Login Register Cart 0
Generic placeholder image

Current Cardiology Reviews

Editor-in-Chief

ISSN (Print): 1573-403X
ISSN (Online): 1875-6557

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
General Review Article

Endothelial to Mesenchymal Transition in the Cardiogenesis and Cardiovascular Diseases

Author(s): Taha Anbara, Masuomeh Sharifi and Nahid Aboutaleb*

Volume 16, Issue 4, 2020

Page: [306 - 314] Pages: 9

DOI: 10.2174/1573403X15666190808100336

Price: $65

Abstract

Today, cardiovascular diseases remain a leading cause of morbidity and mortality worldwide. Endothelial to mesenchymal transition (EndMT) does not only play a major role in the course of development but also contributes to several cardiovascular diseases in adulthood. EndMT is characterized by down-regulation of the endothelial proteins and highly up-regulated fibrotic specific genes and extracellular matrix-forming proteins. EndMT is also a transforming growth factor- β-driven (TGF-β) process in which endothelial cells lose their endothelial characteristics and acquire a mesenchymal phenotype with expression of α-smooth muscle actin (α-SMA), fibroblastspecific protein 1, etc. EndMT is a vital process during cardiac development, thus disrupted EndMT gives rise to the congenital heart diseases, namely septal defects and valve abnormalities. In this review, we have discussed the main signaling pathways and mechanisms participating in the process of EndMT such as TGF-β and Bone morphogenetic protein (BMP), Wnt#, and Notch signaling pathway and also studied the role of EndMT in physiological cardiovascular development and pathological conditions including myocardial infarction, pulmonary arterial hypertension, congenital heart defects, cardiac fibrosis, and atherosclerosis. As a perspective view, having a clear understanding of involving cellular and molecular mechanisms in EndMT and conducting Randomized controlled trials (RCTs) with a large number of samples for involving pharmacological agents may guide us into novel therapeutic approaches of congenital disorders and heart diseases.

Keywords: Endothelial to mesenchymal transition, cardiovascular disease, congenital heart diseases, cardiogenesis, TGF-β.

