Nrf2 deficiency aggravates Angiotensin II-induced cardiac injury by increasing hypertrophy and enhancing IL-6/STAT3-dependent inflammation

Dandan Chen1, Zhe Li2,3,4, Peiqing Bao1, Miao Chen1, Miao Zhang1, Fangrong Yan5, Yitao Xu6, Caoyu Ji5, Xinyue Hu1, Daniel Sanchis7, Yubin Zhang1, Junmei Ye1
1State Key Laboratory of Natural Medicines, Department of Biochemistry, School of Life Science and Technology, China Pharmaceutical University, Nanjing 210006, China
2Department of Cardiology, Renmin Hospital of Wuhan University, Wuhan 430060, China
3Cardiovascular Research Institute, Wuhan University, Wuhan 430060, China
4Hubei Key Laboratory of Cardiology Wuhan 430060, China
5Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing 210006, China
6Division of Cancer, Department of Surgery and Cancer, Imperial College London, London W120NN, United Kingdom
7Institut de Recerca Biomedica de Lleida (IRBLLEIDA), Universitat de Lleida, Edifici Biomedicina-I. Av. Rovira Roure, 80, 25198 Lleida, Spain

Tài liệu tham khảo

Swynghedauw, 1999 Dahlof, 2002, Cardiovascular morbidity and mortality in the Losartan Intervention For End point reduction in hypertension study (LIFE): a randomised trial against atenolol, Lancet, 359, 995, 10.1016/S0140-6736(02)08089-3 Swynghedauw, 2010, Molecular mechanisms in evolutionary cardiology failure, Ann. N. Y. Acad. Sci., 1188, 58, 10.1111/j.1749-6632.2009.05084.x Diaz, 2018, Angiotensin II requires an intact cardiac thyrotropin-releasing hormone (TRH) system to induce cardiac hypertrophy in mouse, J. Mol. Cell. Cardiol., 24, 1, 10.1016/j.yjmcc.2018.09.009 P.C. Group, 2001, Randomised trial of a perindopril-based blood-pressure-lowering regimen among 6,105 individuals with previous stroke or transient ischaemic attack, Lancet, 358, 1033, 10.1016/S0140-6736(01)06178-5 Fox, 2003, Efficacy of perindopril in reduction of cardiovascular events among patients with stable coronary artery disease: randomised, double-blind, placebo-controlled, multicentre trial (the EUROPA study), Lancet, 362, 782, 10.1016/S0140-6736(03)14286-9 Yusuf, 2000, Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators, N. Engl. J. Med., 342, 145, 10.1056/NEJM200001203420301 Sadoshima, 1993, Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro, Cell, 75, 977, 10.1016/0092-8674(93)90541-W Sugden, 2001, Mechanotransduction in Cardiomyocyte Hypertrophy, Circulation, 103, 1375, 10.1161/01.CIR.103.10.1375 Yang, 2018, Deletion of protein kinase B2 preserves cardiac function by blocking interleukin-6-mediated injury and restores blood pressure during angiotensin II/high-salt-diet-induced hypertension, J. Hypertens., 36, 834, 10.1097/HJH.0000000000001613 Al, 2016, Binding of EBP50 to Nox organizing subunit p47phox is pivotal to cellular reactive species generation and altered vascular phenotype, Proc. Natl. Acad. Sci. U. S. A., 113 Choi, 2016, Preservation of myocardial fatty acid oxidation prevents diastolic dysfunction in mice subjected to angiotensin II infusion, J. Mol. Cell. Cardiol., 100, 64, 10.1016/j.yjmcc.2016.09.001 Takayanagi, 2015, Role of epidermal growth factor receptor and endoplasmic reticulum stress in vascular remodeling induced by angiotensin II, Hypertension, 65, 1349, 10.1161/HYPERTENSIONAHA.115.05344 Lau, 2013, The predicted molecular weight of Nrf2: it is what it is not, Antioxid. Redox Signal., 18, 91, 10.1089/ars.2012.4754 Rojo de la Vega, 2018, NRF2 and the hallmarks of cancer, Cancer Cell., 34, 21, 10.1016/j.ccell.2018.03.022 Best, 2018, Synergy between the KEAP1/NRF2 and PI3K pathways drives non-small-cell lung cancer with an altered immune microenvironment, Cell Metab., 27, 935, 10.1016/j.cmet.2018.02.006 Chartoumpekis, 2018, Nrf2 prevents Notch-induced insulin resistance and tumorigenesis in mice, JCI Insight, 3, 10.1172/jci.insight.97735 Kuda, 2018, Nrf2-mediated antioxidant defense and peroxiredoxin 6 are linked to