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Current Medicinal Chemistry

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ISSN (Online): 1875-533X

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Review Article

The Roles of Signaling Pathways in Cardiac Regeneration

Author(s): Amir Valizadeh, Samira Asghari, Parinaz Mansouri, Forough Alemi, Maryam Majidinia, Ata Mahmoodpoor and Bahman Yousefi*

Volume 29, Issue 12, 2022

Published on: 11 January, 2022

Page: [2142 - 2166] Pages: 25

DOI: 10.2174/0929867328666210914115411

Price: $65

Abstract

In recent years, knowledge of cardiac regeneration mechanisms has dramatically expanded. Regeneration can replace lost parts of organs, common among animal species. The heart is commonly considered an organ with terminal development, which has no reparability potential during post-natal life. However, some intrinsic regeneration capacity has been reported for cardiac muscle, which opens novel avenues in cardiovascular disease treatment. Different endogenous mechanisms have been studied for cardiac repairing and regeneration in recent decades. Survival, proliferation, inflammation, angiogenesis, cell-cell communication, cardiomyogenesis, and anti-aging pathways are the most important mechanisms that have been studied in this regard. Several in vitro and animal model studies focused on proliferation induction for cardiac regeneration reported promising results. These studies have mainly focused on promoting proliferation signaling pathways and demonstrated various signaling pathways such as Wnt, PI3K/Akt, IGF- 1, TGF-β, Hippo, and VEGF signaling cardiac regeneration. Therefore, in this review, we intend to discuss the connection between different critical signaling pathways in cardiac repair and regeneration.

Keywords: Signaling pathways, heart, regeneration, Wnt signaling, notch signaling, VEGF signaling, IGF-1 signaling.

« Previous Next »
[1]
Kawakami, Y.; Rodriguez Esteban, C.; Raya, M.; Kawakami, H.; Martí, M.; Dubova, I.; Izpisúa Belmonte, J.C. Wnt/beta-catenin signaling regulates vertebrate limb regeneration. Genes Dev., 2006, 20(23), 3232-3237.
[http://dx.doi.org/10.1101/gad.1475106] [PMID: 17114576]
[2]
Polezhaev, L.V.; Kolchin, S.P.; Solntseva, G.N. Stimulation of regeneration of the heart muscle in the course of diphtherial myocarditis. Dokl. Akad. Nauk SSSR, 1965, 164(4), 949-952.
[PMID: 5877446]
[3]
He, L.; Nguyen, N.B.; Ardehali, R.; Zhou, B. Heart Regeneration by Endogenous Stem Cells and Cardiomyocyte Proliferation: Controversy, Fallacy, and Progress. Circulation, 2020, 142(3), 275-291.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.119.045566] [PMID: 32687441]
[4]
Voges, H.K.; Mills, R.J.; Elliott, D.A.; Parton, R.G.; Porrello, E.R.; Hudson, J.E.J.D. Development of a human cardiac organoid injury model reveals innate regenerative potential. Development, 2017, 144(6), 1118-1127.
[http://dx.doi.org/10.1242/dev.143966] [PMID: 28174241]
[5]
Torrini, C.; Cubero, R.J.; Dirkx, E.; Braga, L.; Ali, H.; Prosdocimo, G.; Gutierrez, M.I.; Collesi, C.; Licastro, D.; Zentilin, L.; Mano, M.; Zacchigna, S.; Vendruscolo, M.; Marsili, M.; Samal, A.; Giacca, M. Common Regulatory Pathways Mediate Activity of MicroRNAs Inducing Cardiomyocyte Proliferation. Cell Rep., 2019, 27(9), 2759-2771.
[http://dx.doi.org/10.1016/j.celrep.2019.05.005] [PMID: 31141697]
[6]
Porrello, E.R.; Mahmoud, A.I.; Simpson, E.; Hill, J.A.; Richardson, J.A.; Olson, E.N.; Sadek, H.A. Transient regenerative potential of the neonatal mouse heart. Science, 2011, 331(6020), 1078-1080.
[http://dx.doi.org/10.1126/science.1200708] [PMID: 21350179]
[7]
Lenneman, A.J.; Birks, E.J. Treatment strategies for myocardial recovery in heart failure. Curr. Treat. Options Cardiovasc. Med., 2014, 16(3), 287.
[http://dx.doi.org/10.1007/s11936-013-0287-9] [PMID: 24492922]
[8]
Xin, M.; Kim, Y.; Sutherland, L.B.; Murakami, M.; Qi, X.; McAnally, J.; Porrello, E.R.; Mahmoud, A.I.; Tan, W.; Shelton, J.M.; Richardson, J.A.; Sadek, H.A.; Bassel-Duby, R.; Olson, E.N. Hippo pathway effector Yap promotes cardiac regeneration. Proc. Natl. Acad. Sci. USA, 2013, 110(34), 13839-13844.
[http://dx.doi.org/10.1073/pnas.1313192110] [PMID: 23918388]
[9]
Flinn, M.A.; Link, B.A.; O’Meara, C.C. Upstream regulation of the Hippo-Yap pathway in cardiomyocyte regeneration. Semin. Cell Dev. Biol., 2020, 100, 11-19.
[http://dx.doi.org/10.1016/j.semcdb.2019.09.004] [PMID: 31606277]
[10]
Dogra, D.; Ahuja, S.; Kim, H-T.; Rasouli, S.J.; Stainier, D.Y.R.; Reischauer, S. Opposite effects of Activin type 2 receptor ligands on cardiomyocyte proliferation during development and repair. Nat. Commun., 2017, 8(1), 1902.
[http://dx.doi.org/10.1038/s41467-017-01950-1] [PMID: 29196619]
[11]
Beffagna, G. Zebrafish as a Smart Model to Understand Regeneration After Heart Injury: How Fish Could Help Humans. Front. Cardiovasc. Med., 2019, 6(107), 107.
[http://dx.doi.org/10.3389/fcvm.2019.00107] [PMID: 31448289]
[12]
Gomes, R.S.; Skroblin, P.; Munster, A.B.; Tomlins, H.; Langley, S.R.; Zampetaki, A.; Yin, X.; Wardle, F.C.; Mayr, M. “Young at heart”: Regenerative potential linked to immature cardiac phenotypes. J. Mol. Cell. Cardiol., 2016, 92, 105-108.
[http://dx.doi.org/10.1016/j.yjmcc.2016.01.026] [PMID: 26827899]
[13]
Poss, K.D.; Wilson, L.G.; Keating, M.T. Heart regeneration in zebrafish. Science, 2002, 298(5601), 2188-2190.
[http://dx.doi.org/10.1126/science.1077857] [PMID: 12481136]
[14]
Chablais, F.; Veit, J.; Rainer, G.; Jaźwińska, A. The zebrafish heart regenerates after cryoinjury-induced myocardial infarction. BMC Dev. Biol., 2011, 11(1), 21.
[http://dx.doi.org/10.1186/1471-213X-11-21] [PMID: 21473762]
[15]
Leung, C.S.; Yang, K.Y.; Li, X.; Chan, V.W.; Ku, M.; Waldmann, H.; Hori, S.; Tsang, J.C.H.; Lo, Y.M.D.; Lui, K.O. Single-cell transcriptomics reveal that PD-1 mediates immune tolerance by regulating proliferation of regulatory T cells. Genome Med., 2018, 10(1), 71.
[http://dx.doi.org/10.1186/s13073-018-0581-y] [PMID: 30236153]
[16]
Günthel, M.; Barnett, P.; Christoffels, V.M. Development, proliferation, and growth of the mammalian heart. Mol. Ther., 2018, 26(7), 1599-1609.
[http://dx.doi.org/10.1016/j.ymthe.2018.05.022] [PMID: 29929790]
[17]
Uygur, A.; Lee, R.T. Mechanisms of Cardiac Regeneration. Dev. Cell, 2016, 36(4), 362-374.
[http://dx.doi.org/10.1016/j.devcel.2016.01.018] [PMID: 26906733]
[18]
Cao, J.; Poss, K.D.J.N.R.C. The epicardium as a hub for heart regeneration. Nat. Rev. Cardiol., 2018, 15(10), 631-647.
[http://dx.doi.org/10.1038/s41569-018-0046-4] [PMID: 29950578]
[19]
Cahill, T.J.; Choudhury, R.P.; Riley, P.R. Heart regeneration and repair after myocardial infarction: translational opportunities for novel therapeutics. Nat. Rev. Drug Discov., 2017, 16(10), 699-717.
[http://dx.doi.org/10.1038/nrd.2017.106] [PMID: 28729726]
[20]
Vilahur, G.; Juan-Babot, O.; Peña, E.; Oñate, B.; Casaní, L.; Badimon, L. Molecular and cellular mechanisms involved in cardiac remodeling after acute myocardial infarction. J. Mol. Cell. Cardiol., 2011, 50(3), 522-533.
[http://dx.doi.org/10.1016/j.yjmcc.2010.12.021] [PMID: 21219908]
[21]
Karra, R.; Knecht, A.K.; Kikuchi, K.; Poss, K.D. Myocardial NF-κB activation is essential for zebrafish heart regeneration. Proc. Natl. Acad. Sci. USA, 2015, 112(43), 13255-13260.