Graphical Abstract

[1]
Huang X-P, Sun Z, Miyagi Y, et al. Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair. Circulation 2010; 122(23): 2419-29.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.110.955971] [PMID: 21098445]
[2]
Ghadrdoost B, Khoshravesh R, Aboutaleb N, Amirfarhangi A, Dashti S, Azizi Y. Heparin enhances the effects of mesenchymal stem cell transplantation in a rabbit model of acute myocardial infarction. Niger J Physiol Sci 2018; 33(1): 9-15.
[PMID: 30091727]
[3]
Evrard SM, Lecce L, Michelis KC, et al. Endothelial to mesenchymal transition is common in atherosclerotic lesions and is associated with plaque instability. Nat Commun 2016; 7: 11853.
[http://dx.doi.org/10.1038/ncomms11853] [PMID: 27340017]
[4]
Becerra A, Rojas M, Vallejos A, et al. Endothelial fibrosis induced by suppressed STAT3 expression mediated by signaling involving the TGF-β1/ALK5/Smad pathway. Lab Invest 2017; 97(9): 1033-46.
[http://dx.doi.org/10.1038/labinvest.2017.61] [PMID: 28737766]
[5]
Germani A, Foglio E, Capogrossi MC, Russo MA, Limana F. Generation of cardiac progenitor cells through epicardial to mesenchymal transition. J Mol Med (Berl) 2015; 93(7): 735-48.
[http://dx.doi.org/10.1007/s00109-015-1290-2] [PMID: 25943780]
[6]
Chen P-Y, Qin L, Tellides G, Simons M. Fibroblast growth factor receptor 1 is a key inhibitor of TGFβ signaling in the endothelium. Sci Signal 2014; 7(344): ra90-0.
[http://dx.doi.org/10.1126/scisignal.2005504] [PMID: 25249657]
[7]
Lagendijk AK, Szabó A, Merks RM, Bakkers J. Hyaluronan: a critical regulator of endothelial-to-mesenchymal transition during cardiac valve formation. Trends Cardiovasc Med 2013; 23(5): 135-42.
[http://dx.doi.org/10.1016/j.tcm.2012.10.002] [PMID: 23295082]
[8]
Hofmann JJ, et al. Endothelial deletion of murine Jag1 leads to valve calcification and congenital heart defects associated with Alagille syndrome.Development 2012; p. dev. 084871..
[http://dx.doi.org/10.1242/dev.084871]
[9]
Lin F-J, You LR, Yu CT, Hsu WH, Tsai MJ, Tsai SY. Endocardial cushion morphogenesis and coronary vessel development require chicken ovalbumin upstream promoter-transcription factor II. Arterioscler Thromb Vasc Biol 2012; 32(11): e135-46.
[http://dx.doi.org/10.1161/ATVBAHA.112.300255] [PMID: 22962329]
[10]
Yoshimatsu Y, Watabe T. Roles of TGF-β signals in endothelialmesenchymal transition during cardiac fibrosis. International journal of inflammation 2011; 2011.
[11]
Doerr M, Morrison J, Bergeron L, Coomber BL, Viloria-Petit A. Differential effect of hypoxia on early endothelial-mesenchymal transition response to transforming growth beta isoforms 1 and 2. Microvasc Res 2016; 108: 48-63.
[http://dx.doi.org/10.1016/j.mvr.2016.08.001] [PMID: 27503671]
[12]
Zeisberg EM, Tarnavski O, Zeisberg M, et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007; 13(8): 952-61.
[http://dx.doi.org/10.1038/nm1613] [PMID: 17660828]
[13]
Mercado-Pimentel ME, Runyan RB. Multiple transforming growth factor-β isoforms and receptors function during epithelial-mesenchymal cell transformation in the embryonic heart. Cells Tissues Organs (Print) 2007; 185(1-3): 146-56.
[http://dx.doi.org/10.1159/000101315] [PMID: 17587820]
[14]
Yang Y, Luo NS, Ying R, et al. Macrophage-derived foam cells impair endothelial barrier function by inducing endothelial-mesenchymal transition via CCL-4. Int J Mol Med 2017; 40(2): 558-68.
[http://dx.doi.org/10.3892/ijmm.2017.3034] [PMID: 28656247]
[15]
Xiao Y, Wu QQ, Jiang XH, Tang QZ. Cinnamaldehyde attenuates pressure overload-induced cardiac fibrosis via inhibition of endothelial mesenchymal transition. Zhonghua Yi Xue Za Zhi 2017; 97(11): 869-73.
