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Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Review Article

Resveratrol and Cardiac Fibrosis Prevention and Treatment

Author(s): Parinaz Zivarpour, Željko Reiner, Jamal Hallajzadeh* and Liaosadat Mirsafaei

Volume 23, Issue 2, 2022

Published on: 12 February, 2021

Page: [190 - 200] Pages: 11

DOI: 10.2174/1389201022666210212125003

Price: $65

Abstract

Cardiovascular diseases are some of the major causes of morbidity and mortality in developed and developing countries. Cardiac fibrosis is one of the most often pathological changes of heart tissues. It occurs as a result of extracellular matrix proteins accumulation at myocardia. Cardiac fibrosis results in impaired cardiac systolic and diastolic functions and is associated with other effects. Therapies with medicines have not been sufficiently successful in treating chronic diseases such as CVD. Therefore, the interest for therapeutic potential of natural compounds and medicinal plants has increased. Plants such as grapes, berries and peanuts contain a polyphenolic compound called "resveratrol" which has been reported to have various therapeutic properties for a variety of diseases. Studies on laboratory models show that resveratrol has beneficial effects on cardiovascular diseases, including myocardial infarction, high blood pressure cardiomyopathy, thrombosis, cardiac fibrosis, and atherosclerosis. In vitro animal models using resveratrol indicated protective effects on the heart by neutralizing reactive oxygen species, preventing inflammation, increasing neoangiogenesis, dilating blood vessels, suppressing apoptosis and delaying atherosclerosis. In this review, we are presenting experimental and clinical results of studies concerning resveratrol effects on cardiac fibrosis as a CVD outcome in humans.

Keywords: Cardiovascular disease, cardiomyopathy, cardiac fibrosis, resveratrol, cardiovascular remodeling, thrombosis, atherosclerosis.

Graphical Abstract

[1]
Mach, F.; Baigent, C.; Catapano, A.L.; Koskinas, K.C.; Casula, M.; Badimon, L.; Chapman, M.J.; De Backer, G.G.; Delgado, V.; Ference, B.A.; Graham, I.M.; Halliday, A.; Landmesser, U.; Mihaylova, B.; Pedersen, T.R.; Riccardi, G.; Richter, D.J.; Sabatine, M.S.; Taskinen, M.R.; Tokgozoglu, L.; Wiklund, O. ESC Scientific Document Group. 2019 ESC/EAS Guidelines for the management of dyslipidaemias: lipid modification to reduce cardiovascular risk. Eur. Heart J., 2020, 41(1), 111-188.
[http://dx.doi.org/10.1093/eurheartj/ehz455] [PMID: 31504418]
[2]
Dobaczewski, M.; Frangogiannis, N.G. Chemokines and cardiac fibrosis. Front. Biosci. (Schol. Ed.), 2009, 1, 391-405.
[http://dx.doi.org/10.2741/s33] [PMID: 19482709]
[3]
Kong, P.; Christia, P.; Frangogiannis, N.G. The pathogenesis of cardiac fibrosis. Cell. Mol. Life Sci., 2014, 71(4), 549-574.
[http://dx.doi.org/10.1007/s00018-013-1349-6] [PMID: 23649149]
[4]
Berk, B.C.; Fujiwara, K.; Lehoux, S. ECM remodeling in hypertensive heart disease. J. Clin. Invest., 2007, 117(3), 568-575.
[http://dx.doi.org/10.1172/JCI31044] [PMID: 17332884]
[5]
Ma, Z-G.; Yuan, Y-P.; Wu, H-M.; Zhang, X.; Tang, Q-Z. Cardiac fibrosis: new insights into the pathogenesis. Int. J. Biol. Sci., 2018, 14(12), 1645-1657.
[http://dx.doi.org/10.7150/ijbs.28103] [PMID: 30416379]
[6]
Weber, K.T.; Brilla, C.G. Pathological hypertrophy and cardiac interstitium. Fibrosis and renin-angiotensin-aldosterone system. Circulation, 1991, 83(6), 1849-1865.
[http://dx.doi.org/10.1161/01.CIR.83.6.1849] [PMID: 1828192]
[7]
Frangogiannis, N.G. Cardiac fibrosis: Cell biological mechanisms, molecular pathways and therapeutic opportunities. Mol. Aspects Med., 2019, 65, 70-99.
[http://dx.doi.org/10.1016/j.mam.2018.07.001] [PMID: 30056242]
[8]
Banerjee, I.; Yekkala, K.; Borg, T.K.; Baudino, T.A. Dynamic interactions between myocytes, fibroblasts, and extracellular matrix. Ann. N. Y. Acad. Sci., 2006, 1080(1), 76-84.
[http://dx.doi.org/10.1196/annals.1380.007] [PMID: 17132776]
[9]
Chilton, L.; Giles, W.R.; Smith, G.L. Evidence of intercellular coupling between co-cultured adult rabbit ventricular myocytes and myofibroblasts. J. Physiol., 2007, 583(Pt 1), 225-236.
[http://dx.doi.org/10.1113/jphysiol.2007.135038] [PMID: 17569734]
[10]
Frangogiannis, N.G. Regulation of the inflammatory response in cardiac repair. Circ. Res., 2012, 110(1), 159-173.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.243162] [PMID: 22223212]
[11]
Nagueh, S.F.; Mikati, I.; Weilbaecher, D.; Reardon, M.J.; Al-Zaghrini, G.J.; Cacela, D.; He, Z.X.; Letsou, G.; Noon, G.; Howell, J.F.; Espada, R.; Verani, M.S.; Zoghbi, W.A. Relation of the contractile reserve of hibernating myocardium to myocardial structure in humans. Circulation, 1999, 100(5), 490-496.
[http://dx.doi.org/10.1161/01.CIR.100.5.490] [PMID: 10430762]
[12]
Aggarwal, M.; Aggarwal, B.; Rao, J. Integrative medicine for cardiovascular disease and prevention. Med. Clin. North Am., 2017, 101(5), 895-923.