[http://dx.doi.org/10.1073/pnas.1511209112] [PMID: 26472034]
[22]
Lin, Z.; Pu, W.T. Harnessing Hippo in the heart: Hippo/Yap signaling and applications to heart regeneration and rejuvenation. Stem Cell Res. (Amst.), 2014, 13(3 Pt B), 571-581.
[http://dx.doi.org/10.1016/j.scr.2014.04.010] [PMID: 24881775]
[23]
Bersell, K.; Arab, S.; Haring, B.; Kühn, B. Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell, 2009, 138(2), 257-270.
[http://dx.doi.org/10.1016/j.cell.2009.04.060] [PMID: 19632177]
[24]
Hashimoto, H.; Olson, E.N.; Bassel-Duby, R. Therapeutic approaches for cardiac regeneration and repair. Nat. Rev. Cardiol., 2018, 15(10), 585-600.
[http://dx.doi.org/10.1038/s41569-018-0036-6] [PMID: 29872165]
[25]
Artap, S.; Manderfield, L.J.; Smith, C.L.; Poleshko, A.; Aghajanian, H.; See, K.; Li, L.; Jain, R.; Epstein, J.A. Endocardial Hippo signaling regulates myocardial growth and cardiogenesis. Dev. Biol., 2018, 440(1), 22-30.
[http://dx.doi.org/10.1016/j.ydbio.2018.04.026] [PMID: 29727635]
[26]
Gemberling, M.; Karra, R.; Dickson, A.L.; Poss, K.D. Nrg1 is an injury-induced cardiomyocyte mitogen for the endogenous heart regeneration program in zebrafish. eLife, 2015, 4 ,e05871.
[http://dx.doi.org/10.7554/eLife.05871] [PMID: 25830562]
[27]
Maier, H.J.; Schips, T.G.; Wietelmann, A.; Krüger, M.; Brunner, C.; Sauter, M.; Klingel, K.; Böttger, T.; Braun, T.; Wirth, T. Cardiomyocyte-specific IκB kinase (IKK)/NF-κB activation induces reversible inflammatory cardiomyopathy and heart failure. Proc. Natl. Acad. Sci. USA, 2012, 109(29), 11794-11799.
[http://dx.doi.org/10.1073/pnas.1116584109] [PMID: 22753500]
[28]
Bruneau, B.G. Signaling and transcriptional networks in heart development and regeneration. Cold Spring Harb. Perspect. Biol., 2013, 5(3) ,a008292.
[http://dx.doi.org/10.1101/cshperspect.a008292] [PMID: 23457256]
[29]
Ling, L.; Gu, S.; Cheng, Y. Resveratrol activates endogenous cardiac stem cells and improves myocardial regeneration following acute myocardial infarction. Mol. Med. Rep., 2017, 15(3), 1188-1194.
[http://dx.doi.org/10.3892/mmr.2017.6143] [PMID: 28138705]
[30]
Liu, J.; Wang, Y.; Cui, J.; Sun, M.; Pu, Z.; Wang, C.; Du, W.; Liu, X.; Wu, J.; Hou, J.; Zhang, S.; Yu, B. miR199a-3p regulates P53 by targeting CABLES1 in mouse cardiac c-kit+ cells to promote proliferation and inhibit apoptosis through a negative feedback loop. Stem Cell Res. Ther., 2017, 8(1), 127.
[http://dx.doi.org/10.1186/s13287-017-0515-4] [PMID: 28583208]
[31]
Zhou, Q.; Sun, Q.; Zhang, Y.; Teng, F.; Sun, J. Up-regulation of miRNA-21 expression promotes migration and proliferation of Sca-1+ cardiac stem cells in mice. Med. Sci. Monit., 2016, 22, 1724-1732.
[http://dx.doi.org/10.12659/MSM.895753] [PMID: 27210794]
[32]
Sayed, A.; Valente, M.; Sassoon, D. Does cardiac development provide heart research with novel therapeutic approaches? F1000 Res., 1756, 2018, 7.
[33]
Kim, J.; Shapiro, L.; Flynn, A. The clinical application of mesenchymal stem cells and cardiac stem cells as a therapy for cardiovascular disease. Pharmacol. Ther., 2015, 151, 8-15.
[http://dx.doi.org/10.1016/j.pharmthera.2015.02.003] [PMID: 25709098]
[34]
Li, W.; Ma, N.; Ong, L.L.; Nesselmann, C.; Klopsch, C.; Ladilov, Y.; Furlani, D.; Piechaczek, C.; Moebius, J.M.; Lützow, K.; Lendlein, A.; Stamm, C.; Li, R.K.; Steinhoff, G. Bcl-2 engineered MSCs inhibited apoptosis and improved heart function. Stem Cells, 2007, 25(8), 2118-2127.
[http://dx.doi.org/10.1634/stemcells.2006-0771] [PMID: 17478584]
[35]
Liang, X.; Ding, Y.; Zhang, Y.; Chai, Y.H.; He, J.; Chiu, S.M.; Gao, F.; Tse, H.F.; Lian, Q. Activation of NRG1-ERBB4 signaling potentiates mesenchymal stem cell-mediated myocardial repairs following myocardial infarction. Cell Death Dis., 2015, 6 ,e1765.
[http://dx.doi.org/10.1038/cddis.2015.91] [PMID: 25996292]
[36]
Hara, H.; Takeda, N.; Kondo, M.; Kubota, M.; Saito, T.; Maruyama, J.; Fujiwara, T.; Maemura, S.; Ito, M.; Naito, A.T.; Harada, M.; Toko, H.; Nomura, S.; Kumagai, H.; Ikeda, Y.; Ueno, H.; Takimoto, E.; Akazawa, H.; Morita, H.; Aburatani, H.; Hata, Y.; Uchiyama, M.; Komuro, I. Discovery of a small molecule to increase cardiomyocytes and protect the heart after ischemic injury. JACC Basic Transl. Sci., 2018, 3(5), 639-653.
[http://dx.doi.org/10.1016/j.jacbts.2018.07.005] [PMID: 30456335]
[37]
Zhang, Y.; Hu, Y.W.; Zheng, L.; Wang, Q. Characteristics and roles of exosomes in cardiovascular disease. DNA Cell Biol., 2017, 36(3), 202-211.
[http://dx.doi.org/10.1089/dna.2016.3496] [PMID: 28112546]
[38]
Shanmuganathan, M.; Vughs, J.; Noseda, M.; Emanueli, C. Exosomes: basic biology and technological advancements suggesting their potential as ischemic heart disease therapeutics. Front. Physiol., 2018, 9, 1159.
[http://dx.doi.org/10.3389/fphys.2018.01159] [PMID: 30524292]
[39]
Ibrahim, A.G-E.; Cheng, K.; Marbán, E. Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Reports, 2014, 2(5), 606-619.
[http://dx.doi.org/10.1016/j.stemcr.2014.04.006] [PMID: 24936449]
[40]
Namazi, H.; Mohit, E.; Namazi, I.; Rajabi, S.; Samadian, A.; Hajizadeh-Saffar, E.; Aghdami, N.; Baharvand, H. Exosomes secreted by hypoxic cardiosphere-derived cells enhance tube formation and increase pro-angiogenic miRNA. J. Cell. Biochem., 2018, 119(5), 4150-4160.
[http://dx.doi.org/10.1002/jcb.26621] [PMID: 29243842]
[41]
Fu, W.B.; Wang, W.E.; Zeng, C.Y. Wnt signaling pathways in myocardial infarction and the therapeutic effects of Wnt pathway inhibitors. Acta Pharmacol. Sin., 2019, 40(1), 9-12.
[http://dx.doi.org/10.1038/s41401-018-0060-4] [PMID: 30002488]
[42]
Palpant, N.J.; Pabon, L.; Roberts, M.; Hadland, B.; Jones, D.; Jones, C.; Moon, R.T.; Ruzzo, W.L.; Bernstein, I.; Zheng, Y.; Murry, C.E. Inhibition of β-catenin signaling respecifies anterior-like endothelium into beating human cardiomyocytes. Development, 2015, 142(18), 3198-3209.
[PMID: 26153229]
[43]
Ozhan, G.; Weidinger, G. Wnt/β-catenin signaling in heart regeneration. Cell Regen. (Lond.), 2015, 4(1), 3.
[http://dx.doi.org/10.1186/s13619-015-0017-8] [PMID: 26157574]
[44]
Bergmann, M.W. WNT signaling in adult cardiac hypertrophy and remodeling: lessons learned from cardiac development. Circ. Res., 2010, 107(10), 1198-1208.
[http://dx.doi.org/10.1161/CIRCRESAHA.110.223768] [PMID: 21071717]
[45]
Meyer, I.S.; Leuschner, F. The role of Wnt signaling in the healing myocardium: a focus on cell specificity. Basic Res. Cardiol., 2018, 113(6), 44.
[http://dx.doi.org/10.1007/s00395-018-0705-y] [PMID: 30327885]
[46]
Li, V.S.; Ng, S.S.; Boersema, P.J.; Low, T.Y.; Karthaus, W.R.; Gerlach, J.P.; Mohammed, S.; Heck, A.J.; Maurice, M.M.; Mahmoudi, T.; Clevers, H. Wnt signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell, 2012, 149(6), 1245-1256.