[PMID: 28355745]
[16]
Zhang H, et al. Yap1 is required for endothelial to mesenchymal transition of the atrioventricular cushion. J Biol Chem 2014; 89(27): 18681-92.
[http://dx.doi.org/10.1074/jbc.M114.554584] [PMID: 24831012]
[17]
Wu M, Peng Z, Zu C, et al. Losartan attenuates myocardial endothelial-to-mesenchymal transition in spontaneous hypertensive rats via inhibiting TGF-β/Smad signaling. PLoS One 2016; 11(5)e0155730
[http://dx.doi.org/10.1371/journal.pone.0155730] [PMID: 27176484]
[18]
Wylie-Sears J, Levine RA, Bischoff J. Losartan inhibits endothelial-to-mesenchymal transformation in mitral valve endothelial cells by blocking transforming growth factor-β-induced phosphorylation of ERK. Biochem Biophys Res Commun 2014; 446(4): 870-5.
[http://dx.doi.org/10.1016/j.bbrc.2014.03.014] [PMID: 24632204]
[19]
Dufton NP, Peghaire CR, Osuna-Almagro L, et al. Dynamic regulation of canonical TGFβ signalling by endothelial transcription factor ERG protects from liver fibrogenesis. Nat Commun 2017; 8(1): 895.
[http://dx.doi.org/10.1038/s41467-017-01169-0] [PMID: 29026072]
[20]
Chen XY, Lv RJ, Zhang W, et al. Inhibition of myocyte-specific enhancer factor 2A improved diabetic cardiac fibrosis partially by regulating endothelial-to-mesenchymal transition. Oncotarget 2016; 7(21): 31053-66.
[http://dx.doi.org/10.18632/oncotarget.8842] [PMID: 27105518]
[21]
Medici D, Potenta S, Kalluri R. Transforming growth factor-β2 promotes Snail-mediated endothelial-mesenchymal transition through convergence of Smad-dependent and Smad-independent signalling. Biochem J 2011; 437(3): 515-20.
[http://dx.doi.org/10.1042/BJ20101500] [PMID: 21585337]
[22]
Xiao L, Kim DJ, Davis CL, et al. Tumor endothelial cells with distinct patterns of TGFβ-driven endothelial-to-mesenchymal transition. Cancer Res 2015; 75(7): 1244-54.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-1616] [PMID: 25634211]
[23]
Mahler GJ, Farrar EJ, Butcher JT. Inflammatory cytokines promote mesenchymal transformation in embryonic and adult valve endothelial cells. Arterioscler Thromb Vasc Biol 2013; 33(1): 121-30.
[http://dx.doi.org/10.1161/ATVBAHA.112.300504] [PMID: 23104848]
[24]
Crestani B, Marchand-Adam S, Quesnel C, et al. Hepatocyte growth factor and lung fibrosis. Proc Am Thorac Soc 2012; 9(3): 158-63.
[http://dx.doi.org/10.1513/pats.201202-018AW] [PMID: 22802291]
[25]
Shu Y, Liu Y, Li X, et al. Aspirin-triggered resolvin D1 inhibits TGF-β1-induced EndMT through increasing the expression of smad7 and is closely related to oxidative stress. Biomol Ther (Seoul) 2016; 24(2): 132-9.
[http://dx.doi.org/10.4062/biomolther.2015.088] [PMID: 26869523]
[26]
Combs MD, Yutzey KE. Heart valve development: Regulatory networks in development and disease. Circ Res 2009; 105(5): 408-21.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.201566] [PMID: 19713546]
[27]
Luna-Zurita L, Prados B, Grego-Bessa J, et al. Integration of a Notch-dependent mesenchymal gene program and Bmp2-driven cell invasiveness regulates murine cardiac valve formation. J Clin Invest 2010; 120(10): 3493-507.
[http://dx.doi.org/10.1172/JCI42666] [PMID: 20890042]
[28]
Kaneko K, Li X, Zhang X, Lamberti JJ, Jamieson SW, Thistlethwaite PA. Endothelial expression of bone morphogenetic protein receptor type 1a is required for atrioventricular valve formation. Ann Thorac Surg 2008; 85(6): 2090-8.
[http://dx.doi.org/10.1016/j.athoracsur.2008.02.027] [PMID: 18498827]
[29]
Townsend TA, Robinson JY, How T, DeLaughter DM, Blobe GC, Barnett JV. Endocardial cell epithelial-mesenchymal transformation requires Type III TGFβ receptor interaction with GIPC. Cell Signal 2012; 24(1): 247-56.