[http://dx.doi.org/10.1016/j.mcna.2017.04.007] [PMID: 28802470]
[13]
Cicero, A.F.G.; Colletti, A.; Bajraktari, G.; Descamps, O.; Djuric, D.M.; Ezhov, M.; Fras, Z.; Katsiki, N.; Langlois, M.; Latkovskis, G.; Panagiotakos, D.B.; Paragh, G.; Mikhailidis, D.P.; Mitchenko, O.; Paulweber, B.; Pella, D.; Pitsavos, C.; Reiner, Ž.; Ray, K.K.; Rizzo, M.; Sahebkar, A.; Serban, M.C.; Sperling, L.S.; Toth, P.P.; Vinereanu, D.; Vrablík, M.; Wong, N.D.; Banach, M. Lipid-lowering nutraceuticals in clinical practice: position paper from an International Lipid Expert Panel. Nutr. Rev., 2017, 75(9), 731-767.
[http://dx.doi.org/10.1093/nutrit/nux047] [PMID: 28938795]
[14]
Harikumar, K.B.; Aggarwal, B.B. Resveratrol: a multitargeted agent for age-associated chronic diseases. Cell Cycle, 2008, 7(8), 1020-1035.
[http://dx.doi.org/10.4161/cc.7.8.5740] [PMID: 18414053]
[15]
Saiko, P.; Szakmary, A.; Jaeger, W.; Szekeres, T. Resveratrol and its analogs: defense against cancer, coronary disease and neurodegenerative maladies or just a fad? Mutat. Res., 2008, 658(1-2), 68-94.
[http://dx.doi.org/10.1016/j.mrrev.2007.08.004] [PMID: 17890139]
[16]
Baur, J.A.; Sinclair, D.A. Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug Discov., 2006, 5(6), 493-506.
[http://dx.doi.org/10.1038/nrd2060] [PMID: 16732220]
[17]
Hsieh, T.C.; Wu, J.M. Resveratrol: Biological and pharmaceutical properties as anticancer molecule. Biofactors, 2010, 36(5), 360-369.
[http://dx.doi.org/10.1002/biof.105] [PMID: 20623546]
[18]
Jannin, B.; Menzel, M.; Berlot, J-P.; Delmas, D.; Lançon, A.; Latruffe, N. Transport of resveratrol, a cancer chemopreventive agent, to cellular targets: plasmatic protein binding and cell uptake. Biochem. Pharmacol., 2004, 68(6), 1113-1118.
[http://dx.doi.org/10.1016/j.bcp.2004.04.028] [PMID: 15313407]
[19]
Casper, R.F.; Quesne, M.; Rogers, I.M.; Shirota, T.; Jolivet, A.; Milgrom, E.; Savouret, J.F. Resveratrol has antagonist activity on the aryl hydrocarbon receptor: implications for prevention of dioxin toxicity. Mol. Pharmacol., 1999, 56(4), 784-790.
[PMID: 10496962]
[20]
Lin, H-Y.; Lansing, L.; Merillon, J-M.; Davis, F.B.; Tang, H-Y.; Shih, A.; Vitrac, X.; Krisa, S.; Keating, T.; Cao, H.J.; Bergh, J.; Quackenbush, S.; Davis, P.J. Integrin alphaVbeta3 contains a receptor site for resveratrol. FASEB J., 2006, 20(10), 1742-1744.
[http://dx.doi.org/10.1096/fj.06-5743fje] [PMID: 16790523]
[21]
Caruso, F.; Tanski, J.; Villegas-Estrada, A.; Rossi, M. Structural basis for antioxidant activity of trans-resveratrol: ab initio calculations and crystal and molecular structure. J. Agric. Food Chem., 2004, 52(24), 7279-7285.
[http://dx.doi.org/10.1021/jf048794e] [PMID: 15563207]
[22]
Cao, Z.; Fang, J.; Xia, C.; Shi, X.; Jiang, B-H. trans--3,4,5′-Trihydroxystibene inhibits hypoxia-inducible factor 1α and vascular endothelial growth factor expression in human ovarian cancer cells. Clin. Cancer Res., 2004, 10(15), 5253-5263.
[http://dx.doi.org/10.1158/1078-0432.CCR-03-0588] [PMID: 15297429]
[23]
Renaud, S.; de Lorgeril, M. Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet, 1992, 339(8808), 1523-1526.
[http://dx.doi.org/10.1016/0140-6736(92)91277-F] [PMID: 1351198]
[24]
Hao, H.D.; He, L.R. Mechanisms of cardiovascular protection by resveratrol. J. Med. Food, 2004, 7(3), 290-298.
[http://dx.doi.org/10.1089/jmf.2004.7.290] [PMID: 15383221]
[25]
Asensi, M.; Medina, I.; Ortega, A.; Carretero, J.; Baño, M.C.; Obrador, E.; Estrela, J.M. Inhibition of cancer growth by resveratrol is related to its low bioavailability. Free Radic. Biol. Med., 2002, 33(3), 387-398.
[http://dx.doi.org/10.1016/S0891-5849(02)00911-5] [PMID: 12126761]
[26]
Marier, J-F.; Vachon, P.; Gritsas, A.; Zhang, J.; Moreau, J-P.; Ducharme, M.P. Metabolism and disposition of resveratrol in rats: extent of absorption, glucuronidation, and enterohepatic recirculation evidenced by a linked-rat model. J. Pharmacol. Exp. Ther., 2002, 302(1), 369-373.
[http://dx.doi.org/10.1124/jpet.102.033340] [PMID: 12065739]
[27]
Goldberg, D.M.; Yan, J.; Soleas, G.J. Absorption of three wine-related polyphenols in three different matrices by healthy subjects. Clin. Biochem., 2003, 36(1), 79-87.
[http://dx.doi.org/10.1016/S0009-9120(02)00397-1] [PMID: 12554065]
[28]
Das, D.K.; Mukherjee, S.; Ray, D. Erratum to: resveratrol and red wine, healthy heart and longevity. Heart Fail. Rev., 2011, 16(4), 425-435.