[http://dx.doi.org/10.1016/j.cell.2012.05.002] [PMID: 22682247]
[47]
Paik, D.T.; Rai, M.; Ryzhov, S.; Sanders, L.N.; Aisagbonhi, O.; Funke, M.J.; Feoktistov, I.; Hatzopoulos, A.K. Wnt10b gain-of-function improves cardiac repair by arteriole formation and attenuation of fibrosis. Circ. Res., 2015, 117(9), 804-816.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.306886] [PMID: 26338900]
[48]
Hofsteen, P.; Robitaille, A.M.; Strash, N.; Palpant, N.; Moon, R.T.; Pabon, L.; Murry, C.E. ALPK2 promotes cardiogenesis in zebrafish and human pluripotent stem cells. iScience, 2018, 2, 88-100.
[http://dx.doi.org/10.1016/j.isci.2018.03.010] [PMID: 29888752]
[49]
Yang, D.; Fu, W.; Li, L.; Xia, X.; Liao, Q.; Yue, R.; Chen, H.; Chen, X.; An, S.; Zeng, C.; Wang, W.E. Therapeutic effect of a novel Wnt pathway inhibitor on cardiac regeneration after myocardial infarction. Clin. Sci. (Lond.), 2017, 131(24), 2919-2932.
[http://dx.doi.org/10.1042/CS20171256] [PMID: 29162747]
[50]
Bastakoty, D.; Young, P.P. Wnt/β-catenin pathway in tissue injury: roles in pathology and therapeutic opportunities for regeneration. FASEB J., 2016, 30(10), 3271-3284.
[http://dx.doi.org/10.1096/fj.201600502R] [PMID: 27335371]
[51]
Xie, S.; Fu, W.; Yu, G.; Hu, X.; Lai, K.S.; Peng, X.; Zhou, Y.; Zhu, X.; Christov, P.; Sawyer, L. Discovering small molecules as Wnt inhibitors that promote heart regeneration and injury repair. J. Mol. Cell Biol., 2020, 12(1), 42-54.
[PMID: 30925593]
[52]
Ng, L.F.; Kaur, P.; Bunnag, N.; Suresh, J.; Sung, I.C.H.; Tan, Q.H.; Gruber, J.; Tolwinski, N.S. WNT Signaling in Disease. Cells, 2019, 8(8) ,E826.
[http://dx.doi.org/10.3390/cells8080826] [PMID: 31382613]
[53]
Abraityte, A.; Vinge, L.E.; Askevold, E.T.; Lekva, T.; Michelsen, A.E.; Ranheim, T.; Alfsnes, K.; Fiane, A.; Aakhus, S.; Lunde, I.G.; Dahl, C.P.; Aukrust, P.; Christensen, G.; Gullestad, L.; Yndestad, A.; Ueland, T. Wnt5a is elevated in heart failure and affects cardiac fibroblast function. J. Mol. Med. (Berl.), 2017, 95(7), 767-777.
[http://dx.doi.org/10.1007/s00109-017-1529-1] [PMID: 28357477]
[54]
Tao, S.; Tang, D.; Morita, Y.; Sperka, T.; Omrani, O.; Lechel, A.; Sakk, V.; Kraus, J.; Kestler, H.A.; Kühl, M.; Rudolph, K.L. Wnt activity and basal niche position sensitize intestinal stem and progenitor cells to DNA damage. EMBO J., 2015, 34(5), 624-640.
[http://dx.doi.org/10.15252/embj.201490700] [PMID: 25609789]
[55]
Meyer, I.S.; Jungmann, A.; Dieterich, C.; Zhang, M.; Lasitschka, F.; Werkmeister, S.; Haas, J.; Müller, O.J.; Boutros, M.; Nahrendorf, M.; Katus, H.A.; Hardt, S.E.; Leuschner, F. The cardiac microenvironment uses non-canonical WNT signaling to activate monocytes after myocardial infarction. EMBO Mol. Med., 2017, 9(9), 1279-1293.
[http://dx.doi.org/10.15252/emmm.201707565] [PMID: 28774883]
[56]
Duan, J.; Gherghe, C.; Liu, D.; Hamlett, E.; Srikantha, L.; Rodgers, L.; Regan, J.N.; Rojas, M.; Willis, M.; Leask, A.; Majesky, M.; Deb, A. Wnt1/βcatenin injury response activates the epicardium and cardiac fibroblasts to promote cardiac repair. EMBO J., 2012, 31(2), 429-442.
[http://dx.doi.org/10.1038/emboj.2011.418] [PMID: 22085926]
[57]
Ueno, S.; Weidinger, G.; Osugi, T.; Kohn, A.D.; Golob, J.L.; Pabon, L.; Reinecke, H.; Moon, R.T.; Murry, C.E.J.P.N.A.S. Biphasic role for Wnt/β-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Natl. Acad. Sci. USA, 2007, 104(23), 9685-9690.
[http://dx.doi.org/10.1073/pnas.0702859104] [PMID: 17522258]
[58]
Paige, S.L.; Osugi, T.; Afanasiev, O.K.; Pabon, L.; Reinecke, H.; Murry, C.E. Endogenous Wnt/β-catenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS One, 2010, 5(6) ,e11134.
[http://dx.doi.org/10.1371/journal.pone.0011134] [PMID: 20559569]
[59]
Cui, X.; He, Z.; Liang, Z.; Chen, Z.; Wang, H.; Zhang, J. Exosomes from adipose-derived mesenchymal stem cells protect the myocardium against ischemia/reperfusion injury through Wnt/β-Catenin signaling pathway. J. Cardiovasc. Pharmacol., 2017, 70(4), 225-231.
[http://dx.doi.org/10.1097/FJC.0000000000000507] [PMID: 28582278]
[60]
Werner, J.H.; Rosenberg, J.H.; Um, J.Y.; Moulton, M.J.; Agrawal, D.K. Molecular discoveries and treatment strategies by direct reprogramming in cardiac regeneration. Transl. Res., 2019, 203, 73-87.
[http://dx.doi.org/10.1016/j.trsl.2018.07.012] [PMID: 30142308]
[61]
Münch, J.; Grivas, D.; González-Rajal, Á.; Torregrosa-Carrión, R.; de la Pompa, J.L. Notch signalling restricts inflammation and serpine1 expression in the dynamic endocardium of the regenerating zebrafish heart. Development, 2017, 144(8), 1425-1440.
[PMID: 28242613]
[62]
Balistreri, C.R.; Madonna, R.; Melino, G.; Caruso, C. The emerging role of Notch pathway in ageing: Focus on the related mechanisms in age-related diseases. Ageing Res. Rev., 2016, 29, 50-65.
[http://dx.doi.org/10.1016/j.arr.2016.06.004] [PMID: 27328278]
[63]
Liu, Z.; Brunskill, E.; Varnum-Finney, B.; Zhang, C.; Zhang, A.; Jay, P.Y.; Bernstein, I.; Morimoto, M.; Kopan, R. The intracellular domains of Notch1 and Notch2 are functionally equivalent during development and carcinogenesis. Development, 2015, 142(14), 2452-2463.
[http://dx.doi.org/10.1242/dev.125492] [PMID: 26062937]
[64]
MacGrogan, D.; Nus, M.; de la Pompa, J.L. Notch signaling in cardiac development and disease. Curr. Top. Dev. Biol., 2010, 92, 333-365.
[http://dx.doi.org/10.1016/S0070-2153(10)92011-5] [PMID: 20816401]
[65]
Salazar, J.L.; Yamamoto, S. Integration of drosophila and human genetics to understand notch signaling related diseases. Adv. Exp. Med. Biol., 2018, 1066, 141-185.
[http://dx.doi.org/10.1007/978-3-319-89512-3_8] [PMID: 30030826]
[66]
Lee, A.; Wei, S.; Schwertani, A. A Notch more: Molecular players in bicuspid aortic valve disease. J. Mol. Cell. Cardiol., 2019, 134, 62-68.
[http://dx.doi.org/10.1016/j.yjmcc.2019.05.018] [PMID: 31150732]
[67]
Yu, L.; Liang, H.; Lu, Z.; Zhao, G.; Zhai, M.; Yang, Y.; Yang, J.; Yi, D.; Chen, W.; Wang, X.; Duan, W.; Jin, Z.; Yu, S. Membrane receptor-dependent Notch1/Hes1 activation by melatonin protects against myocardial ischemia-reperfusion injury: In vivo and in vitro studies. J. Pineal Res., 2015, 59(4), 420-433.
[http://dx.doi.org/10.1111/jpi.12272] [PMID: 26308963]
[68]
Yu, B.; Song, B. Notch 1 signalling inhibits cardiomyocyte apoptosis in ischaemic postconditioning. Heart Lung Circ., 2014, 23(2), 152-158.
[http://dx.doi.org/10.1016/j.hlc.2013.07.004] [PMID: 23948289]
[69]
MacGrogan, D.; Münch, J.; de la Pompa, J.L. Notch and interacting signalling pathways in cardiac development, disease, and regeneration. Nat. Rev. Cardiol., 2018, 15(11), 685-704.
