NOX4-derived reactive oxygen species limit fibrosis and inhibit proliferation of vascular smooth muscle cells in diabetic atherosclerosis

Lassègue, 2003, Vascular NAD(P)H oxidases: specific features, expression, and regulation, Am. J. Physiol. – Regul. Integr. Comp. Physiol., 285, R277, 10.1152/ajpregu.00758.2002 Clempus, 2007, Nox4 is required for maintenance of the differentiated vascular smooth muscle cell phenotype, Arterioscler. Thromb. Vasc. Biol., 27, 42, 10.1161/01.ATV.0000251500.94478.18 Schroder, 2009, Nox4 acts as a switch between differentiation and proliferation in preadipocytes, Arterioscler. Thromb. Vasc. Biol., 29, 239, 10.1161/ATVBAHA.108.174219 Schroder, 2012, Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase, Circ. Res., 110, 1217, 10.1161/CIRCRESAHA.112.267054 Goettsch, 2013, NADPH oxidase 4 limits bone mass by promoting osteoclastogenesis, J. Clin. Investig., 123, 4731, 10.1172/JCI67603 Di Marco, 2015, Are reactive oxygen species still the basis for diabetic complications?, Clin. Sci., 129, 199, 10.1042/CS20150093 Craige, 2015, Endothelial NADPH oxidase 4 protects ApoE−/− mice from atherosclerotic lesions, Free Radic. Biol. Med., 89, 1, 10.1016/j.freeradbiomed.2015.07.004 Schurmann, 2015, The NADPH oxidase Nox4 has anti-atherosclerotic functions, Eur. Heart J., 10.1093/eurheartj/ehv460 Gray, 2015, Reactive oxygen species can provide atheroprotection via NOX4-dependent inhibition of inflammation and vascular remodeling, Arterioscler. Thromb. Vasc. Biol. Langbein, 2016, NADPH oxidase 4 protects against development of endothelial dysfunction and atherosclerosis in LDL receptor deficient mice, Eur. Heart J., 37, 1753, 10.1093/eurheartj/ehv564 Gomez, 2012, Smooth muscle cell phenotypic switching in atherosclerosis, Cardiovasc. Res., 95, 156, 10.1093/cvr/cvs115 Shankman, 2015, KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis, Nat. Med., 21, 628, 10.1038/nm.3866 Steitz, 2001, Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers, Circ. Res., 89, 1147, 10.1161/hh2401.101070 Speer, 2009, Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries, Circ. Res., 104, 733, 10.1161/CIRCRESAHA.108.183053 Owens, 2004, Molecular regulation of vascular smooth muscle cell differentiation in development and disease, Physiol. Rev., 84, 767, 10.1152/physrev.00041.2003 Pandolfi, 2003, Phenotype modulation in cultures of vascular smooth muscle cells from diabetic rats: association with increased nitric oxide synthase expression and superoxide anion generation, J. Cell. Physiol., 196, 378, 10.1002/jcp.10325 Mori, 2002, Hyperglycemia-induced alteration of vascular smooth muscle phenotype, J. Diabetes Complicat., 16, 65, 10.1016/S1056-8727(01)00189-1 Inaba, 1996, Normalization of diabetes by xenotransplantation of cryopreserved microencapsulated pancreatic islets. Application of a new strategy in islet banking, Transplantation, 61, 175, 10.1097/00007890-199601270-00001 Takemoto, 2000, Enhanced expression of osteopontin in human diabetic artery and analysis of its functional role in accelerated atherogenesis, Arterioscler. Thromb. Vasc. Biol., 20, 624, 10.1161/01.ATV.20.3.624 Lyle, 2014, Hydrogen peroxide regulates osteopontin expression through activation of transcriptional and translational pathways, J. Biol. Chem., 289, 275, 10.1074/jbc.M113.489641 Kleinschnitz, 2010, Post-stroke inhibition of induced nadph oxidase type 4 prevents oxidative stress and neurodegeneration, PLoS Biol., 8, e1000479, 10.1371/journal.pbio.1000479 Hsueh, 2007, Recipes for creating animal models of diabetic cardiovascular disease, Circ. Res., 100, 1415, 