[http://dx.doi.org/10.1007/s10741-011-9234-6] [PMID: 21400036]
[29]
Pagliaro, BPagliaro, B. Santolamazza, C.; Simonelli, F.; Rubattu, S. Phytochemical Compounds and Protection from Cardiovascular Diseases: A State of the Art. BioMed Res. Int., 2015, 2015918069
[30]
Kanamori, H.; Takemura, G.; Goto, K.; Tsujimoto, A.; Ogino, A.; Takeyama, T.; Kawaguchi, T.; Watanabe, T.; Morishita, K.; Kawasaki, M.; Mikami, A.; Fujiwara, T.; Fujiwara, H.; Seishima, M.; Minatoguchi, S. Resveratrol reverses remodeling in hearts with large, old myocardial infarctions through enhanced autophagy-activating AMP kinase pathway. Am. J. Pathol., 2013, 182(3), 701-713.
[http://dx.doi.org/10.1016/j.ajpath.2012.11.009] [PMID: 23274061]
[31]
Kuwahara, F.; Kai, H.; Tokuda, K.; Kai, M.; Takeshita, A.; Egashira, K.; Imaizumi, T. Transforming growth factor-beta function blocking prevents myocardial fibrosis and diastolic dysfunction in pressure-overloaded rats. Circulation, 2002, 106(1), 130-135.
[http://dx.doi.org/10.1161/01.CIR.0000020689.12472.E0]
[32]
Villarreal, F.J. Cardiac hypertrophy-induced changes in mRNA levels for TGF-beta 1, fibronectin, and collagen. Dillmann WHJAJoP-H. Physiology C, 1992, 262(6), H1861-H6.
[33]
Koitabashi, N.; Arai, M.; Kogure, S.; Niwano, K.; Watanabe, A.; Aoki, Y.; Maeno, T.; Nishida, T.; Kubota, S.; Takigawa, M.; Kurabayashi, M. Increased connective tissue growth factor relative to brain natriuretic peptide as a determinant of myocardial fibrosis. Hypertension, 2007, 49(5), 1120-1127.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.106.077537]
[34]
Piacentini, L.; Gray, M.; Honbo, N.Y.; Chentoufi, J.; Bergman, M.; Karliner, J.S. Endothelin-1 stimulates cardiac fibroblast proliferation through activation of protein kinase C. J. Mol. Cell. Cardiol., 2000, 32(4), 565-576.
[35]
Shi-Wen, X.; Denton, C.P.; Dashwood, M.R.; Holmes, A.M.; Bou-Gharios, G.; Pearson, J.D.; Black, C.M.; Abraham, D.J. Fibroblast matrix gene expression and connective tissue remodeling: Role of endothelin-1. J. Invest. Dermatol., 2001, 116(3), 417-425.
[36]
Shibasaki, Y.; Nishiue, T.; Masaki, H.; Tamura, K.; Matsumoto, N.; Mori, Y.; Nishikawa, M.; Matsubara, H.; Iwasaka, T. Impact of the angiotensin ii receptor antagonist, losartan, on myocardial fibrosis in patients with end-stage renal disease: Assessment by ultrasonic integrated backscatter and biochemical markers. Hypertens. Res., 2005, 28(10), 787-795.
[37]
Shi, Y.; Massagué, J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell, 2003, 113(6), 685-700.
[38]
Heldin, C.H.; Miyazono, K.; ten Dijke, P. Tgf-beta signalling from cell membrane to nucleus through smad proteins. Nature, 1997, 390(6659), 465-471.
[http://dx.doi.org/10.1038/37284]
[39]
Lawson, J.S.; Syme, H.M.; Wheeler-Jones, C.P.D.; Elliott, J. Characterisation of feline renal cortical fibroblast cultures and their transcriptional response to transforming growth factor β1. BMC Vet. Res., 2018, 14
[http://dx.doi.org/10.1186/s12917-018-1387-2.]
[40]
Lam, S.; van der Geest, R.N.; Verhagen, N.A.M.; van Nieuwenhoven, F.A.; Blom, I.E.; Aten, J.; Goldschmeding, R.; Daha, M.R.; van Kooten, C. Connective tissue growth factor and igf-i are produced by human renal fibroblasts and cooperate in the induction of collagen production by high glucose. Diabetes, 2003, 52(12), 2975-2983.
[41]
Duncan, M.R.; Frazier, K.S.; Abramson, S.; Williams, S.; Klapper, H.; Huang, X.; Grotendorst, G.R. Connective tissue growth factor mediates transforming growth factor beta-induced collagen synthesis: down-regulation by camp. FASEB J., 1999, 13(13), 1774-1786.
[42]
Daniels, J.T.; Schultz, G.S.; Blalock, T.D.; Garrett, Q.; Grotendorst, G.R.; Dean, N.M.; Khaw, P.T. Mediation of transforming growth factor-β1-stimulated matrix contraction by fibroblasts. Am. J. Pathol., 2003, 163(5), 2043-2052.
[43]
Grotendorst, G.R.; Rahmanie, H.; Duncan, M.R. Combinatorial signaling pathways determine fibroblast proliferation and myofibroblast differentiation. FASEB J., 2004, 18(3), 469-479.
[44]
Sadoshima, J.; Xu, Y.; Slayter, H.S.; Izumo, S. Autocrine release of angiotensin ii mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell, 1993, 75(5), 977-984.
[45]
Kawano, H.; Do, Y.S.; Kawano, Y.; Starnes, V.; Barr, M.; Law, R.E.; Hsueh, W.A. Angiotensin II has multiple profibrotic effects in human cardiac fibroblasts. Circulation, 2000, 101(10), 1130-1137.
[46]
Kamo, T.; Akazawa, H.; Komuro, I. Cardiac nonmyocytes in the hub of cardiac hypertrophy. Circ. Res., 2015, 117(1), 89-98.
[47]
Mitchell, M.D.; Laird, R.E. Brown. Rd il-1β stimulates rat cardiac fibroblast migration via map kinase pathways. Long CSJAJoP-H. Physiol. C., 2007, 292(2), 1139-1147.
[48]
Honsho, S.; Nishikawa, S.; Amano, K.; Zen, K.; Adachi, Y.; Kishita, E.; Matsui, A.; Katsume, A.; Yamaguchi, S.; Nishikawa, K.; Isoda, K.; Riches, D.W.H.; Matoba, S.; Okigaki, M.; Matsubara, H. Pressure-mediated hypertrophy and mechanical stretch induces il-1 release and subsequent igf-1 generation to maintain compensative hypertrophy by affecting akt and jnk pathways. Circ. Res., 2009, 105(11), 1149-1158.
