An epigenetic perspective on the failing heart and pluripotent-derived-cardiomyocytes for cell replacement therapy
Received date: 15 Sep 2014
Accepted date: 22 Oct 2014
Published date: 14 Feb 2015
Copyright
As life expectancy rises, the prevalence of heart failure is steadily increasing, while donors for organ transplantation remain in short supply (Zwi-Dantsis and Gepstein, 2012). Indeed, myocardial infarction represents the foremost cause of death within industrialized nations (Henning, 2011) and further, approximately 1% of all newborns harbor a congenital heart defect. Although medical interventions allow>80% of those with cardiac defects to survive to adulthood, there are often extreme emotional and financial burdens that accompany such congenital anomalies, and many individuals will remain at a heightened risk for myocardial infarction throughout the remainder of their lives (Verheugt et al., 2010; Amianto et al., 2011). In this review, we will discuss the nature of the failing heart and strategies for repair from an epigenetic standpoint. Significant focus will reside on pluripotent-to-cardiomyocyte differentiation for cell replacement, epigenetic mechanisms of cardiomyocyte differentiation, epigenetic “memories,” and epigenetic control of cardiomyocyte cell fate toward translational utility.
Key words： heart failure; pluripotent; cardiomyocytes; epigenetics; DNA methylation; lncRNA
Joshua D. TOMPKINS , Arthur D. RIGGS . An epigenetic perspective on the failing heart and pluripotent-derived-cardiomyocytes for cell replacement therapy[J]. Frontiers in Biology, 2015 , 10(1) : 11 -27 . DOI: 10.1007/s11515-014-1340-0
| 1 |
Ahmed W, Ali I S, Riaz M, Younas A, Sadeque A, Niazi A K, Niazi S H, Ali S H B, Azam M, Qamar R (2013). Association of ANRIL polymorphism (rs1333049:C>G) with myocardial infarction and its pharmacogenomic role in hypercholesterolemia. Gene, 515(2): 416–420
|
| 2 |
Amianto F, Bergui G, Abbate-Daga G, Bellicanta A, Munno D, Fassino S (2011). Growing up with a congenital heart disease: neuro-cognitive, psychopathological and quality of life outcomes. Panminerva Med, 53(2): 109–127
|
| 3 |
Anderson D, Self T, Mellor I R, Goh G, Hill S J, Denning C (2007). Transgenic enrichment of cardiomyocytes from human embryonic stem cells. Mol Ther, 15(11): 2027–2036
|
| 4 |
Antos C L, McKinsey T A, Dreitz M, Hollingsworth L M, Zhang C L, Schreiber K, Rindt H, Gorczynski R J, Olson E N (2003). Dose-dependent blockade to cardiomyocyte hypertrophy by histone deacetylase inhibitors. J Biol Chem, 278(31): 28930–28937
|
| 5 |
Arya G, Maitra A, Grigoryev S A (2010). A structural perspective on the where, how, why, and what of nucleosome positioning. J Biomol Struct Dyn, 27(6): 803–820
|
| 6 |
Awad S, Kunhi M, Little G H, Bai Y, An W, Bers D, Kedes L, Poizat C (2013). Nuclear CaMKII enhances histone H3 phosphorylation and remodels chromatin during cardiac hypertrophy. Nucleic Acids Res, 41(16): 7656–7672
|
| 7 |
Backs J, Song K, Bezprozvannaya S, Chang S, Olson E N (2006). CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J Clin Invest, 116(7): 1853–1864
|
| 8 |
Bannister A J, Kouzarides T (2011). Regulation of chromatin by histone modifications. Cell Res, 21(3): 381–395
|
| 9 |
Bar-Nur O, Russ H A, Efrat S, Benvenisty N (2011). Epigenetic memory and preferential lineage-specific differentiation in induced pluripotent stem cells derived from human pancreatic islet beta cells. Cell Stem Cell, 9(1): 17–23
|
| 10 |
