108, 1031-1040.
48. Veillard, N.R., Kwak, B., Pelli, G., Mulhaupt, F., James, R.W., Proudfoot, A.E. and Mach, F. (2004) Antagonism of RANTES receptors reduces atherosclerotic plaque formation in mice. Circ. Res. 94, 253-261.
49. Guan, H., Nagarkatti, P.S. and Nagarkatti, M. (2009) Role of CD44 in the differentiation of Th1 and Th2 cells: CD44-deficiency enhances the development of Th2 effectors in response to sheep RBC and chicken ovalbumin. J. Immunol. 183, 172-180.
50. Vendrov, A.E., Madamanchi, N.R., Niu, X.-L., Molnar, K.C., Runge, M., Szyndralewiez, C., Page, P. and Runge, M.S. (2010) NADPH oxidases regulate CD44 and hyaluronic acid expression in thrombin-treated vascular smooth muscle cells and in atherosclerosis. J. Biol. Chem. 285, 26545-26557.
51. Nandi, A., Estess, P. and Siegelman, M.H. (2000) Hyaluronan anchoring and regulation on the surface of vascular endothelial cells is mediated through the functionally active form of CD44. J. Biol. Chem. 275, 14939-14948.
52. Makino, Y., Cook, D.N., Smithies, O., Hwang, O.Y., Neilson, E.G., Turka, L.A., Sato, H., Wells, A.D. and Danoff, T.M. (2002) Impaired T cell function in RANTES-deficient mice. Clin. Immunol. 102, 302-309.