[49]
Testa, M.; Yeh, M.; Lee, P.; Fanelli, R.; Loperfido, F.; Berman, J.W.; LeJemtel, T.H. Circulating levels of cytokines and their endogenous modulators in patients with mild to severe congestive heart failure due to coronary artery disease or hypertension. J. Am. Coll. Cardiol., 1996, 28(4), 964-971.
[50]
Testa, M.; Yeh, M.; Lee, P.; Fanelli, R.; Loperfido, F.; Berman, J.W.; LeJemtel, T.H. Circulating levels of cytokines and their endogenous modulators in patients with mild to severe congestive heart failure due to coronary artery disease or hypertension. J. Am. Coll. Cardiol., 1996, 28(4), 964-971.
[51]
Kubota, T.; McTiernan, C.F.; Frye, C.S.; Slawson, S.E.; Lemster, B.H.; Koretsky, A.P.; Demetris, A.J.; Feldman, A.M. Dilated cardiomyopathy in transgenic mice with cardiac-specific overexpression of tumor necrosis factor-alpha. Circ. Res., 1997, 81(4), 627-635.
[52]
Meléndez, G.C.; McLarty, J.L.; Levick, S.P.; Du, Y.; Janicki, J.S.; Brower, G.L. Interleukin 6 mediates myocardial fibrosis, concentric hypertrophy, and diastolic dysfunction in rats. Hypertension, 2010, 56(2), 225-231.
[53]
Frieler, R.A.; Mortensen, R.M. Immune cell and other noncardiomyocyte regulation of cardiac hypertrophy and remodeling. Circulation, 2015, 131(11), 1019-1030.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.114.008788] [PMID: 25779542]
[54]
Li, L.; Zhao, Q.; Kong, W. Extracellular matrix remodeling and cardiac fibrosis. Matrix Biol., 2018, 68-69, 490-506.
[http://dx.doi.org/10.1016/j.matbio.2018.01.013] [PMID: 29371055]
[55]
Krejci, J; Mlejnek, D; Sochorova, D; Nemec, P. Inflammatory cardiomyopathy: a current view on the pathophysiology, diagnosis, and treatment., 2016.
[http://dx.doi.org/10.1155/2016/4087632]
[56]
Ho, C.Y.; López, B.; Coelho-Filho, O.R.; Lakdawala, N.K.; Cirino, A.L.; Jarolim, P.; Kwong, R.; González, A.; Colan, S.D.; Seidman, J.G.; Díez, J.; Seidman, C.E. Myocardial fibrosis as an early manifestation of hypertrophic cardiomyopathy. N. Engl. J. Med., 2010, 363(6), 552-563.
[http://dx.doi.org/10.1056/NEJMoa1002659] [PMID: 20818890]
[57]
Assomull, R.G.; Prasad, S.K.; Lyne, J.; Smith, G.; Burman, E.D.; Khan, M.; Sheppard, M.N.; Poole-Wilson, P.A.; Pennell, D.J. Cardiovascular magnetic resonance, fibrosis, and prognosis in dilated cardiomyopathy. J. Am. Coll. Cardiol., 2006, 48(10), 1977-1985.
[http://dx.doi.org/10.1016/j.jacc.2006.07.049] [PMID: 17112987]
[58]
Fox, P.R. Endomyocardial fibrosis and restrictive cardiomyopathy: pathologic and clinical features. J. Vet. Cardiol., 2004, 6(1), 25-31.
[http://dx.doi.org/10.1016/S1760-2734(06)70061-3] [PMID: 19083301]
[59]
Krenning, G.; Zeisberg, E.M.; Kalluri, R. The origin of fibroblasts and mechanism of cardiac fibrosis. J. Cell. Physiol., 2010, 225(3), 631-637.
[http://dx.doi.org/10.1002/jcp.22322] [PMID: 20635395]
[60]
Wang, J.; Chen, H.; Seth, A.; McCulloch, C.A. Mechanical force regulation of myofibroblast differentiation in cardiac fibroblasts. Am. J. Physiol. Heart Circ. Physiol., 2003, 285(5), H1871-H1881.
[http://dx.doi.org/10.1152/ajpheart.00387.2003] [PMID: 12842814]
[61]
Hinz, B. The myofibroblast: paradigm for a mechanically active cell. J. Biomech., 2010, 43(1), 146-155.
[http://dx.doi.org/10.1016/j.jbiomech.2009.09.020] [PMID: 19800625]
[62]
Stempien-Otero, A.; Kim, D-H.; Davis, J. Molecular networks underlying myofibroblast fate and fibrosis. J. Mol. Cell. Cardiol., 2016, 97, 153-161.
[http://dx.doi.org/10.1016/j.yjmcc.2016.05.002] [PMID: 27167848]
[63]
Lorenzo-Almorós, A.; Tuñón, J.; Orejas, M.; Cortés, M.; Egido, J.; Lorenzo, Ó. Diagnostic approaches for diabetic cardiomyopathy. Cardiovasc. Diabetol., 2017, 16(1), 28.
[http://dx.doi.org/10.1186/s12933-017-0506-x] [PMID: 28231848]
[64]
Wynn, TA Cellular and molecular mechanisms of fibrosis. The Journal of Pathology: A Journal of the Pathological Society of Great Britain and Ireland, 2008, 214(2), 199-210.,
[http://dx.doi.org/10.1002/path.2277]
[65]
Leask, A. Potential therapeutic targets for cardiac fibrosis: TGFbeta, angiotensin, endothelin, CCN2, and PDGF, partners in fibroblast activation. Circ. Res., 2010, 106(11), 1675-1680.
[http://dx.doi.org/10.1161/CIRCRESAHA.110.217737] [PMID: 20538689]
[66]
Frangogiannis, N.G. Chemokines in the ischemic myocardium: from inflammation to fibrosis. Inflamm. Res., 2004, 53(11), 585-595.