[http://dx.doi.org/10.1038/s41569-018-0100-2] [PMID: 30287945]
[70]
Grego-Bessa, J.; Luna-Zurita, L.; del Monte, G.; Bolós, V.; Melgar, P.; Arandilla, A.; Garratt, A.N.; Zang, H.; Mukouyama, Y.S.; Chen, H.; Shou, W.; Ballestar, E.; Esteller, M.; Rojas, A.; Pérez-Pomares, J.M.; de la Pompa, J.L. Notch signaling is essential for ventricular chamber development. Dev. Cell, 2007, 12(3), 415-429.
[http://dx.doi.org/10.1016/j.devcel.2006.12.011] [PMID: 17336907]
[71]
Fang, X.; Miao, S.; Yu, Y.; Ding, F.; Han, X.; Wu, H.; Zhao, Z-A.; Wang, Y.; Hu, S.; Lei, W. MIR148A family regulates cardiomyocyte differentiation of human embryonic stem cells by inhibiting the DLL1-mediated NOTCH signaling pathway. J. Mol. Cell. Cardiol., 2019, 134, 1-12.
[http://dx.doi.org/10.1016/j.yjmcc.2019.06.014] [PMID: 31233755]
[72]
Diez-Cuñado, M.; Wei, K.; Bushway, P.J.; Maurya, M.R.; Perera, R.; Subramaniam, S.; Ruiz-Lozano, P.; Mercola, M. miRNAs that induce human cardiomyocyte proliferation converge on the hippo pathway. Cell Rep., 2018, 23(7), 2168-2174.
[http://dx.doi.org/10.1016/j.celrep.2018.04.049] [PMID: 29768213]
[73]
Collesi, C.; Zentilin, L.; Sinagra, G.; Giacca, M. Notch1 signaling stimulates proliferation of immature cardiomyocytes. J. Cell Biol., 2008, 183(1), 117-128.
[http://dx.doi.org/10.1083/jcb.200806091] [PMID: 18824567]
[74]
Croquelois, A.; Domenighetti, A.A.; Nemir, M.; Lepore, M.; Rosenblatt-Velin, N.; Radtke, F.; Pedrazzini, T. Control of the adaptive response of the heart to stress via the Notch1 receptor pathway. J. Exp. Med., 2008, 205(13), 3173-3185.
[http://dx.doi.org/10.1084/jem.20081427] [PMID: 19064701]
[75]
Badalzadeh, R.; Azimi, A.; Alihemmati, A.; Yousefi, B. Chronic type-I diabetes could not impede the anti-inflammatory and anti-apoptotic effects of combined postconditioning with ischemia and cyclosporine A in myocardial reperfusion injury. J. Physiol. Biochem., 2017, 73(1), 111-120.
[http://dx.doi.org/10.1007/s13105-016-0530-4] [PMID: 27771871]
[76]
Zhou, X.L.; Wan, L.; Xu, Q.R.; Zhao, Y.; Liu, J.C. Notch signaling activation contributes to cardioprotection provided by ischemic preconditioning and postconditioning. J. Transl. Med., 2013, 11, 251.
[http://dx.doi.org/10.1186/1479-5876-11-251] [PMID: 24098939]
[77]
Zhao, L.; Ben-Yair, R.; Burns, C.E.; Burns, C.G. Endocardial notch signaling promotes cardiomyocyte proliferation in the regenerating zebrafish heart through wnt pathway antagonism. Cell Rep., 2019, 26(3), 546-554.
[http://dx.doi.org/10.1016/j.celrep.2018.12.048] [PMID: 30650349]
[78]
Zhao, L.; Borikova, A.L.; Ben-Yair, R.; Guner-Ataman, B.; MacRae, C.A.; Lee, R.T.; Burns, C.G.; Burns, C.E. Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. Proc. Natl. Acad. Sci. USA, 2014, 111(4), 1403-1408.
[http://dx.doi.org/10.1073/pnas.1311705111] [PMID: 24474765]
[79]
Xiao, N.; Qi, X.Y.; Tang, L.N.; Tan, L.L.; Chen, Y.Q.; Zhao, H.M. VEGF promotes cardiac stem cells differentiation into vascular endothelial cells via the PI3K/Akt signaling pathway. Artif. Cells Nanomed. Biotechnol., 2014, 42(6), 400-405.
[http://dx.doi.org/10.3109/21691401.2013.837473] [PMID: 24059532]
[80]
Olsson, A-K.; Dimberg, A.; Kreuger, J.; Claesson-Welsh, L. VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol., 2006, 7(5), 359-371.
[http://dx.doi.org/10.1038/nrm1911] [PMID: 16633338]
[81]
Eichmann, A.; Simons, M. VEGF signaling inside vascular endothelial cells and beyond. Curr. Opin. Cell Biol., 2012, 24(2), 188-193.
[http://dx.doi.org/10.1016/j.ceb.2012.02.002] [PMID: 22366328]
[82]
Kivelä, R.; Hemanthakumar, K.A.; Vaparanta, K.; Robciuc, M.; Izumiya, Y.; Kidoya, H.; Takakura, N.; Peng, X.; Sawyer, D.B.; Elenius, K.; Walsh, K.; Alitalo, K. Endothelial cells regulate physiological cardiomyocyte growth via VEGFR2-mediated paracrine signaling. Circulation, 2019, 139(22), 2570-2584.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.118.036099] [PMID: 30922063]
[83]
Madonna, R.; De Caterina, R. VEGF receptor switching in heart development and disease. Cardiovasc. Res., 2009, 84(1), 4-6.
[http://dx.doi.org/10.1093/cvr/cvp270] [PMID: 19654124]
[84]
Taimeh, Z.; Loughran, J.; Birks, E.J.; Bolli, R. Vascular endothelial growth factor in heart failure. Nat. Rev. Cardiol., 2013, 10(9), 519-530.
[http://dx.doi.org/10.1038/nrcardio.2013.94] [PMID: 23856679]
[85]
Binsalamah, Z.M.; Paul, A.; Khan, A.A.; Prakash, S.; Shum-Tim, D. Intramyocardial sustained delivery of placental growth factor using nanoparticles as a vehicle for delivery in the rat infarct model. Int. J. Nanomed, 2011, 6, 2667-2678.
[PMID: 22114497]
[86]
Cho, H.M.; Kim, P.H.; Chang, H.K.; Shen, Y.M.; Bonsra, K.; Kang, B.J.; Yum, S.Y.; Kim, J.H.; Lee, S.Y.; Choi, M.C.; Kim, H.H.; Jang, G.; Cho, J.Y. Targeted genome engineering to control VEGF expression in human umbilical cord blood‐derived mesenchymal stem cells: Potential implications for the treatment of myocardial infarction. Stem Cells Transl. Med., 2017, 6(3), 1040-1051.
[http://dx.doi.org/10.1002/sctm.16-0114] [PMID: 28186692]
[87]
Tang, J.M.; Luo, B.; Xiao, J.H.; Lv, Y.X.; Li, X.L.; Zhao, J.H.; Zheng, F.; Zhang, L.; Chen, L.; Yang, J.Y.; Guo, L.Y.; Wang, L.; Yan, Y.W.; Pan, Y.M.; Wang, J.N.; Li, D.S.; Wan, Y.; Chen, S.Y. VEGF-A promotes cardiac stem cell engraftment and myocardial repair in the infarcted heart. Int. J. Cardiol., 2015, 183, 221-231.
[http://dx.doi.org/10.1016/j.ijcard.2015.01.050] [PMID: 25679991]
[88]
Zangi, L.; Lui, K.O.; von Gise, A.; Ma, Q.; Ebina, W.; Ptaszek, L.M.; Später, D.; Xu, H.; Tabebordbar, M.; Gorbatov, R.; Sena, B.; Nahrendorf, M.; Briscoe, D.M.; Li, R.A.; Wagers, A.J.; Rossi, D.J.; Pu, W.T.; Chien, K.R. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat. Biotechnol., 2013, 31(10), 898-907.
[http://dx.doi.org/10.1038/nbt.2682] [PMID: 24013197]
[89]
Karra, R.; Foglia, M.J.; Choi, W-Y.; Belliveau, C.; DeBenedittis, P.; Poss, K.D. Vegfaa instructs cardiac muscle hyperplasia in adult zebrafish. Proc. Natl. Acad. Sci. USA, 2018, 115(35), 8805-8810.
[http://dx.doi.org/10.1073/pnas.1722594115] [PMID: 30104362]
[90]
Zhu, D.; Fang, Y.; Gao, K.; Shen, J.; Zhong, T.P.; Li, F. Vegfa impacts early myocardium development in zebrafish. Int. J. Mol. Sci., 2017, 18(2), 444.
[http://dx.doi.org/10.3390/ijms18020444] [PMID: 28230770]
[91]
Psarras, S.; Beis, D.; Nikouli, S.; Tsikitis, M.; Capetanaki, Y. Three in a box: understanding cardiomyocyte, fibroblast, and innate immune cell interactions to orchestrate cardiac repair processes. Front. Cardiovasc. Med., 2019, 6(32), 32.