[http://dx.doi.org/10.1016/j.cellsig.2011.09.006] [PMID: 21945156]
[30]
Bai Y, Wang J, Morikawa Y, Bonilla-Claudio M, Klysik E, Martin JF. Bmp signaling represses Vegfa to promote outflow tract cushion development. Development 2013; 14: 3395-402.
[http://dx.doi.org/10.1242/dev.097360]
[31]
Hopper RK, Moonen J-RAR, Diebold I, et al. In pulmonary arterial hypertension, reduced BMPR2 promotes endothelial-to-mesenchymal transition via HMGA1 and its target slug. Circulation 2016; 133: 1783-94.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.115.020617]
[32]
Tian Y, Cohen ED, Morrisey EE. The importance of Wnt signaling in cardiovascular development. Pediatr Cardiol 2010; 31(3): 342-8.
[http://dx.doi.org/10.1007/s00246-009-9606-z] [PMID: 19967349]
[33]
Reis M, Liebner S. Wnt signaling in the vasculature. Exp Cell Res 2013; 319(9): 1317-23.
[http://dx.doi.org/10.1016/j.yexcr.2012.12.023] [PMID: 23291327]
[34]
Chen Z, Zhu JY, Fu Y, Richman A, Han Z. Wnt4 is required for ostia development in the Drosophila heart. Dev Biol 2016; 413(2): 188-98.
[http://dx.doi.org/10.1016/j.ydbio.2016.03.008] [PMID: 26994311]
[35]
Aisagbonhi O, Rai M, Ryzhov S, Atria N, Feoktistov I, Hatzopoulos AK. Experimental myocardial infarction triggers canonical Wnt signaling and endothelial-to-mesenchymal transition. Disease Models & Mechanisms 2011; 4: 469-83.
[http://dx.doi.org/10.1242/dmm.006510]
[36]
Hahn J-Y, Cho HJ, Bae JW, et al. β-catenin overexpression reduces myocardial infarct size through differential effects on cardiomyocytes and cardiac fibroblasts. J Biol Chem 2006; 281(41): 30979-89.
[http://dx.doi.org/10.1074/jbc.M603916200] [PMID: 16920707]
[37]
Stawski L, Han R, Bujor AM, Trojanowska M. Angiotensin II induces skin fibrosis: A novel mouse model of dermal fibrosis. Arthritis Res Ther 2012; 14(4): R194.
[http://dx.doi.org/10.1186/ar4028] [PMID: 22913887]
[38]
Cheng S-L, Shao JS, Behrmann A, Krchma K, Towler DA. Dkk1 and MSX2-Wnt7b signaling reciprocally regulate the endothelial-mesenchymal transition in aortic endothelial cells. Arterioscler Thromb Vasc Biol 2013; 33(7): 1679-89.
[http://dx.doi.org/10.1161/ATVBAHA.113.300647] [PMID: 23685555]
[39]
MacGrogan D, D’Amato G, Travisano S, et al. Sequential ligand-dependent Notch signaling activation regulates valve primordium formation and morphogenesis. Circ Res 2016; 118(10): 1480-97.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.308077] [PMID: 27056911]
[40]
Wiese C, Heisig J, Gessler M. Hey bHLH factors in cardiovascular development. Pediatr Cardiol 2010; 31(3): 363-70.
[http://dx.doi.org/10.1007/s00246-009-9609-9] [PMID: 20033145]
[41]
Niessen K, Karsan A. Notch signaling in cardiac development. Circ Res 2008; 102(10): 1169-81.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.174318] [PMID: 18497317]
[42]
de la Pompa JL. Notch signaling in cardiac development and disease. Pediatr Cardiol 2009; 30(5): 643-50.
[http://dx.doi.org/10.1007/s00246-008-9368-z] [PMID: 19184573]
[43]
Kostina AS, Uspensky VE, Irtyuga OB, et al. Notch-dependent EMT is attenuated in patients with aortic aneurysm and bicuspid aortic valve. Biochim Biophys Acta 2016; 1862(4): 733-40.
[http://dx.doi.org/10.1016/j.bbadis.2016.02.006] [PMID: 26876948]
[44]
Fu Y, et al. RUNX3 maintains the mesenchymal phenotype after termination of the Notch signal. J Biol Chem 2011; 286: 11803-13.
[http://dx.doi.org/10.1074/jbc.M111.222331]
[45]
High FA, Jain R, Stoller JZ, et al. Murine Jagged1/Notch signaling in the second heart field orchestrates Fgf8 expression and tissue-tissue interactions during outflow tract development. J Clin Invest 2009; 119(7): 1986-96.
[http://dx.doi.org/10.1172/JCI38922] [PMID: 19509466]