[http://dx.doi.org/10.1007/s00011-004-1298-5] [PMID: 15693606]
[67]
Subramanian, S.V.; Polikandriotis, J.A.; Kelm, R.J., Jr; David, J.J.; Orosz, C.G.; Strauch, A.R. Induction of vascular smooth muscle α-actin gene transcription in transforming growth factor β1-activated myofibroblasts mediated by dynamic interplay between the Pur repressor proteins and Sp1/Smad coactivators. Mol. Biol. Cell, 2004, 15(10), 4532-4543.
[http://dx.doi.org/10.1091/mbc.e04-04-0348] [PMID: 15282343]
[68]
Small, E.M.; Thatcher, J.E.; Sutherland, L.B.; Kinoshita, H.; Gerard, R.D.; Richardson, J.A. Novelty and significance. Circ. Res., 2010, 107(2), 294-304.
[http://dx.doi.org/10.1161/CIRCRESAHA.110.223172] [PMID: 20558820]
[69]
Khalil, H.; Kanisicak, O.; Prasad, V.; Correll, R.N.; Fu, X.; Schips, T.; Vagnozzi, R.J.; Liu, R.; Huynh, T.; Lee, S.J.; Karch, J.; Molkentin, J.D. Fibroblast-specific TGF-β-Smad2/3 signaling underlies cardiac fibrosis. J. Clin. Invest., 2017, 127(10), 3770-3783.
[http://dx.doi.org/10.1172/JCI94753] [PMID: 28891814]
[70]
Nahrendorf, M.; Swirski, F.K.; Aikawa, E.; Stangenberg, L.; Wurdinger, T.; Figueiredo, J-L.; Libby, P.; Weissleder, R.; Pittet, M.J. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med., 2007, 204(12), 3037-3047.
[71]
Kong, P; Christia, P; Frangogiannis, NGJC The pathogenesis of cardiac fibrosis. Sciences ml, 2014, 71(4), 549-74.,
[72]
Mantovani, A.; Sica, A.; Locati, M. Macrophage polarization comes of age. Immunity, 2005, 23(4), 344-346.
[73]
Yang, M.; Zheng, J.; Miao, Y.; Wang, Y.; Cui, W.; Guo, J.; Qiu, S.; Han, Y.; Jia, L.; Li, H.; Cheng, J.; Du, J. Serum-glucocorticoid regulated kinase 1 regulates alternatively activated macrophage polarization contributing to angiotensin ii-induced inflammation and cardiac fibrosis. Arterioscler. Thromb. Vasc. Biol., 2012, 32(7), 1675-1686.
[74]
Tokuda, K.; Kai, H.; Kuwahara, F.; Yasukawa, H.; Tahara, N.; Kudo, H.; Takemiya, K.; Koga, M.; Yamamoto, T.; Imaizumi, T. Pressure-independent effects of angiotensin ii on hypertensive myocardial fibrosis. Hypertension, 2004, 43(2), 499-503.
[75]
Sun, Y.; Zhang, J.; Lu, L.; Chen, S.S.; Quinn, M.T.; Weber, K.T. Aldosterone-induced inflammation in the rat heart : role of oxidative stress. Am. J. Pathol., 2002, 161(5), 1773-1781.
[76]
Fallowfield, J.A.; Mizuno, M.; Kendall, T.J.; Constandinou, C.M.; Benyon, R.C.; Duffield, J.S.; Iredale, J.P. Scar-associated macrophages are a major source of hepatic matrix metalloproteinase-13 and facilitate the resolution of murine hepatic fibrosis. J. Immunol., 2007, 178(8), 5288-5295.
[77]
Ramachandran, P; Pellicoro, A; Vernon, MA; Boulter, L; Aucott, RL ; Ali, A Differential Ly-6C expression identifies the recruited macrophage phenotype, which orchestrates the regression of murine liver fibrosis., 2012, 109(46), E3186-E95.,
[http://dx.doi.org/10.1073/pnas.1119964109]
[78]
Koitabashi, N.; Danner, T.; Zaiman, A.L.; Pinto, Y.M.; Rowell, J.; Mankowski, J.; Zhang, D.; Nakamura, T.; Takimoto, E.; Kass, D.A. Pivotal role of cardiomyocyte TGF-β signaling in the murine pathological response to sustained pressure overload. J. Clin. Invest., 2011, 121(6), 2301-2312.
[http://dx.doi.org/10.1172/JCI44824] [PMID: 21537080]
[79]
Barallobre-Barreiro, J.; Didangelos, A.; Yin, X.; Doménech, N.; Mayr, M. A sequential extraction methodology for cardiac extracellular matrix prior to proteomics analysis; Heart Proteomics, 2013, pp. 215-223.
[80]
Fang, M.; Xiang, F-L.; Braitsch, C.M.; Yutzey, K.E. Epicardium-derived fibroblasts in heart development and disease. J. Mol. Cell. Cardiol., 2016, 91, 23-27.
[http://dx.doi.org/10.1016/j.yjmcc.2015.12.019] [PMID: 26718723]
[81]
Fan, D.; Takawale, A.; Lee, J.; Kassiri, Z. Cardiac fibroblasts, fibrosis and extracellular matrix remodeling in heart disease. Fibrogenesis Tissue Repair, 2012, 5(1), 15.
[http://dx.doi.org/10.1186/1755-1536-5-15] [PMID: 22943504]
[82]
Nebigil, C.G.; Désaubry, L. The role of GPCR signaling in cardiac Epithelial to Mesenchymal Transformation (EMT). Trends Cardiovasc. Med., 2019, 29(4), 200-204.
[http://dx.doi.org/10.1016/j.tcm.2018.08.007] [PMID: 30172578]
[83]
Gurevich, V.V.; Gurevich, E.V. GPCRs and signal transducers: interaction stoichiometry. Trends Pharmacol. Sci., 2018, 39(7), 672-684.
[http://dx.doi.org/10.1016/j.tips.2018.04.002] [PMID: 29739625]
[84]
Chen, T.; Li, J.; Liu, J.; Li, N.; Wang, S.; Liu, H.; Zeng, M.; Zhang, Y.; Bu, P. Activation of SIRT3 by resveratrol ameliorates cardiac fibrosis and improves cardiac function via the TGF-β/Smad3 pathway. Am. J. Physiol. Heart Circ. Physiol., 2015, 308(5), H424-H434.