[http://dx.doi.org/10.3389/fcvm.2019.00032] [PMID: 31001541]
[92]
Huang, Y.; Harrison, M.R.; Osorio, A.; Kim, J.; Baugh, A.; Duan, C.; Sucov, H.M.; Lien, C-L. Igf signaling is required for cardiomyocyte proliferation during zebrafish heart development and regeneration. PLoS One, 2013, 8(6) ,e67266.
[http://dx.doi.org/10.1371/journal.pone.0067266] [PMID: 23840646]
[93]
Troncoso, R.; Ibarra, C.; Vicencio, J.M.; Jaimovich, E.; Lavandero, S. New insights into IGF-1 signaling in the heart. Trends Endocrinol. Metab., 2014, 25(3), 128-137.
[http://dx.doi.org/10.1016/j.tem.2013.12.002] [PMID: 24380833]
[94]
Ren, J.; Anversa, P. The insulin-like growth factor I system: physiological and pathophysiological implication in cardiovascular diseases associated with metabolic syndrome. Biochem. Pharmacol., 2015, 93(4), 409-417.
[http://dx.doi.org/10.1016/j.bcp.2014.12.006] [PMID: 25541285]
[95]
Kennedy-Lydon, T.; Rosenthal, N. Cardiac regeneration: epicardial mediated repair. Proc. Biol. Sci., 2015, 282(1821), 20152147.
[http://dx.doi.org/10.1098/rspb.2015.2147] [PMID: 26702046]
[96]
Durham, W.J.; Li, Y.-P.; Gerken, E.; Farid, M.; Arbogast, S.; Wolfe, R.R.; Reid, M.B. Fatiguing exercise reduces DNA-binding activity of NF-κB in skeletal muscle nuclei. J Appl Physiol (1985), 2004, 97(5), 1740-1745
[97]
Rabbani, S.; Soleimani, M.; Sahebjam, M.; Imani, M.; Haeri, A.; Ghiaseddin, A.; Nassiri, S.M.; Majd Ardakani, J. Tajik Rostami, M.; Jalali, A.; Ahmadi Tafti, S.H. Simultaneous delivery of Wharton’s jelly mesenchymal stem cells and insulin-like growth factor-1 in acute myocardial infarction. Iran. J. Pharm. Res., 2018, 17(2), 426-441.
[PMID: 29881402]
[98]
Davis, M.E.; Hsieh, P.C.H.; Takahashi, T.; Song, Q.; Zhang, S.; Kamm, R.D.; Grodzinsky, A.J.; Anversa, P.; Lee, R.T. Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc. Natl. Acad. Sci. USA, 2006, 103(21), 8155-8160.
[http://dx.doi.org/10.1073/pnas.0602877103] [PMID: 16698918]
[99]
Haider, H.Kh.; Jiang, S.; Idris, N.M.; Ashraf, M. IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1α/CXCR4 signaling to promote myocardial repair. Circ. Res., 2008, 103(11), 1300-1308.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.186742] [PMID: 18948617]
[100]
Gómez-Mauricio, G.; Moscoso, I.; Martín-Cancho, M-F.; Crisóstomo, V.; Prat-Vidal, C.; Báez-Díaz, C.; Sánchez-Margallo, F.M.; Bernad, A. Combined administration of mesenchymal stem cells overexpressing IGF-1 and HGF enhances neovascularization but moderately improves cardiac regeneration in a porcine model. Stem Cell Res. Ther., 2016, 7(1), 94.
[http://dx.doi.org/10.1186/s13287-016-0350-z] [PMID: 27423905]
[101]
Vinciguerra, M.; Santini, M.P.; Claycomb, W.C.; Ladurner, A.G.; Rosenthal, N. Local IGF-1 isoform protects cardiomyocytes from hypertrophic and oxidative stresses via SirT1 activity. Aging (Albany NY), 2009, 2(1), 43-62.
[http://dx.doi.org/10.18632/aging.100107] [PMID: 20228935]
[102]
Vinciguerra, M.; Santini, M.P.; Martinez, C.; Pazienza, V.; Claycomb, W.C.; Giuliani, A.; Rosenthal, N. mIGF-1/JNK1/SirT1 signaling confers protection against oxidative stress in the heart. Aging Cell, 2012, 11(1), 139-149.
[http://dx.doi.org/10.1111/j.1474-9726.2011.00766.x] [PMID: 22051242]
[103]
Choi, W.Y.; Gemberling, M.; Wang, J.; Holdway, J.E.; Shen, M.C.; Karlstrom, R.O.; Poss, K.D. In vivo monitoring of cardiomyocyte proliferation to identify chemical modifiers of heart regeneration. Development, 2013, 140(3), 660-666.
[http://dx.doi.org/10.1242/dev.088526] [PMID: 23293297]
[104]
Hedhli, N.; Huang, Q.; Kalinowski, A.; Palmeri, M.; Hu, X.; Russell, R.R.; Russell, K.S. Endothelium-derived neuregulin protects the heart against ischemic injury. Circulation, 2011, 123(20), 2254-2262.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.110.991125] [PMID: 21555713]
[105]
Singh, A.P.; Umbarkar, P.; Guo, Y.; Force, T.; Gupte, M.; Lal, H. Inhibition of GSK-3 to induce cardiomyocyte proliferation: a recipe for in situ cardiac regeneration. Cardiovasc. Res., 2019, 115(1), 20-30.
[http://dx.doi.org/10.1093/cvr/cvy255] [PMID: 30321309]
[106]
Gassmann, M.; Casagranda, F.; Orioli, D.; Simon, H.; Lai, C.; Klein, R.; Lemke, G. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature, 1995, 378(6555), 390-394.
[http://dx.doi.org/10.1038/378390a0] [PMID: 7477376]
[107]
Rentschler, S.; Zander, J.; Meyers, K.; France, D.; Levine, R.; Porter, G.; Rivkees, S.A.; Morley, G.E.; Fishman, G.I. Neuregulin-1 promotes formation of the murine cardiac conduction system. Proc. Natl. Acad. Sci. USA, 2002, 99(16), 10464-10469.
[http://dx.doi.org/10.1073/pnas.162301699] [PMID: 12149465]
[108]
Rochais, F.; Fischmeister, R. Acute cardiac effects of neuregulin-1/ErbB signalling. Cardiovasc. Res., 2010, 88(3), 393-394.
[http://dx.doi.org/10.1093/cvr/cvq316] [PMID: 20926427]
[109]
Xin, M.; Olson, E.N.; Bassel-Duby, R. Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair. Nat. Rev. Mol. Cell Biol., 2013, 14(8), 529-541.
[http://dx.doi.org/10.1038/nrm3619] [PMID: 23839576]
[110]
Begeman, I.J.; Kang, J. Transcriptional programs and regeneration enhancers underlying heart regeneration. J. Cardiovasc. Dev. Dis., 2018, 6(1), 2.
[http://dx.doi.org/10.3390/jcdd6010002] [PMID: 30583498]
[111]
Cai, M.X.; Shi, X.C.; Chen, T.; Tan, Z.N.; Lin, Q.Q.; Du, S.J.; Tian, Z.J. Exercise training activates neuregulin 1/ErbB signaling and promotes cardiac repair in a rat myocardial infarction model. Life Sci., 2016, 149, 1-9.
[http://dx.doi.org/10.1016/j.lfs.2016.02.055] [PMID: 26892146]
[112]
Polizzotti, B.D.; Ganapathy, B.; Walsh, S.; Choudhury, S.; Ammanamanchi, N.; Bennett, D.G.; dos Remedios, C.G.; Haubner, B.J.; Penninger, J.M.; Kühn, B. Neuregulin stimulation of cardiomyocyte regeneration in mice and human myocardium reveals a therapeutic window. Sci. Transl. Med., 2015, 7(281) ,281ra45.
[http://dx.doi.org/10.1126/scitranslmed.aaa5171] [PMID: 25834111]
[113]
Rockey, D.C.; Bell, P.D.; Hill, J.A. Fibrosis--a common pathway to organ injury and failure. N. Engl. J. Med., 2015, 372(12), 1138-1149.
[http://dx.doi.org/10.1056/NEJMra1300575] [PMID: 25785971]
[114]
Gilbert, R.W.D.; Vickaryous, M.K.; Viloria-Petit, A.M. Signalling by transforming growth factor beta isoforms in wound healing and tissue regeneration. J. Dev. Biol., 2016, 4(2) ,E21.
[http://dx.doi.org/10.3390/jdb4020021] [PMID: 29615587]
[115]
Talman, V.; Ruskoaho, H. Cardiac fibrosis in myocardial infarction-from repair and remodeling to regeneration. Cell Tissue Res., 2016, 365(3), 563-581.
[http://dx.doi.org/10.1007/s00441-016-2431-9] [PMID: 27324127]
[116]
Frangogiannis, N.G. The inflammatory response in myocardial injury, repair, and remodelling. Nat. Rev. Cardiol., 2014, 11(5), 255-265.
[http://dx.doi.org/10.1038/nrcardio.2014.28] [PMID: 24663091]
[117]
Dobaczewski, M.; Chen, W.; Frangogiannis, N.G. Transforming growth factor (TGF)-β signaling in cardiac remodeling. J. Mol. Cell. Cardiol., 2011, 51(4), 600-606.