biosynthesis of palmitic acid ester of 9-hydroxystearic acid, Diabetes, 67, 1190, 10.2337/db17-1087 Wang, 2014, Nrf2 enhances myocardial clearance of toxic ubiquitinated proteins, J. Mol. Cell. Cardiol., 72, 305, 10.1016/j.yjmcc.2014.04.006 Li, 2011, Up-regulation of p27kip1 contributes to Nrf2-mediated protection against angiotensin II-induced cardiac hypertrophy, Carbohydr. Res., 90, 315 Qin, 2015, Nrf2-mediated cardiac maladaptive remodeling and dysfunction in a setting of autophagy insufficiency, Hypertension, 67, 107, 10.1161/HYPERTENSIONAHA.115.06062 Lee, 2003, Identification of the NF-E2-related Factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis, J. Biol. Chem., 278, 12029, 10.1074/jbc.M211558200 Nguyen, 2009, The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress, J. Biol. Chem., 284, 13291, 10.1074/jbc.R900010200 Li, 2009, Molecular mechanisms of Nrf2-mediated antioxidant response, Mol. Carcinog., 48, 91, 10.1002/mc.20465 Ma, 2013, Role of Nrf2 in oxidative stress and toxicity, Annu. Rev. Pharmacol. Toxicol., 53, 401, 10.1146/annurev-pharmtox-011112-140320 Kensler, 2006, Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway, Annu. Rev. Pharmacol. Toxicol., 47, 89, 10.1146/annurev.pharmtox.46.120604.141046 Li, 2009, Nrf2 protects against maladaptive cardiac responses to hemodynamic stress, Arterioscler. Thromb. Vasc. Biol., 29, 1843, 10.1161/ATVBAHA.109.189480 Barančík, 2016, Nrf2 as a key player of redox regulation in cardiovascular diseases, Physiol. Res., 65, S1, 10.33549/physiolres.933403 Erkens, 2015, Left ventricular diastolic dysfunction in Nrf2 knock out mice Is associated with cardiac hypertrophy, decreased expression of SERCA2a, and preserved endothelial function, Free Radic. Biol. Med., 89, 906, 10.1016/j.freeradbiomed.2015.10.409 Chen, 2017, Interleukin-6 deficiency attenuates angiotensin II-induced cardiac pathogenesis with increased myocyte hypertrophy, Biochem. Biophys. Res. Commun., 494, 534, 10.1016/j.bbrc.2017.10.119 Fredj, 2005, Role of interleukin-6 in cardiomyocyte/cardiac fibroblast interactions during myocyte hypertrophy and fibroblast proliferation, J. Cell. Physiol., 204, 428, 10.1002/jcp.20307 Sano, 2000, Autocrine/Paracrine secretion of IL-6 family cytokines causes angiotensin II-induced delayed STAT3 activation, Biochem. Biophys. Res. Commun., 269, 798, 10.1006/bbrc.2000.2364 Mann, 2003, Stress-activated cytokines and the heart: from adaptation to maladaptation, Annu. Rev. Physiol., 65, 81, 10.1146/annurev.physiol.65.092101.142249 Yang, 2007, STAT3 regulates cytokine-mediated generation of inflammatory helper T cells, J. Biol. Chem., 282, 9358, 10.1074/jbc.C600321200 Loperena, 2018, Hypertension and increased endothelial mechanical stretch promote monocyte differentiation and activation: Roles of STAT3, interleukin 6 and hydrogen peroxide, Cardiovasc. Res., 114, 1547, 10.1093/cvr/cvy112 Wruck, 2011, Nrf2 induces interleukin-6 (IL-6) expression via an antioxidant response element within the IL-6 promoter, J. Biol. Chem., 286, 4493, 10.1074/jbc.M110.162008 Minami, 2018, Prognostic significance of CD68, CD163 and folate receptor-β positive macrophages in hepatocellular carcinoma, Exp. Ther. Med., 15 Boytard, 2013, Role of proinflammatory CD68(+) mannose receptor(−) macrophages in peroxiredoxin-1 expression and in abdominal aortic aneurysms in humans, Arterioscler. Thromb. Vasc. Biol., 33, 431, 10.1161/ATVBAHA.112.300663 Chen, 2017, AKT2 deficiency induces retardation of myocyte development through EndoG-MEF2A signaling in mouse heart, Biochem. Biophys. Res. Commun., 493, 1410, 10.1016/j.bbrc.2017.09.149 Ye, 2012, Translation of myocyte enhancer factor-2 is induced by hypertrophic stimuli in cardiomyocytes through a calcineurin-dependent pathway, J. Mol. Cell. Cardiol., 53, 578, 10.1016/j.yjmcc.2012.07.013 Naya, 2002, Mitochondrial deficiency and cardiac sudden death in mice