[http://dx.doi.org/10.1152/ajpheart.00454.2014] [PMID: 25527776]
[85]
Bellizzi, D.; Rose, G.; Cavalcante, P.; Covello, G.; Dato, S.; De Rango, F.; Greco, V.; Maggiolini, M.; Feraco, E.; Mari, V.; Franceschi, C.; Passarino, G.; De Benedictis, G. A novel VNTR enhancer within the SIRT3 gene, a human homologue of SIR2, is associated with survival at oldest ages. Genomics, 2005, 85(2), 258-263.
[http://dx.doi.org/10.1016/j.ygeno.2004.11.003] [PMID: 15676284]
[86]
Sundaresan, N.R.; Samant, S.A.; Pillai, V.B.; Rajamohan, S.B.; Gupta, M.P. SIRT3 is a stress-responsive deacetylase in cardiomyocytes that protects cells from stress-mediated cell death by deacetylation of Ku70. Mol. Cell. Biol., 2008, 28(20), 6384-6401.
[http://dx.doi.org/10.1128/MCB.00426-08] [PMID: 18710944]
[87]
Hoseini, A.; Namazi, G.; Farrokhian, A.; Reiner, Ž.; Aghadavod, E.; Bahmani, F.; Asemi, Z. The effects of resveratrol on metabolic status in patients with type 2 diabetes mellitus and coronary heart disease. Food Funct., 2019, 10(9), 6042-6051.
[http://dx.doi.org/10.1039/C9FO01075K] [PMID: 31486447]
[88]
Bujak, M.; Frangogiannis, N.G. The role of tgf-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc. Res., 2007, 74(2), 184-195.
[http://dx.doi.org/10.1016/j.cardiores.2006.10.002.]
[89]
Dobaczewski, M Chen, W Transforming growth factor (TGF)-β signaling in cardiac remodeling. cardiology c., 2011, 51(4), 600-6.,
[90]
Howitz, K.T.; Bitterman, K.J.; Cohen, H.Y.; Lamming, D.W.; Lavu, S.; Wood, J.G.; Zipkin, R.E.; Chung, P.; Kisielewski, A.; Zhang, L.L.; Scherer, B.; Sinclair, D.A. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature, 2003, 425(6954), 191-196.
[http://dx.doi.org/10.1038/nature01960] [PMID: 12939617]
[91]
Dolinsky, V.W.; Chakrabarti, S.; Pereira, T.J.; Oka, T.; Levasseur, J.; Beker, D.; Zordoky, B.N.; Morton, J.S.; Nagendran, J.; Lopaschuk, G.D.; Davidge, S.T.; Dyck, J.R. Resveratrol prevents hypertension and cardiac hypertrophy in hypertensive rats and mice. Biochim. Biophys. Acta, 2013, 1832(10), 1723-1733.
[http://dx.doi.org/10.1016/j.bbadis.2013.05.018] [PMID: 23707558]
[92]
Baur, J.A.; Pearson, K.J.; Price, N.L.; Jamieson, H.A.; Lerin, C.; Kalra, A.; Prabhu, V.V.; Allard, J.S.; Lopez-Lluch, G.; Lewis, K.; Pistell, P.J.; Poosala, S.; Becker, K.G.; Boss, O.; Gwinn, D.; Wang, M.; Ramaswamy, S.; Fishbein, K.W.; Spencer, R.G.; Lakatta, E.G.; Le Couteur, D.; Shaw, R.J.; Navas, P.; Puigserver, P.; Ingram, D.K.; de Cabo, R.; Sinclair, D.A. Resveratrol improves health and survival of mice on a high-calorie diet. Nature, 2006, 444(7117), 337-342.
[http://dx.doi.org/10.1038/nature05354] [PMID: 17086191]
[93]
Pearson, K.J.; Baur, J.A.; Lewis, K.N.; Peshkin, L.; Price, N.L.; Labinskyy, N.; Swindell, W.R.; Kamara, D.; Minor, R.K.; Perez, E.; Jamieson, H.A.; Zhang, Y.; Dunn, S.R.; Sharma, K.; Pleshko, N.; Woollett, L.A.; Csiszar, A.; Ikeno, Y.; Le Couteur, D.; Elliott, P.J.; Becker, K.G.; Navas, P.; Ingram, D.K.; Wolf, N.S.; Ungvari, Z.; Sinclair, D.A.; de Cabo, R. Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span. Cell Metab., 2008, 8(2), 157-168.
[http://dx.doi.org/10.1016/j.cmet.2008.06.011] [PMID: 18599363]
[94]
Sulaiman, M.; Matta, M.J.; Sunderesan, N.R.; Gupta, M.P.; Periasamy, M.; Gupta, M. Resveratrol, an activator of SIRT1, upregulates sarcoplasmic calcium ATPase and improves cardiac function in diabetic cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol., 2010, 298(3), H833-H843.
[http://dx.doi.org/10.1152/ajpheart.00418.2009] [PMID: 20008278]
[95]
Wood, J.G.; Rogina, B.; Lavu, S.; Howitz, K.; Helfand, S.L.; Tatar, M.; Sinclair, D. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature, 2004, 430(7000), 686-689.
[http://dx.doi.org/10.1038/nature02789] [PMID: 15254550]
[96]
Ma, S; Feng, J; Zhang, R; Chen, J; Han, D; Li, X SIRT1 activation by resveratrol alleviates cardiac dysfunction via mitochondrial regulation in diabetic cardiomyopathy mice.Oxidative medicine and cellular longevit, 2017.,
[http://dx.doi.org/10.1155/2017/4602715]
[97]
Bujak, M.; Ren, G.; Kweon, H.J.; Dobaczewski, M.; Reddy, A.; Taffet, G.; Wang, X-F.; Frangogiannis, N.G. Essential role of smad3 in infarct healing and in the pathogenesis of cardiac remodeling. Circulation, 2007, 116(19), 2127-2138.
[98]
Massagué, J. How cells read tgf-beta signals. Nat. Rev. Mol. Cell Biol., 2000, 1(3), 169-178.