[http://dx.doi.org/10.1016/j.yjmcc.2010.10.033] [PMID: 21059352]
[118]
Frangogiannis, N.G. The role of transforming growth factor (TGF)-β in the infarcted myocardium. J. Thorac. Dis., 2017, 9(Suppl. 1), S52-S63.
[http://dx.doi.org/10.21037/jtd.2016.11.19] [PMID: 28446968]
[119]
Derynck, R.; Zhang, Y.E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature, 2003, 425(6958), 577-584.
[http://dx.doi.org/10.1038/nature02006] [PMID: 14534577]
[120]
Lv, Y.; Liu, B.; Wang, H.P.; Zhang, L. Intramyocardial implantation of differentiated rat bone marrow mesenchymal stem cells enhanced by TGF-β1 improves cardiac function in heart failure rats. Braz. J. Med. Biol. Res., 2016, 49(6) ,e5273.
[http://dx.doi.org/10.1590/1414-431x20165273] [PMID: 27254663]
[121]
Hanna, A.; Frangogiannis, N.G. The role of the TGF-β superfamily in myocardial infarction. Front. Cardiovasc. Med., 2019, 6, 140.
[http://dx.doi.org/10.3389/fcvm.2019.00140] [PMID: 31620450]
[122]
Behfar, A.; Zingman, L.V.; Hodgson, D.M.; Rauzier, J.M.; Kane, G.C.; Terzic, A.; Pucéat, M. Stem cell differentiation requires a paracrine pathway in the heart. FASEB J., 2002, 16(12), 1558-1566.
[http://dx.doi.org/10.1096/fj.02-0072com] [PMID: 12374778]
[123]
Singh, A.; Singh, A.; Sen, D. Mesenchymal stem cells in cardiac regeneration: a detailed progress report of the last 6 years (2010-2015). Stem Cell Res. Ther., 2016, 7(1), 82-82.
[http://dx.doi.org/10.1186/s13287-016-0341-0] [PMID: 27259550]
[124]
Bartram, U.; Molin, D.G.; Wisse, L.J.; Mohamad, A.; Sanford, L.P.; Doetschman, T.; Speer, C.P.; Poelmann, R.E.; Gittenberger-de Groot, A.C. Double-outlet right ventricle and overriding tricuspid valve reflect disturbances of looping, myocardialization, endocardial cushion differentiation, and apoptosis in TGF-β(2)-knockout mice. Circulation, 2001, 103(22), 2745-2752.
[http://dx.doi.org/10.1161/01.CIR.103.22.2745] [PMID: 11390347]
[125]
Dewald, O.; Ren, G.; Duerr, G.D.; Zoerlein, M.; Klemm, C.; Gersch, C.; Tincey, S.; Michael, L.H.; Entman, M.L.; Frangogiannis, N.G. Of mice and dogs: species-specific differences in the inflammatory response following myocardial infarction. Am. J. Pathol., 2004, 164(2), 665-677.
[http://dx.doi.org/10.1016/S0002-9440(10)63154-9] [PMID: 14742270]
[126]
Ferreira, R.R.; Abreu, R.D.S.; Vilar-Pereira, G.; Degrave, W.; Meuser-Batista, M.; Ferreira, N.V.C.; da Cruz Moreira, O.; da Silva Gomes, N.L.; Mello de Souza, E.; Ramos, I.P.; Bailly, S.; Feige, J-J.; Lannes-Vieira, J.; de Araújo-Jorge, T.C.; Waghabi, M.C. TGF-β inhibitor therapy decreases fibrosis and stimulates cardiac improvement in a pre-clinical study of chronic Chagas’ heart disease. PLoS Negl. Trop. Dis., 2019, 13(7) ,e0007602.
[http://dx.doi.org/10.1371/journal.pntd.0007602] [PMID: 31365537]
[127]
Hodges, M.M.; Zgheib, C.; Xu, J.; Hu, J.; Dewberry, L.C.; Hilton, S.A.; Allukian, M.W.; Gorman, J.H., III; Gorman, R.C.; Liechty, K.W. Differential expression of transforming growth factor-β1 is associated with fetal regeneration after myocardial infarction. Ann. Thorac. Surg., 2019, 108(1), 59-66.
[http://dx.doi.org/10.1016/j.athoracsur.2018.12.042] [PMID: 30690019]
[128]
Yndestad, A.; Ueland, T.; Øie, E.; Florholmen, G.; Halvorsen, B.; Attramadal, H.; Simonsen, S.; Frøland, S.S.; Gullestad, L.; Christensen, G.; Damås, J.K.; Aukrust, P. Elevated levels of activin A in heart failure: potential role in myocardial remodeling. Circulation, 2004, 109(11), 1379-1385.
[http://dx.doi.org/10.1161/01.CIR.0000120704.97934.41] [PMID: 14993131]
[129]
Wang, Y.; Lu, P.; Zhao, D.; Sheng, J. Targeting the hedgehog signaling pathway for cardiac repair and regeneration. Herz, 2017, 42(7), 662-668.
[http://dx.doi.org/10.1007/s00059-016-4500-y] [PMID: 27878328]
[130]
Johnson, N.R.; Wang, Y. Controlled delivery of sonic hedgehog morphogen and its potential for cardiac repair. PLoS One, 2013, 8(5) ,e63075.
[http://dx.doi.org/10.1371/journal.pone.0063075] [PMID: 23690982]
[131]
Lee, R.T.H.; Zhao, Z.; Ingham, P.W. Hedgehog signalling. Development, 2016, 143(3), 367-372.
[http://dx.doi.org/10.1242/dev.120154] [PMID: 26839340]
[132]
Dunaeva, M.; Waltenberger, J. Hh signaling in regeneration of the ischemic heart. Cell. Mol. Life Sci., 2017, 74(19), 3481-3490.
[http://dx.doi.org/10.1007/s00018-017-2534-9] [PMID: 28523343]
[133]
Brennan, D.; Chen, X.; Cheng, L.; Mahoney, M.; Riobo, N.A. Noncanonical Hedgehog signaling. Vitam. Horm., 2012, 88, 55-72.
[http://dx.doi.org/10.1016/B978-0-12-394622-5.00003-1] [PMID: 22391299]
[134]
Kawagishi, H.; Xiong, J.; Rovira, I.I.; Pan, H.; Yan, Y.; Fleischmann, B.K.; Yamada, M.; Finkel, T. Sonic hedgehog signaling regulates the mammalian cardiac regenerative response. J. Mol. Cell. Cardiol., 2018, 123, 180-184.
[http://dx.doi.org/10.1016/j.yjmcc.2018.09.005] [PMID: 30236923]
[135]
Praktiknjo, S.D.; Saad, F.; Maier, D.; Ip, P.; Hipfner, D.R.J.J.B.C. Activation of Smoothened in the Hedgehog pathway unexpectedly increases Gαs-dependent cAMP levels in Drosophila. J. Biol. Chem., 2018, 293(35), 13496-13508.
[http://dx.doi.org/10.1074/jbc.RA118.001953] [PMID: 30018136]
[136]
Carbe, C.J.; Cheng, L.; Addya, S.; Gold, J.I.; Gao, E.; Koch, W.J.; Riobo, N.A.J.A.J.P-H. Gi proteins mediate activation of the canonical hedgehog pathway in the myocardium. Am. J. Physiol. Heart Circ. Physiol., 2014, 307(1), H66-H72.
[http://dx.doi.org/10.1152/ajpheart.00166.2014] [PMID: 24816261]
[137]
Paulis, L.; Fauconnier, J.; Cazorla, O.; Thireau, J.; Soleti, R.; Vidal, B.; Ouillé, A.; Bartholome, M.; Bideaux, P.; Roubille, F.; Le Guennec, J.Y.; Andriantsitohaina, R.; Martínez, M.C.; Lacampagne, A. Activation of Sonic hedgehog signaling in ventricular cardiomyocytes exerts cardioprotection against ischemia reperfusion injuries. Sci. Rep., 2015, 5, 7983.
[http://dx.doi.org/10.1038/srep07983] [PMID: 25613906]
[138]
Rowton, M.; Hoffmann, A.D.; Steimle, J.D.; Yang, X.H.; Guzzetta, A.; Lazarevic, S.; Kim, C.; Deng, N.; Lu, E.; Jacobs-Li, J.; Yu, S.; Hanson, E.; Perez-Cervantes, C.; Chan, S.S-K.; Ikegami, K.; Garry, D.J.; Kyba, M.; Moskowitz, I.P. Hedgehog signaling controls progenitor differentiation timing during heart development. Semin. Cell Dev. Biol., 2021.
[http://dx.doi.org/10.1016/j.semcdb.2021.06.002] [PMID: 34144893]
[139]
Mackie, A.R.; Klyachko, E.; Thorne, T.; Schultz, K.M.; Millay, M.; Ito, A.; Kamide, C.E.; Liu, T.; Gupta, R.; Sahoo, S.; Misener, S.; Kishore, R.; Losordo, D.W. Sonic hedgehog-modified human CD34+ cells preserve cardiac function after acute myocardial infarction. Circ. Res., 2012, 111(3), 312-321.
[http://dx.doi.org/10.1161/CIRCRESAHA.112.266015] [PMID: 22581926]
[140]
Hayden, M.S.; Ghosh, S. NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev., 2012, 26(3), 203-234.