Bergmann O, Bhardwaj R D, Bernard S, Zdunek S, Barnabé-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz B A, Druid H, Jovinge S, Frisén J (2009). Evidence for cardiomyocyte renewal in humans. Science, 324(5923): 98–102
|
| 11 |
Bossuyt J, Helmstadter K, Wu X, Clements-Jewery H, Haworth R S, Avkiran M, Martin J L, Pogwizd S M, Bers D M (2008). Ca2+/calmodulin-dependent protein kinase IIdelta and protein kinase D overexpression reinforce the histone deacetylase 5 redistribution in heart failure. Circ Res, 102(6): 695–702
|
| 12 |
Brito-Martins M, Harding S E, Ali N N (2008). beta(1)- and beta(2)-adrenoceptor responses in cardiomyocytes derived from human embryonic stem cells: comparison with failing and non-failing adult human heart. Br J Pharmacol, 153(4): 751–759
|
| 13 |
Brons I G, Smithers L E, Trotter M W, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes S M, Howlett S K, Clarkson A, Ahrlund-Richter L, Pedersen R A, Vallier L (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature, 448(7150): 191–195
|
| 14 |
Cai X, Hagedorn C H, Cullen B R (2004). Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA, 10(12): 1957–1966
|
| 15 |
Cai Y, Geutjes E J, de Lint K, Roepman P, Bruurs L, Yu L R, Wang W, van Blijswijk J, Mohammad H, de Rink I, Bernards R, Baylin S B (2014). The NuRD complex cooperates with DNMTs to maintain silencing of key colorectal tumor suppressor genes. Oncogene, 33(17): 2157–2168
|
| 16 |
Carpenter L, Carr C, Yang C T, Stuckey D J, Clarke K, Watt S M (2012). Efficient differentiation of human induced pluripotent stem cells generates cardiac cells that provide protection following myocardial infarction in the rat. Stem Cells Dev, 21(6): 977–986
|
| 17 |
Caspi O, Huber I, Kehat I, Habib M, Arbel G, Gepstein A, Yankelson L, Aronson D, Beyar R, Gepstein L (2007a). Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. J Am Coll Cardiol, 50(19): 1884–1893
|
| 18 |
Caspi O, Lesman A, Basevitch Y, Gepstein A, Arbel G, Habib I H, Gepstein L, Levenberg S (2007b). Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res, 100(2): 263–272
|
| 19 |
Chang S, McKinsey T A, Zhang C L, Richardson J A, Hill J A, Olson E N (2004). Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol Cell Biol, 24(19): 8467–8476
|
| 20 |
Chen J, Huang Z P, Seok H Y, Ding J, Kataoka M, Zhang Z, Hu X, Wang G, Lin Z, Wang S, Pu W T, Liao R, Wang D Z (2013). mir-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts. Circ Res, 112(12): 1557–1566
|
| 21 |
Chen T, Dent S Y (2014). Chromatin modifiers and remodellers: regulators of cellular differentiation. Nat Rev Genet, 15(2): 93–106
|
| 22 |
Chimenti I, Gaetani R, Barile L, Forte E, Ionta V, Angelini F, Frati G, Messina E, Giacomello A (2012). Isolation and expansion of adult cardiac stem/progenitor cells in the form of cardiospheres from human cardiac biopsies and murine hearts. Methods Mol Biol, 879: 327–338
|
| 23 |
Choi S C, Yoon J, Shim W J, Ro Y M, Lim D S (2004). 5-azacytidine induces cardiac differentiation of P19 embryonic stem cells. Exp Mol Med, 36(6): 515–523
|
| 24 |
Chong J J, Yang X, Don C W, Minami E, Liu Y W, Weyers J J, Mahoney W M, Van Biber B, Cook S M, Palpant N J, Gantz J A, Fugate J A, Muskheli V, Gough G M, Vogel K W, Astley C A, Hotchkiss C E, Baldessari A, Pabon L, Reinecke H, Gill E A, Nelson V, Kiem H P, Laflamme M A, Murry C E (2014). Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature, 510(7504): 273–277
|
| 25 |
Chow M, Boheler K R, Li R A (2013a). Human pluripotent stem cell-derived cardiomyocytes for heart regeneration, drug discovery and disease modeling: from the genetic, epigenetic, and tissue modeling perspectives. Stem Cell Res Ther, 4(4): 97