[http://dx.doi.org/10.1038/35043051]
[99]
Funaba, M.; Zimmerman, C.M.; Mathews, L.S. Modulation of Smad2-mediated signaling by extracellular signal-regulated kinase. J. Biol. Chem., 2002, 277(44), 41361-41368.
[http://dx.doi.org/10.1074/jbc.M204597200.]
[100]
Engel, M.E.; McDonnell, M.A.; Law, B.K.; Moses, H.L. Interdependent smad and jnk signaling in transforming growth factor-β-mediated transcription. J. Biol. Chem., 1999, 274(52), 37413-37420.
[http://dx.doi.org/10.1074/jbc.274.52.37413.]
[101]
Venkatachalam, K.; Mummidi, S.; Cortez, D.M.; Prabhu, S.D.; Valente, A.J.; Chandrasekar, B. Resveratrol inhibits high glucose-induced PI3K/Akt/ERK-dependent interleukin-17 expression in primary mouse cardiac fibroblasts. Am. J. Physiol. Heart Circ. Physiol., 2008, 294(5), H2078-H2087.
[http://dx.doi.org/10.1152/ajpheart.01363.2007] [PMID: 18310510]
[102]
Brown, R.D.; Ambler, S.K.; Mitchell, M.D.; Long, C.S. The cardiac fibroblast: therapeutic target in myocardial remodeling and failure. Annu. Rev. Pharmacol. Toxicol., 2005, 45, 657-687.
[http://dx.doi.org/10.1146/annurev.pharmtox.45.120403.095802] [PMID: 15822192]
[103]
Eghbali, M. Cardiac fibroblasts: function, regulation of gene expression, and phenotypic modulation.Cardiac adaptation in heart failure., 1992, , 183-189.,
[104]
Frangogiannis, N.G.; Smith, C.W.; Entman, M.L. The inflammatory response in myocardial infarction. Cardiovasc. Res., 2002, 53(1), 31-47.
[http://dx.doi.org/10.1016/S0008-6363(01)00434-5] [PMID: 11744011]
[105]
Prabhu, S.D. Post-infarction ventricular remodeling: an array of molecular events. J. Mol. Cell. Cardiol., 2005, 38(4), 547-550.
[http://dx.doi.org/10.1016/j.yjmcc.2005.01.014] [PMID: 15808830]
[106]
Seta, Y.; Shan, K.; Bozkurt, B.; Oral, H.; Mann, D.L. Basic mechanisms in heart failure: the cytokine hypothesis. J. Card. Fail., 1996, 2(3), 243-249.
[http://dx.doi.org/10.1016/S1071-9164(96)80047-9] [PMID: 8891862]
[107]
Wilson, E.M.; Spinale, F.G. Myocardial remodelling and matrix metalloproteinases in heart failure: turmoil within the interstitium. Ann. Med., 2001, 33(9), 623-634.
[http://dx.doi.org/10.3109/07853890109002108] [PMID: 11817657]
[108]
Asbun, J.; Manso, A.M.; Villarreal, F.J. Profibrotic influence of high glucose concentration on cardiac fibroblast functions: effects of losartan and vitamin E. Am. J. Physiol. Heart Circ. Physiol., 2005, 288(1), H227-H234.
[http://dx.doi.org/10.1152/ajpheart.00340.2004] [PMID: 15345478]
[109]
Asbun, J.; Villarreal, F.J. The pathogenesis of myocardial fibrosis in the setting of diabetic cardiomyopathy. J. Am. Coll. Cardiol., 2006, 47(4), 693-700.
[http://dx.doi.org/10.1016/j.jacc.2005.09.050] [PMID: 16487830]
[110]
Ceriello, A. New insights on oxidative stress and diabetic complications may lead to a “causal” antioxidant therapy. Diabetes Care, 2003, 26(5), 1589-1596.
[http://dx.doi.org/10.2337/diacare.26.5.1589] [PMID: 12716823]
[111]
Green, K.; Brand, M.D.; Murphy, M.P. Prevention of mitochondrial oxidative damage as a therapeutic strategy in diabetes. Diabetes, 2004, 53(Suppl. 1), S110-S118.
[http://dx.doi.org/10.2337/diabetes.53.2007.S110] [PMID: 14749275]
[112]
Johansen, J.S.; Harris, A.K.; Rychly, D.J.; Ergul, A. Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice. Cardiovasc. Diabetol., 2005, 4(1), 5.
[http://dx.doi.org/10.1186/1475-2840-4-5] [PMID: 15862133]
[113]
Wang, G.; Song, X.; Zhao, L.; Li, Z.; Liu, B. Resveratrol prevents diabetic cardiomyopathy by increasing Nrf2 expression and transcriptional activity. BioMed Research international., 2018.
[http://dx.doi.org/10.1155/2018/2150218]
[114]
Harrington, L.E.; Hatton, R.D.; Mangan, P.R.; Turner, H.; Murphy, T.L.; Murphy, K.M.; Weaver, C.T. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol., 2005, 6(11), 1123-1132.
[http://dx.doi.org/10.1038/ni1254] [PMID: 16200070]
[115]
Huang, S-h.; Brett, E.; Frydas, S.; Kempuraj, D.; Barbacane, R.C.; Grilli, A., Eds.; Huang, S-h.; Brett, E.; Frydas, S.; Kempuraj, D.; Barbacane, R.C.; Grilli, A., Eds.; Interleukin-17 and the interleukin-17 family member network; , 2004.
[116]
Park, H.; Li, Z.; Yang, X.O.; Chang, S.H.; Nurieva, R.; Wang, Y-H.; Wang, Y.; Hood, L.; Zhu, Z.; Tian, Q.; Dong, C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol., 2005, 6(11), 1133-1141.
[http://dx.doi.org/10.1038/ni1261] [PMID: 16200068]
[117]
Kramer, J.M.; Gaffen, S.L. Interleukin-17: a new paradigm in inflammation, autoimmunity, and therapy. J. Periodontol., 2007, 78(6), 1083-1093.