[http://dx.doi.org/10.1101/gad.183434.111] [PMID: 22302935]
[141]
Park, S.R.; Kim, K.H.; Kwun, M.J.; Lee, J.Y.; Won, R.; Han, C.W.; Choi, J.Y.; Joo, M. Differential Regulation of NF-κB and Nrf2 by Bojungikki-Tang Is Associated with Suppressing Lung Inflammation. Evid. Based Complement. Alternat. Med., 2018, 2018
[http://dx.doi.org/10.1155/2018/5059469]
[142]
Gaspar-Pereira, S.; Fullard, N.; Townsend, P.A.; Banks, P.S.; Ellis, E.L.; Fox, C.; Maxwell, A.G.; Murphy, L.B.; Kirk, A.; Bauer, R.; Caamaño, J.H.; Figg, N.; Foo, R.S.; Mann, J.; Mann, D.A.; Oakley, F. The NF-κB subunit c-Rel stimulates cardiac hypertrophy and fibrosis. Am. J. Pathol., 2012, 180(3), 929-939.
[http://dx.doi.org/10.1016/j.ajpath.2011.11.007] [PMID: 22210479]
[143]
Tsoulfas, G.; Geller, D.A. NF-kappaB in transplantation: friend or foe? Transpl. Infect. Dis., 2001, 3(4), 212-219.
[http://dx.doi.org/10.1034/j.1399-3062.2001.30405.x] [PMID: 11844153]
[144]
Frantz, S.; Fraccarollo, D.; Wagner, H.; Behr, T.M.; Jung, P.; Angermann, C.E.; Ertl, G.; Bauersachs, J. Sustained activation of nuclear factor kappa B and activator protein 1 in chronic heart failure. Cardiovasc. Res., 2003, 57(3), 749-756.
[http://dx.doi.org/10.1016/S0008-6363(02)00723-X] [PMID: 12618236]
[145]
Peterson, J.M.; Wang, D.J.; Shettigar, V.; Roof, S.R.; Canan, B.D.; Bakkar, N.; Shintaku, J.; Gu, J-M.; Little, S.C.; Ratnam, N.M.; Londhe, P.; Lu, L.; Gaw, C.E.; Petrosino, J.M.; Liyanarachchi, S.; Wang, H.; Janssen, P.M.L.; Davis, J.P.; Ziolo, M.T.; Sharma, S.M.; Guttridge, D.C. NF-κB inhibition rescues cardiac function by remodeling calcium genes in a Duchenne muscular dystrophy model. Nat. Commun., 2018, 9(1), 3431.
[http://dx.doi.org/10.1038/s41467-018-05910-1] [PMID: 30143619]
[146]
Ye, W.; Tang, X.; Yang, Z.; Liu, C.; Zhang, X.; Jin, J.; Lyu, J. Plasma-derived exosomes contribute to inflammation via the TLR9-NF-κB pathway in chronic heart failure patients. Mol. Immunol., 2017, 87, 114-121.
[http://dx.doi.org/10.1016/j.molimm.2017.03.011] [PMID: 28433888]
[147]
Okkenhaug, K. Signaling by the phosphoinositide 3-kinase family in immune cells. Annu. Rev. Immunol., 2013, 31, 675-704.
[http://dx.doi.org/10.1146/annurev-immunol-032712-095946] [PMID: 23330955]
[148]
Tian, H.; Guo, M.; Zhuang, Y.; Chu, J.; Zhang, S. Enhanced proliferation of bone marrow mesenchymal stem cells by co-culture with TM4 mouse Sertoli cells: involvement of the EGF/PI3K/AKT pathway. Mol. Cell. Biochem., 2014, 393(1-2), 155-164.
[http://dx.doi.org/10.1007/s11010-014-2055-x] [PMID: 24748323]
[149]
Li, J.W.; Wang, X.Y.; Zhang, X.; Gao, L.; Wang, L.F.; Yin, X.H. ( -)- Epicatechin protects against myocardial ischemia induced cardiac injury via activation of the PTEN/PI3K/AKT pathway. Mol. Med. Rep., 2018, 17(6), 8300-8308.
[http://dx.doi.org/10.3892/mmr.2018.8870] [PMID: 29658565]
[150]
Chang, Z.; Zhang, Q.; Feng, Q.; Xu, J.; Teng, T.; Luan, Q.; Shan, C.; Hu, Y.; Hemmings, B.A.; Gao, X.; Yang, Z. Deletion of Akt1 causes heart defects and abnormal cardiomyocyte proliferation. Dev. Biol., 2010, 347(2), 384-391.
[http://dx.doi.org/10.1016/j.ydbio.2010.08.033] [PMID: 20816796]
[151]
Chen, J.; Crawford, R.; Chen, C.; Xiao, Y. The key regulatory roles of the PI3K/Akt signaling pathway in the functionalities of mesenchymal stem cells and applications in tissue regeneration. Tissue Eng. Part B Rev., 2013, 19(6), 516-528.
[http://dx.doi.org/10.1089/ten.teb.2012.0672] [PMID: 23651329]
[152]
Leach, J.P.; Martin, J.F. Cardiomyocyte proliferation for therapeutic regeneration. Curr. Cardiol. Rep., 2018, 20(8), 63.
[http://dx.doi.org/10.1007/s11886-018-1011-x] [PMID: 29904823]
[153]
Bareja, A.; Hodgkinson, C.P.; Payne, A.J.; Pratt, R.E.; Dzau, V.J. HASF (C3orf58) is a novel ligand of the insulin-like growth factor 1 receptor. Biochem. J., 2017, 474(5), 771-780.
[http://dx.doi.org/10.1042/BCJ20160976] [PMID: 28096202]
[154]
Yang, B.; Yan, P.; Gong, H.; Zuo, L.; Shi, Y.; Guo, J.; Guo, R.; Xie, J.; Li, B. TWEAK protects cardiomyocyte against apoptosis in a PI3K/AKT pathway dependent manner. Am. J. Transl. Res., 2016, 8(9), 3848-3860.
[PMID: 27725864]
[155]
Leach, J.P.; Heallen, T.; Zhang, M.; Rahmani, M.; Morikawa, Y.; Hill, M.C.; Segura, A.; Willerson, J.T.; Martin, J.F. Hippo pathway deficiency reverses systolic heart failure after infarction. Nature, 2017, 550(7675), 260-264.
[http://dx.doi.org/10.1038/nature24045] [PMID: 28976966]
[156]
Heallen, T.; Morikawa, Y.; Leach, J.; Tao, G.; Willerson, J.T.; Johnson, R.L.; Martin, J.F. Hippo signaling impedes adult heart regeneration. Development, 2013, 140(23), 4683-4690.
[http://dx.doi.org/10.1242/dev.102798] [PMID: 24255096]
[157]
von Gise, A.; Lin, Z.; Schlegelmilch, K.; Honor, L.B.; Pan, G.M.; Buck, J.N.; Ma, Q.; Ishiwata, T.; Zhou, B.; Camargo, F.D.; Pu, W.T. YAP1, the nuclear target of Hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy. Proc. Natl. Acad. Sci. USA, 2012, 109(7), 2394-2399.
[http://dx.doi.org/10.1073/pnas.1116136109] [PMID: 22308401]
[158]
Jang, J.W.; Kim, M.K.; Bae, S.C. Reciprocal regulation of YAP/TAZ by the Hippo pathway and the Small GTPase pathway. Small GTPases, 2020, 11(14), 280-288.
[http://dx.doi.org/10.1080/21541248.2018.1435986] [PMID: 29457552]
[159]
Ikeda, S.; Sadoshima, J. Regulation of myocardial cell growth and death by the hippo pathway. Circ. J., 2016, 80(7), 1511-1519.
[http://dx.doi.org/10.1253/circj.CJ-16-0476] [PMID: 27302848]
[160]
Zhou, Q.; Li, L.; Zhao, B.; Guan, K.L. The hippo pathway in heart development, regeneration, and diseases. Circ. Res., 2015, 116(8), 1431-1447.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.303311] [PMID: 25858067]
[161]
Haskins, J.W.; Nguyen, D.X.; Stern, D.F. Neuregulin 1-activated ERBB4 interacts with YAP to induce Hippo pathway target genes and promote cell migration. Sci. Signal., 2014, 7(355), ra116.
[http://dx.doi.org/10.1126/scisignal.2005770] [PMID: 25492965]
[162]
Xiao, Y.; Hill, M.C.; Zhang, M.; Martin, T.J.; Morikawa, Y.; Wang, S.; Moise, A.R.; Wythe, J.D.; Martin, J.F. Hippo signaling plays an essential role in cell state transitions during cardiac fibroblast development. Dev. Cell, 2018, 45(2), 153-169.
[http://dx.doi.org/10.1016/j.devcel.2018.03.019] [PMID: 29689192]
[163]
Xin, M.; Kim, Y.; Sutherland, L.B.; Qi, X.; McAnally, J.; Schwartz, R.J.; Richardson, J.A.; Bassel-Duby, R.; Olson, E.N. Regulation of insulin-like growth factor signaling by Yap governs cardiomyocyte proliferation and embryonic heart size. Sci. Signal., 2011, 4(196), ra70.