10.1161/01.RES.0000266449.37396.1f Lee, 2009, Mechanisms of vascular smooth muscle NADPH oxidase 1 (Nox1) contribution to injury-induced neointimal formation, Arterioscler. Thromb. Vasc. Biol., 29, 480, 10.1161/ATVBAHA.108.181925 Brown, 2014, Poldip2 knockout results in perinatal lethality, reduced cellular growth and increased autophagy of mouse embryonic fibroblasts, PLoS One, 9, e96657, 10.1371/journal.pone.0096657 Gray, 2013, NADPH Oxidase 1 plays a key role in diabetes mellitus-accelerated atherosclerosis, Circulation, 127, 1888, 10.1161/CIRCULATIONAHA.112.132159 Williams, 2012, Role of coronin 1B in PDGF-induced migration of vascular smooth muscle cells, Circ. Res., 111, 56, 10.1161/CIRCRESAHA.111.255745 Stanic, 2010, An oxidized extracellular oxidation-reduction state increases Nox1 expression and proliferation in vascular smooth muscle cells via epidermal growth factor receptor activation, Arterioscler. Thromb. Vasc. Biol., 30, 2234, 10.1161/ATVBAHA.110.207639 Lassègue, 2001, Novel gp91phox homologues in vascular smooth muscle cells: Nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways, Circ. Res., 88, 888, 10.1161/hh0901.090299 Seshiah, 2002, Activated monocytes induce smooth muscle cell death: role of macrophage colony-stimulating factor and cell contact, Circulation, 105, 174, 10.1161/hc0202.102248 Gadeau, 1993, Osteopontin overexpression is associated with arterial smooth muscle cell proliferation in vitro, Arterioscler. Thromb., 13, 120, 10.1161/01.ATV.13.1.120 Arnold, 2001, Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1, Proc. Natl. Acad. Sci. USA, 98, 5550, 10.1073/pnas.101505898 Shinohara, 2008, Alternative translation of osteopontin generates intracellular and secreted isoforms that mediate distinct biological activities in dendritic cells, Proc. Natl. Acad. Sci. USA, 105, 7235, 10.1073/pnas.0802301105 Inoue, 2011, Intracellular osteopontin (iOPN) and immunity, Immunol. Res., 49, 160, 10.1007/s12026-010-8179-5 MacLeod, 1994, Proliferation and extracellular matrix synthesis of smooth muscle cells cultured from human coronary atherosclerotic and restenotic lesions, J. Am. Coll. Cardiol., 23, 59, 10.1016/0735-1097(94)90502-9 Babelova, 2012, Role of Nox4 in murine models of kidney disease, Free Radic. Biol. Med., 53, 842, 10.1016/j.freeradbiomed.2012.06.027 Cucoranu, 2005, NAD(P)H oxidase 4 mediates transforming growth factor-beta1-induced differentiation of cardiac fibroblasts into myofibroblasts, Circ. Res., 97, 900, 10.1161/01.RES.0000187457.24338.3D Amara, 2010, NOX4/NADPH oxidase expression is increased in pulmonary fibroblasts from patients with idiopathic pulmonary fibrosis and mediates TGFbeta1-induced fibroblast differentiation into myofibroblasts, Thorax, 65, 733, 10.1136/thx.2009.113456 Martin-Garrido, 2011, NADPH oxidase 4 mediates TGF-beta-induced smooth muscle alpha-actin via p38MAPK and serum response factor, Free Radic. Biol. Med., 50, 354, 10.1016/j.freeradbiomed.2010.11.007 Jarman, 2014, An inhibitor of NADPH oxidase-4 attenuates established pulmonary fibrosis in a rodent disease model, Am. J. Respir. Cell Mol. Biol., 50, 158 Carnesecchi, 2011, A key role for NOX4 in epithelial cell death during development of lung fibrosis, Antioxid. Redox Signal., 15, 607, 10.1089/ars.2010.3829 Rhyu, 2012, Role of reactive oxygen species in transforming growth factor-beta1-induced extracellular matrix accumulation in renal tubular epithelial cells, Transplant. Proc., 44, 625, 10.1016/j.transproceed.2011.12.054 Tong, 2016, Pro-atherogenic role of smooth muscle Nox4-based NADPH oxidase, J. Mol. Cell. Cardiol., 10.1016/j.yjmcc.2016.01.020