[http://dx.doi.org/10.1902/jop.2007.060392] [PMID: 17539723]
[118]
Cortez, D.M.; Feldman, M.D.; Mummidi, S.; Valente, A.J.; Steffensen, B.; Vincenti, M.; Barnes, J.L.; Chandrasekar, B. IL-17 stimulates MMP-1 expression in primary human cardiac fibroblasts via p38 MAPK- and ERK1/2-dependent C/EBP-β, NF-kappaB, and AP-1 activation. Am. J. Physiol. Heart Circ. Physiol., 2007, 293(6), H3356-H3365.
[http://dx.doi.org/10.1152/ajpheart.00928.2007] [PMID: 17921324]
[119]
Wong, K-K.; Engelman, J.A.; Cantley, L.C. Targeting the PI3K signaling pathway in cancer. Curr. Opin. Genet. Dev., 2010, 20(1), 87-90.
[http://dx.doi.org/10.1016/j.gde.2009.11.002] [PMID: 20006486]
[120]
Cho, M-L.; Ju, J.H.; Kim, K-W.; Moon, Y-M.; Lee, S-Y.; Min, S-Y.; Cho, Y.G.; Kim, H.S.; Park, K.S.; Yoon, C.H.; Lee, S.H.; Park, S.H.; Kim, H.Y. Cyclosporine A inhibits IL-15-induced IL-17 production in CD4+ T cells via down-regulation of PI3K/Akt and NF-kappaB. Immunol. Lett., 2007, 108(1), 88-96.
[http://dx.doi.org/10.1016/j.imlet.2006.11.001] [PMID: 17161467]
[121]
Wu, H.; Li, G-N.; Xie, J.; Li, R.; Chen, Q-H.; Chen, J-Z.; Wei, Z.H.; Kang, L.N.; Xu, B. Resveratrol ameliorates myocardial fibrosis by inhibiting ROS/ERK/TGF-β/periostin pathway in STZ-induced diabetic mice. BMC Cardiovasc. Disord., 2016, 16(1), 5.
[http://dx.doi.org/10.1186/s12872-015-0169-z] [PMID: 26750922]
[122]
Zou, L.X.; Chen, C.; Yan, X.; Lin, Q.Y.; Fang, J.; Li, P.B.; Han, X.; Wang, Q.S.; Guo, S.B.; Li, H.H.; Zhang, Y.L. Resveratrol attenuates pressure overload-induced cardiac fibrosis and diastolic dysfunction via pten/akt/smad2/3 and nf-κb signaling pathways. Mol. Nutr. Food Res., 2019, 63(24)
[http://dx.doi.org/10.1002/mnfr.201900418] [PMID: 31655498]
[123]
Chen, C.; Zou, L-X.; Lin, Q-Y.; Yan, X.; Bi, H-L.; Xie, X.; Wang, S.; Wang, Q.S.; Zhang, Y.L.; Li, H.H. Resveratrol as a new inhibitor of immunoproteasome prevents PTEN degradation and attenuates cardiac hypertrophy after pressure overload. Redox Biol., 2019, 20, 390-401.
[http://dx.doi.org/10.1016/j.redox.2018.10.021] [PMID: 30412827]
[124]
Liu, F-C.; Tsai, H-I.; Yu, H-P. Organ-protective effects of red wine extract, resveratrol, in oxidative stress-mediated reperfusion injury. Oxidative medicine and cellular longev., 2015.
[http://dx.doi.org/10.1155/2015/568634]
[125]
Dolinsky, V.W.; Chan, A.Y.; Robillard Frayne, I.; Light, P.E.; Des Rosiers, C.; Dyck, J.R. Clinical perspective. Circulation, 2009, 119(12), 1643-1652.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.108.787440] [PMID: 19289642]
[126]
Guo, R.; Liu, B.; Wang, K.; Zhou, S.; Li, W.; Xu, Y. Resveratrol ameliorates diabetic vascular inflammation and macrophage infiltration in db/db mice by inhibiting the NF-κB pathway. Diab. Vasc. Dis. Res., 2014, 11(2), 92-102.
[http://dx.doi.org/10.1177/1479164113520332] [PMID: 24464099]
[127]
Diao, J.; Wei, J.; Yan, R.; Fan, G.; Lin, L.; Chen, M. Effects of resveratrol on regulation on UCP2 and cardiac function in diabetic rats. J. Physiol. Biochem., 2019, 75(1), 39-51.
[http://dx.doi.org/10.1007/s13105-018-0648-7] [PMID: 30225723]
[128]
Sung, M.M.; Das, S.K.; Levasseur, J.; Byrne, N.J.; Fung, D.; Kim, T.T.; Masson, G.; Boisvenue, J.; Soltys, C.L.; Oudit, G.Y.; Dyck, J.R. Resveratrol treatment of mice with pressure-overload-induced heart failure improves diastolic function and cardiac energy metabolism. Circ Heart Fail, 2015, 8(1), 128-137.
[http://dx.doi.org/10.1161/CIRCHEARTFAILURE.114.001677] [PMID: 25394648]
[129]
Li, J.; Wang, S.; Bai, J.; Yang, X-L.; Zhang, Y-L.; Che, Y-L.; Li, H.H.; Yang, Y.Z. Novel role for the Immunoproteasome subunit PSMB10 in angiotensin II–induced atrial fibrillation in mice. Hypertension, 2018, 71(5), 866-876.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.117.10390] [PMID: 29507100]
[130]
White, E.S.; Atrasz, R.G.; Hu, B.; Phan, S.H.; Stambolic, V.; Mak, T.W.; Hogaboam, C.M.; Flaherty, K.R.; Martinez, F.J.; Kontos, C.D.; Toews, G.B. Negative regulation of myofibroblast differentiation by PTEN (Phosphatase and Tensin Homolog Deleted on chromosome 10). Am. J. Respir. Crit. Care Med., 2006, 173(1), 112-121.
[http://dx.doi.org/10.1164/rccm.200507-1058OC] [PMID: 16179636]
[131]
Voloshenyuk, T.G.; Landesman, E.S.; Khoutorova, E.; Hart, A.D.; Gardner, J.D. .Induction of cardiac fibroblast lysyl oxidase by TGF- β1 requires PI3K/Akt, Smad3, and MAPK signaling. Cytokine, 2011, 55(1), 90-97.,
[http://dx.doi.org/10.1016/j.cyto.2011.03.024] [PMID: 21498085]

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