[http://dx.doi.org/10.1126/scisignal.2002278] [PMID: 22028467]
[164]
Wang, J.; Liu, S.; Heallen, T.; Martin, J.F. The Hippo pathway in the heart: pivotal roles in development, disease, and regeneration. Nat. Rev. Cardiol., 2018, 15(11), 672-684.
[http://dx.doi.org/10.1038/s41569-018-0063-3] [PMID: 30111784]
[165]
Moya, I.M.; Halder, G. Hippo-YAP/TAZ signalling in organ regeneration and regenerative medicine. Nat. Rev. Mol. Cell Biol., 2019, 20(4), 211-226.
[http://dx.doi.org/10.1038/s41580-018-0086-y] [PMID: 30546055]
[166]
Wang, P.; Mao, B.; Luo, W.; Wei, B.; Jiang, W.; Liu, D.; Song, L.; Ji, G.; Yang, Z.; Lai, Y-Q.; Yuan, Z. The alteration of Hippo/YAP signaling in the development of hypertrophic cardiomyopathy. Basic Res. Cardiol., 2014, 109(5), 435.
[http://dx.doi.org/10.1007/s00395-014-0435-8] [PMID: 25168380]
[167]
Mia, M.M.; Singh, M.K. The hippo signaling pathway in cardiac development and diseases. Front. Cell Dev. Biol., 2019, 7, 211.
[http://dx.doi.org/10.3389/fcell.2019.00211] [PMID: 31632964]
[168]
Lin, Z.; von Gise, A.; Zhou, P.; Gu, F.; Ma, Q.; Jiang, J.; Yau, A.L.; Buck, J.N.; Gouin, K.A.; van Gorp, P.R.; Zhou, B.; Chen, J.; Seidman, J.G.; Wang, D.Z.; Pu, W.T. Cardiac-specific YAP activation improves cardiac function and survival in an experimental murine MI model. Circ. Res., 2014, 115(3), 354-363.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.303632] [PMID: 24833660]
[169]
Triastuti, E.; Nugroho, A.B.; Zi, M.; Prehar, S.; Kohar, Y.S.; Bui, T.A.; Stafford, N.; Cartwright, E.J.; Abraham, S.; Oceandy, D. Pharmacological inhibition of Hippo pathway, with the novel kinase inhibitor XMU-MP-1, protects the heart against adverse effects during pressure overload. Br. J. Pharmacol., 2019, 176(20), 3956-3971.
[http://dx.doi.org/10.1111/bph.14795] [PMID: 31328787]
[170]
Liu, S.; Martin, J.F. The regulation and function of the Hippo pathway in heart regeneration. Wiley Interdiscip. Rev. Dev. Biol., 2019, 8(1) ,e335.
[http://dx.doi.org/10.1002/wdev.335] [PMID: 30169913]
[171]
Camberos, V.; Baio, J.; Bailey, L.; Hasaniya, N.; Lopez, L.V.; Kearns-Jonker, M. Effects of spaceflight and simulated microgravity on YAP1 expression in cardiovascular progenitors: implications for cell-based repair. Int. J. Mol. Sci., 2019, 20(11) ,E2742.
[http://dx.doi.org/10.3390/ijms20112742] [PMID: 31167392]
[172]
Flinn, M.A.; Jeffery, B.E.; O’Meara, C.C.; Link, B.A. Yap is required for scar formation but not myocyte proliferation during heart regeneration in zebrafish. Cardiovasc. Res., 2019, 115(3), 570-577.
[http://dx.doi.org/10.1093/cvr/cvy243] [PMID: 30295714]
[173]
Ladage, D.; Yaniz-Galende, E.; Rapti, K.; Ishikawa, K.; Tilemann, L.; Shapiro, S.; Takewa, Y.; Muller-Ehmsen, J.; Schwarz, M.; Garcia, M.J.; Sanz, J.; Hajjar, R.J.; Kawase, Y. Stimulating myocardial regeneration with periostin Peptide in large mammals improves function post-myocardial infarction but increases myocardial fibrosis. PLoS One, 2013, 8(5) ,e59656.
[http://dx.doi.org/10.1371/journal.pone.0059656] [PMID: 23700403]
[174]
Shimazaki, M.; Nakamura, K.; Kii, I.; Kashima, T.; Amizuka, N.; Li, M.; Saito, M.; Fukuda, K.; Nishiyama, T.; Kitajima, S.; Saga, Y.; Fukayama, M.; Sata, M.; Kudo, A. Periostin is essential for cardiac healing after acute myocardial infarction. J. Exp. Med., 2008, 205(2), 295-303.
[http://dx.doi.org/10.1084/jem.20071297] [PMID: 18208976]
[175]
Chen, Z.; Xie, J.; Hao, H.; Lin, H.; Wang, L.; Zhang, Y.; Chen, L.; Cao, S.; Huang, X.; Liao, W.; Bin, J.; Liao, Y. Ablation of periostin inhibits post-infarction myocardial regeneration in neonatal mice mediated by the phosphatidylinositol 3 kinase/glycogen synthase kinase 3β/cyclin D1 signalling pathway. Cardiovasc. Res., 2017, 113(6), 620-632.
[http://dx.doi.org/10.1093/cvr/cvx001] [PMID: 28453729]
[176]
Cho, Y.H.; Cha, M.J.; Song, B.W.; Kim, I.K.; Song, H.; Chang, W.; Lim, S.; Ham, O.; Lee, S.Y.; Choi, E.; Kwon, H.M.; Hwang, K.C. Enhancement of MSC adhesion and therapeutic efficiency in ischemic heart using lentivirus delivery with periostin. Biomaterials, 2012, 33(5), 1376-1385.
[http://dx.doi.org/10.1016/j.biomaterials.2011.10.078] [PMID: 22112759]
[177]
Dorn, G.W., II Periostin and myocardial repair, regeneration, and recovery. N. Engl. J. Med., 2007, 357(15), 1552-1554.
[http://dx.doi.org/10.1056/NEJMcibr074816] [PMID: 17928607]
[178]
Maddaluno, L.; Urwyler, C.; Werner, S. Fibroblast growth factors: key players in regeneration and tissue repair. Development, 2017, 144(22), 4047-4060.
[http://dx.doi.org/10.1242/dev.152587] [PMID: 29138288]
[179]
Missinato, M.A.; Saydmohammed, M.; Zuppo, D.A.; Rao, K.S.; Opie, G.W.; Kühn, B.; Tsang, M. Dusp6 attenuates Ras/MAPK signaling to limit zebrafish heart regeneration. Development, 2018, 145(5) ,dev157206.
[http://dx.doi.org/10.1242/dev.157206] [PMID: 29444893]
[180]
Lian, H.; Ma, Y.; Feng, J.; Dong, W.; Yang, Q.; Lu, D.; Zhang, L. Heparin-binding EGF-like growth factor induces heart interstitial fibrosis via an Akt/mTor/p70s6k pathway. PLoS One, 2012, 7(9) ,e44946.
[http://dx.doi.org/10.1371/journal.pone.0044946] [PMID: 22984591]
[181]
Wang, Y.; Ahmad, N.; Wani, M.A.; Ashraf, M. Hepatocyte growth factor prevents ventricular remodeling and dysfunction in mice via Akt pathway and angiogenesis. J. Mol. Cell. Cardiol., 2004, 37(5), 1041-1052.
[http://dx.doi.org/10.1016/j.yjmcc.2004.09.004] [PMID: 15522281]
[182]
Kim, J.; Wu, Q.; Zhang, Y.; Wiens, K.M.; Huang, Y.; Rubin, N.; Shimada, H.; Handin, R.I.; Chao, M.Y.; Tuan, T-L.; Starnes, V.A.; Lien, C.L. PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc. Natl. Acad. Sci. USA, 2010, 107(40), 17206-17210.
[http://dx.doi.org/10.1073/pnas.0915016107] [PMID: 20858732]
[183]
Chong, J.J.; Reinecke, H.; Iwata, M.; Torok-Storb, B.; Stempien-Otero, A.; Murry, C.E. Progenitor cells identified by PDGFR-alpha expression in the developing and diseased human heart. Stem Cells Dev., 2013, 22(13), 1932-1943.
[http://dx.doi.org/10.1089/scd.2012.0542] [PMID: 23391309]
[184]
Yue, Z.; Chen, J.; Lian, H.; Pei, J.; Li, Y.; Chen, X.; Song, S.; Xia, J.; Zhou, B.; Feng, J.; Zhang, X.; Hu, S.; Nie, Y. PDGFR-β Signaling Regulates Cardiomyocyte Proliferation and Myocardial Regeneration. Cell Rep., 2019, 28(4), 966-978.
[http://dx.doi.org/10.1016/j.celrep.2019.06.065] [PMID: 31340157]
[185]
Beets, K.; Staring, M.W.; Criem, N.; Maas, E.; Schellinx, N.; de Sousa Lopes, S.M.C.; Umans, L.; Zwijsen, A. BMP-SMAD signalling output is highly regionalized in cardiovascular and lymphatic endothelial networks. BMC Dev. Biol., 2016, 16(1), 34.
[http://dx.doi.org/10.1186/s12861-016-0133-x] [PMID: 27724845]

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