lacking the MEF2A transcription factor, Nat. Med., 8, 1303, 10.1038/nm789 Marfella, 2013, Circulating microRNA changes in heart failure patients treated with cardiac resynchronization therapy: responders vs. non-responders, Eur. J. Heart Fail., 15, 10.1093/eurjhf/hft088 Sardu, 2014, Functional role of miRNA in cardiac resynchronization therapy, Pharmacogenomics, 15, 10.2217/pgs.14.76 Sardu, 2016, Cardiac resynchronization therapy outcomes in type 2 diabetic patients: role of microRNA changes, J. Diabetes Res., 2016, 10.1155/2016/7292564 Sardu, 2018, Cardiovasc. Diabetol., 17, 137, 10.1186/s12933-018-0778-9 Sardu, 2018, Inflammatory cytokines and SIRT1 levels in subcutaneous abdominal fat: relationship with cardiac performance in overweight pre-diabetics patients, Front. Physiol., 9, 1030, 10.3389/fphys.2018.01030 Vicario, 2006, Effects of volume loading on strain rate and tissue Doppler velocity imaging in patients with idiopathic dilated cardiomyopathy, J. Cardiovasc. Med. (Hagerstown), 7, 852, 10.2459/01.JCM.0000253826.44234.09 Sardu, 2018, Stretch, injury and inflammation markers evaluation to predict clinical outcomes after implantable cardioverter defibrillator therapy in heart failure patients with metabolic syndrome, Front. Physiol., 9, 758, 10.3389/fphys.2018.00758 Ichikawa, 2009, Dihydro-CDDO-trifluoroethyl amide (dh404), a novel Nrf2 activator, suppresses oxidative stress in cardiomyocytes, PLoS One, 4, 10.1371/journal.pone.0008391 He, 2009, Nrf2 is critical in defense against high glucose-induced oxidative damage in cardiomyocytes, J. Mol. Cell. Cardiol., 46, 47, 10.1016/j.yjmcc.2008.10.007 Nako, 2012, Novel mechanism of angiotensin II-induced cardiac injury in hypertensive rats: the critical role of ASK1 and VEGF, Hypertens. Res., 35, 194, 10.1038/hr.2011.175 Soliman, 2017, Antihypertensive therapies and left ventricular hypertrophy, Curr. Hypertens. Rep., 19, 79, 10.1007/s11906-017-0777-3 Fagard, 2009, Regression of left ventricular mass by antihypertensive treatment: a meta-analysis of randomized comparative studies, Hypertension, 54, 1084, 10.1161/HYPERTENSIONAHA.109.136655 Dahlof, 1992, Reversal of cardiovascular structural changes when treating essential hypertension. The importance of the renin-angiotensin-aldosterone system, Am. J. Hypertens., 5, 900, 10.1093/ajh/5.12.900 Schmieder, 1996, Reversal of left ventricular hypertrophy in essential hypertension. A meta-analysis of randomized double-blind studies, JAMA, 275, 1507, 10.1001/jama.1996.03530430051039 Wang, 2016, Scutellarin protects cardiomyocyte ischemia–reperfusion injury by reducing apoptosis and oxidative stress, Life Sci., 157, 200, 10.1016/j.lfs.2016.01.018 Drenckhahn, 2015, Impaired myocardial development resulting in neonatal cardiac hypoplasia alters postnatal growth and stress response in the heart, Cardiovasc. Res., 106, 43, 10.1093/cvr/cvv028 Xu, 2006, Myocyte enhancer factors 2A and 2C induce dilated cardiomyopathy in transgenic mice, J. Biol. Chem., 281, 9152, 10.1074/jbc.M510217200 Kweider, 2011, Interplay between vascular endothelial growth factor (VEGF) and nuclear factor erythroid 2-related factor-2 (Nrf2): implications for preeclampsia, J. Biol. Chem., 286, 42863, 10.1074/jbc.M111.286880 Betz, 1998, Postnatally induced inactivation of gp130 in mice results in neurological, cardiac, hematopoietic, immunological, hepatic, and pulmonary defects, J. Exp. Med., 188, 1955, 10.1084/jem.188.10.1955 Hilfiker-Kleiner, 2004, Signal transducer and activator of transcription 3 is required for myocardial capillary growth, control of interstitial matrix deposition, and heart protection from ischemic injury, Circ. Res., 95, 187, 10.1161/01.RES.0000134921.50377.61 Hirota, 1999, Loss of a gp130 cardiac muscle cell survival pathway is a critical event in the onset of heart failure during biomechanical stress, Cell, 97, 189, 10.1016/S0092-8674(00)80729-1