[46]
Elliott GC, Gurtu R, McCollum C, Newman WG, Wang T. Foramen ovale closure is a process of endothelial-to-mesenchymal transition leading to fibrosis. PLoS One 2014; 9(9)e107175
[http://dx.doi.org/10.1371/journal.pone.0107175] [PMID: 25215881]
[47]
Zhou X, Chen X, Cai JJ, et al. Relaxin inhibits cardiac fibrosis and endothelial-mesenchymal transition via the Notch pathway. Drug Des Devel Ther 2015; 9: 4599-611.
[http://dx.doi.org/10.2147/DDDT.S85399] [PMID: 26316699]
[48]
Welch-Reardon KM, Wu N, Hughes CC. A role for partial endothelial-mesenchymal transitions in angiogenesis? Arterioscler Thromb Vasc Biol 2015; 35(2): 303-8.
[http://dx.doi.org/10.1161/ATVBAHA.114.303220] [PMID: 25425619]
[49]
Pucéat M. Embryological origin of the endocardium and derived valve progenitor cells: From developmental biology to stem cell-based valve repair. Biochim Biophys Acta 2013; 1833(4): 917-22.
[http://dx.doi.org/10.1016/j.bbamcr.2012.09.013] [PMID: 23078978]
[50]
Xu X, Tan X, Tampe B, Sanchez E, Zeisberg M, Zeisberg EM. Snail is a direct target of hypoxia-inducible factor 1α (HIF1α) in hypoxia-induced endothelial to mesenchymal transition of human coronary endothelial cells. J Biol Chem 2015; 290(27): 16653-64.
[http://dx.doi.org/10.1074/jbc.M115.636944] [PMID: 25971970]
[51]
Sucov HM, Gu Y, Thomas S, Li P, Pashmforoush M. Epicardial control of myocardial proliferation and morphogenesis. Pediatr Cardiol 2009; 30(5): 617-25.
[http://dx.doi.org/10.1007/s00246-009-9391-8] [PMID: 19277768]
[52]
Saito A. EMT and EndMT: Regulated in similar ways? J Biochem 2013; 153(6): 493-5.
[http://dx.doi.org/10.1093/jb/mvt032] [PMID: 23613024]
[53]
Garside VC, Chang AC, Karsan A, Hoodless PA. Co-ordinating Notch, BMP, and TGF-β signaling during heart valve development. Cell Mol Life Sci 2013; 70(16): 2899-917.
[http://dx.doi.org/10.1007/s00018-012-1197-9] [PMID: 23161060]
[54]
Chen Q, Zhang H, Liu Y, et al. Endothelial cells are progenitors of cardiac pericytes and vascular smooth muscle cells. Nat Commun 2016; 7: 12422.
[http://dx.doi.org/10.1038/ncomms12422] [PMID: 27516371]
[55]
Li L, Wei C, Kim IK, Janssen-Heininger Y, Gupta S. Inhibition of nuclear factor-κB in the lungs prevents monocrotaline-induced pulmonary hypertension in mice. Hypertension 2014; 63(6): 1260-9.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.114.03220] [PMID: 24614212]
[56]
Cuttano R, Rudini N, Bravi L, et al. KLF4 is a key determinant in the development and progression of cerebral cavernous malformations. EMBO Mol Med 2016; 8(1): 6-24.
[http://dx.doi.org/10.15252/emmm.201505433] [PMID: 26612856]
[57]
Renz M, Otten C, Faurobert E, et al. Regulation of β1 integrin-Klf2-mediated angiogenesis by CCM proteins. Dev Cell 2015; 32(2): 181-90.
[http://dx.doi.org/10.1016/j.devcel.2014.12.016] [PMID: 25625207]
[58]
Zhou Z, Tang AT, Wong WY, et al. Cerebral cavernous malformations arise from endothelial gain of MEKK3-KLF2/4 signalling. Nature 2016; 532(7597): 122-6.
[http://dx.doi.org/10.1038/nature17178] [PMID: 27027284]
[59]
Hautefort A, Chesné J, Preussner J, et al. Pulmonary endothelial cell DNA methylation signature in pulmonary arterial hypertension. Oncotarget 2017; 8(32): 52995-3016.
[http://dx.doi.org/10.18632/oncotarget.18031] [PMID: 28881789]
[60]
Leopold JA, Maron BA. Molecular mechanisms of pulmonary vascular remodeling in pulmonary arterial hypertension. Int J Mol Sci 2016; 17(5): 761.
[http://dx.doi.org/10.3390/ijms17050761] [PMID: 27213345]
[61]
Morrell NW, Adnot S, Archer SL, et al. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol 2009; 54(1)(Suppl.): S20-31.
[http://dx.doi.org/10.1016/j.jacc.2009.04.018] [PMID: 19555855]