|
| 26 |
Chow M Z, Geng L, Kong C W, Keung W, Fung J C, Boheler K R, Li R A (2013b). Epigenetic regulation of the electrophysiological phenotype of human embryonic stem cell-derived ventricular cardiomyocytes: insights for driven maturation and hypertrophic growth. Stem Cells Dev, 22(19): 2678–2690
|
| 27 |
Cohen S M (2014). Everything old is new again: (linc)RNAs make proteins! EMBO J, 33(9): 937–938
|
| 28 |
Cohn J N, Ferrari R, Sharpe N (2000). Cardiac remodeling—concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an International Forum on Cardiac Remodeling. J Am Coll Cardiol, 35(3): 569–582
|
| 29 |
Coppola A, Romito A, Borel C, Gehrig C, Gagnebin M, Falconnet E, Izzo A, Altucci L, Banfi S, Antonarakis S E, Minchiotti G, Cobellis G (2014). Cardiomyogenesis is controlled by the miR-99a/let-7c cluster and epigenetic modifications. Stem Cell Res, 12(2): 323–337
|
| 30 |
Dimmeler S, Zeiher A M, Schneider M D (2005). Unchain my heart: the scientific foundations of cardiac repair. J Clin Invest, 115(3): 572–583
|
| 31 |
Djebali S, Davis C A, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov G K, Khatun J, Williams B A, Zaleski C, Rozowsky J, Röder M, Kokocinski F, Abdelhamid R F, Alioto T, Antoshechkin I, Baer M T, Bar N S, Batut P, Bell K, Bell I, Chakrabortty S, Chen X, Chrast J, Curado J, Derrien T, Drenkow J, Dumais E, Dumais J, Duttagupta R, Falconnet E, Fastuca M, Fejes-Toth K, Ferreira P, Foissac S, Fullwood M J, Gao H, Gonzalez D, Gordon A, Gunawardena H, Howald C, Jha S, Johnson R, Kapranov P, King B, Kingswood C, Luo O J, Park E, Persaud K, Preall J B, Ribeca P, Risk B, Robyr D, Sammeth M, Schaffer L, See L H, Shahab A, Skancke J, Suzuki A M, Takahashi H, Tilgner H, Trout D, Walters N, Wang H, Wrobel J, Yu Y, Ruan X, Hayashizaki Y, Harrow J, Gerstein M, Hubbard T, Reymond A, Antonarakis S E, Hannon G, Giddings M C, Ruan Y, Wold B, Carninci P, Guigó R, Gingeras T R (2012). Landscape of transcription in human cells. Nature, 489(7414): 101–108
|
| 32 |
Dong S, Cheng Y, Yang J, Li J, Liu X, Wang X, Wang D, Krall T J, Delphin E S, Zhang C (2009). MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem, 284(43): 29514–29525
|
| 33 |
Dubois N C, Craft A M, Sharma P, Elliott D A, Stanley E G, Elefanty A G, Gramolini A, Keller G (2011). SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat Biotechnol, 29(11): 1011–1018
|
| 34 |
ENCODE Project Consortium (2012). An integrated encyclopedia of DNA elements in the human genome. Nature, 489(7414): 57–74
|
| 35 |
Fan D, Takawale A, Lee J, Kassiri Z (2012). Cardiac fibroblasts, fibrosis and extracellular matrix remodeling in heart disease. Fibrogenesis Tissue Repair, 5(1): 15
|
| 36 |
Felician G, Collesi C, Lusic M, Martinelli V, Ferro M D, Zentilin L, Zacchigna S, Giacca M (2014). Epigenetic modification at Notch responsive promoters blunts efficacy of inducing notch pathway reactivation after myocardial infarction. Circ Res, 115(7): 636–649
|
| 37 |
Feng Y, Wang J, Asher S, Hoang L, Guardiani C, Ivanov I, Zheng Y G (2011). Histone H4 acetylation differentially modulates arginine methylation by an in Cis mechanism. J Biol Chem, 286(23): 20323–20334
|
| 38 |
Ferrara N, Komici K, Corbi G, Pagano G, Furgi G, Rengo C, Femminella G D, Leosco D, Bonaduce D (2014). β-adrenergic receptor responsiveness in aging heart and clinical implications. Front Physiol, 4: 396
|
| 39 |