[62]
Kato H, Fu YY, Zhu J, et al. Pulmonary vein stenosis and the pathophysiology of “upstream” pulmonary veins. J Thorac Cardiovasc Surg 2014; 148(1): 245-53.
[http://dx.doi.org/10.1016/j.jtcvs.2013.08.046] [PMID: 24084286]
[63]
Atkinson C, Stewart S, Upton PD, et al. Primary pulmonary hypertension is associated with reduced pulmonary vascular expression of type II bone morphogenetic protein receptor. Circulation 2002; 105(14): 1672-8.
[http://dx.doi.org/10.1161/01.CIR.0000012754.72951.3D] [PMID: 11940546]
[64]
Reynolds AM, et al. Targeted gene delivery of BMPR-2 attenuates pulmonary hypertension. Eur Respir J 2012; 39(2): 329-43.
[PMID: 21737550]
[65]
Kang Z, Ji Y, Zhang G, Qu Y, Zhang L, Jiang W. Ponatinib attenuates experimental pulmonary arterial hypertension by modulating Wnt signaling and vasohibin-2/vasohibin-1. Life Sci 2016; 148: 1-8.
[http://dx.doi.org/10.1016/j.lfs.2016.02.017] [PMID: 26860892]
[66]
Moonen J-RA, Lee ES, Schmidt M, et al. Endothelial-to-mesenchymal transition contributes to fibro-proliferative vascular disease and is modulated by fluid shear stress. Cardiovasc Res 2015; 108(3): 377-86.
[http://dx.doi.org/10.1093/cvr/cvv175] [PMID: 26084310]
[67]
Mahmoud MM, Serbanovic-Canic J, Feng S, et al. Shear stress induces endothelial-to-mesenchymal transition via the transcription factor Snail. Sci Rep 2017; 7(1): 3375.
[http://dx.doi.org/10.1038/s41598-017-03532-z] [PMID: 28611395]
[68]
Tomanek RJ, Christensen LP, Simons M, Murakami M, Zheng W, Schatteman GC. Embryonic coronary vasculogenesis and angiogenesis are regulated by interactions between multiple FGFs and VEGF and are influenced by mesenchymal stem cells. Dev Dyn 2010; 239(12): 3182-91.
[http://dx.doi.org/10.1002/dvdy.22460] [PMID: 20981833]
[69]
Stabley JN, Towler DA. Arterial calcification in diabetes mellitus: Preclinical models and translational implications. Arterioscler Thromb Vasc Biol 2017; 37(2): 205-17.
[http://dx.doi.org/10.1161/ATVBAHA.116.306258] [PMID: 28062508]
[70]
Samandari-Rad S, et al. A Comparison of the transplantation effects of mesenchymal stem cells isolated from human Wharton’s Jelly and human bone marrow in rabbit myocardial infarction. Can J Comput Imath Nat Sci Eng Med 2012; 3: 270-6.
[71]
Afousi AG, et al. Targeting necroptotic cell death pathway by high-intensity interval training (HIIT) decreases development of post-ischemic adverse remodelling after myocardial ischemia/reperfusion injury. J Cell Commun Signal 2019; 13(2): 255-67.
[PMID: 30073629]
[72]
Nakaya M, Watari K, Tajima M, et al. Cardiac myofibroblast engulfment of dead cells facilitates recovery after myocardial infarction. J Clin Invest 2017; 127(1): 383-401.
[http://dx.doi.org/10.1172/JCI83822] [PMID: 27918308]
[73]
Bischoff J, Casanovas G, Wylie-Sears J, et al. CD45 expression in mitral valve endothelial cells after myocardial infarction. Circ Res 2016; 119(11): 1215-25.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.309598] [PMID: 27750208]
[74]
Bonet F, Dueñas Á, López-Sánchez C, García-Martínez V, Aránega AE, Franco D. MiR-23b and miR-199a impair epithelial-to-mesenchymal transition during atrioventricular endocardial cushion formation. Dev Dyn 2015; 244(10): 1259-75.
[http://dx.doi.org/10.1002/dvdy.24309] [PMID: 26198058]
[75]
Gong H, Lyu X, Wang Q, Hu M, Zhang X. Endothelial to mesenchymal transition in the cardiovascular system. Life Sci 2017; 184: 95-102.
[http://dx.doi.org/10.1016/j.lfs.2017.07.014] [PMID: 28716564]
[76]
Jeong D, Lee MA, Li Y, et al. Matricellular protein CCN5 reverses established cardiac fibrosis. J Am Coll Cardiol 2016; 67(13): 1556-68.
[http://dx.doi.org/10.1016/j.jacc.2016.01.030] [PMID: 27150688]
[77]
Rakhshan K, Azizi Y, Naderi N, Afousi AG, Aboutaleb N. ELABELA (ELA) peptide exerts cardioprotection against myocardial infarction by targeting oxidative stress and the improvement of heart function. Int J Pept Res Ther 2019; 25: 613-21.
[78]
Fan Z, Guan J. Antifibrotic therapies to control cardiac fibrosis. Biomater Res 2016; 20(1): 13.
[http://dx.doi.org/10.1186/s40824-016-0060-8] [PMID: 27226899]
[79]
Moore-Morris T, Guimarães-Camboa N, Banerjee I, et al. Resident fibroblast lineages mediate pressure overload-induced cardiac fibrosis. J Clin Invest 2014; 124(7): 2921-34.
[http://dx.doi.org/10.1172/JCI74783] [PMID: 24937432]
[80]
Widyantoro B, Emoto N, Nakayama K, et al. Endothelial cell-derived endothelin-1 promotes cardiac fibrosis in diabetic hearts through stimulation of endothelial-to-mesenchymal transition. Circulation 2010; 121(22): 2407-18.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.110.938217] [PMID: 20497976]
[81]
Kim J, Kim J, Lee SH, et al. Cytokine-like 1 regulates cardiac fibrosis via modulation of TGF-β signaling. PLoS One 2016; 11(11)e0166480
[http://dx.doi.org/10.1371/journal.pone.0166480] [PMID: 27835665]
[82]
Murdoch CE, Chaubey S, Zeng L, et al. Endothelial NADPH oxidase-2 promotes interstitial cardiac fibrosis and diastolic dysfunction through proinflammatory effects and endothelial-mesenchymal transition. J Am Coll Cardiol 2014; 63(24): 2734-41.
[http://dx.doi.org/10.1016/j.jacc.2014.02.572] [PMID: 24681145]
[83]
Bartko PE, Dal-Bianco JP, Guerrero JL, et al. Effect of losartan on mitral valve changes after myocardial infarction. J Am Coll Cardiol 2017; 70(10): 1232-44.
[http://dx.doi.org/10.1016/j.jacc.2017.07.734] [PMID: 28859786]
[84]
Tang R-N, Lv LL, Zhang JD, et al. Effects of angiotensin II receptor blocker on myocardial endothelial-to-mesenchymal transition in diabetic rats. Int J Cardiol 2013; 162(2): 92-9.
[http://dx.doi.org/10.1016/j.ijcard.2011.06.052] [PMID: 21704391]
[85]
Charytan DM, Padera R, Helfand AM, et al. Increased concentration of circulating angiogenesis and nitric oxide inhibitors induces endothelial to mesenchymal transition and myocardial fibrosis in patients with chronic kidney disease. Int J Cardiol 2014; 176(1): 99-109.
[http://dx.doi.org/10.1016/j.ijcard.2014.06.062] [PMID: 25049013]
[86]
Hua J, et al. Relationship between endothelial-to-mesenchymal transition and cardiac fibrosis in acute viral myocarditis. Zhejiang da xue xue bao. Yi xue ban= Journal of Zhejiang University. Med Sci 2012; 41(3): 298-304.
[87]
Wawro ME, Sobierajska K, Ciszewski WM, et al. Tubulin beta 3 and 4 are involved in the generation of early fibrotic stages. Cell Signal 2017; 38: 26-38.
[http://dx.doi.org/10.1016/j.cellsig.2017.06.014] [PMID: 28648944]
[88]
Pletinck A, Consoli C, Van Landschoot M, et al. Salt intake induces epithelial-to-mesenchymal transition of the peritoneal membrane in rats. Nephrol Dial Transplant 2010; 25(5): 1688-96.
[http://dx.doi.org/10.1093/ndt/gfq036] [PMID: 20150166]
[89]
Gasparics Á, Rosivall L, Krizbai IA, Sebe A. When the endothelium scores an own goal: Endothelial cells actively augment metastatic extravasation through endothelial-mesenchymal transition. Am J Physiol Heart Circ Physiol 2016; 310(9): H1055-63.
[http://dx.doi.org/10.1152/ajpheart.00042.2016] [PMID: 26993222]
[90]
Lin F, Wang N, Zhang TC. The role of endothelial-mesenchymal transition in development and pathological process. IUBMB Life 2012; 64(9): 717-23.
[http://dx.doi.org/10.1002/iub.1059] [PMID: 22730243]

Rights & Permissions Print Cite
Article Metrics
86
© 2024 Bentham Science Publishers | Privacy Policy