Fisher C L, Fisher A G (2011). Chromatin states in pluripotent, differentiated, and reprogrammed cells. Curr Opin Genet Dev, 21(2): 140–146
|
| 40 |
Fu J D, Rushing S N, Lieu D K, Chan C W, Kong C W, Geng L, Wilson K D, Chiamvimonvat N, Boheler K R, Wu J C, Keller G, Hajjar R J, Li R A (2011). Distinct roles of microRNA-1 and-499 in ventricular specification and functional maturation of human embryonic stem cell-derived cardiomyocytes. PLoS One, 6(11): e27417
|
| 41 |
Fukushige S, Kondo E, Horii A (2008). Methyl-CpG targeted transcriptional activation allows re-expression of tumor suppressor genes in human cancer cells. Biochem Biophys Res Commun, 377(2): 600–605
|
| 42 |
Gadue P, Huber T L, Paddison P J, Keller G M (2006). Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci U S A, 103(45): 16806–16811
|
| 43 |
Gafni O, Weinberger L, Mansour A A, Manor Y S, Chomsky E, Ben-Yosef D, Kalma Y, Viukov S, Maza I, Zviran A, Rais Y, Shipony Z, Mukamel Z, Krupalnik V, Zerbib M, Geula S, Caspi I, Schneir D, Shwartz T, Gilad S, Amann-Zalcenstein D, Benjamin S, Amit I, Tanay A, Massarwa R, Novershtern N, Hanna J H (2013). Derivation of novel human ground state naive pluripotent stem cells. Nature, 504(7479): 282–286
|
| 44 |
Gepstein L, Ding C, Rahmutula D, Wilson E E, Yankelson L, Caspi O, Gepstein A, Huber I, Olgin J E (2010). In vivo assessment of the electrophysiological integration and arrhythmogenic risk of myocardial cell transplantation strategies. Stem Cells, 28(12): 2151–2161
|
| 45 |
Gopalakrishnan S, Van Emburgh B O, Robertson K D (2008). DNA methylation in development and human disease. Mutat Res, 647(1-2): 30–38
|
| 46 |
Graichen R, Xu X, Braam S R, Balakrishnan T, Norfiza S, Sieh S, Soo S Y, Tham S C, Mummery C, Colman A, Zweigerdt R, Davidson B P (2008). Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK. Differentiation, 76(4): 357–370
|
| 47 |
Grote P, Herrmann B G (2013). The long non-coding RNA Fendrr links epigenetic control mechanisms to gene regulatory networks in mammalian embryogenesis. RNA Biol, 10(10): 1579–1585
|
| 48 |
Grote P, Wittler L, Hendrix D, Koch F, Währisch S, Beisaw A, Macura K, Bläss G, Kellis M, Werber M, Herrmann B G (2013). The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell, 24(2): 206–214
|
| 49 |
Gu Y, Liu G H, Plongthongkum N, Benner C, Yi F, Qu J, Suzuki K, Yang J, Zhang W, Li M, Montserrat N, Crespo I, Del Sol A, Esteban C R, Zhang K, Izpisua Belmonte J C (2014). Global DNA methylation and transcriptional analyses of human ESC-derived cardiomyocytes. Protein Cell, 5(1): 59–68
|
| 50 |
Guo J U, Su Y, Shin J H, Shin J, Li H, Xie B, Zhong C, Hu S, Le T, Fan G, Zhu H, Chang Q, Gao Y, Ming G L, Song H (2014). Distribution, recognition and regulation of non-CpG methylation in the adult mammalian brain. Nat Neurosci, 17(2): 215–222
|
| 51 |
Gupta M K, Rao T N (2014). Hearty miR-363 controls HAND1 in cardiac cell specification. Stem Cell Res Ther, 5(4): 89
|
| 52 |
Haas J, Frese K S, Park Y J, Keller A, Vogel B, Lindroth A M, Weichenhan D, Franke J, Fischer S, Bauer A, Marquart S, Sedaghat-Hamedani F, Kayvanpour E, Köhler D, Wolf N M, Hassel S, Nietsch R, Wieland T, Ehlermann P, Schultz J H, Dösch A, Mereles D, Hardt S, Backs J, Hoheisel J D, Plass C, Katus H A, Meder B (2013). Alterations in cardiac DNA methylation in human dilated cardiomyopathy. EMBO Mol Med, 5(3): 413–429
|
| 53 |
Haase A, Olmer R, Schwanke K, Wunderlich S, Merkert S, Hess C, Zweigerdt R, Gruh I, Meyer J, Wagner S, Maier L S, Han D W, Glage S, Miller K, Fischer P, Schöler H R, Martin U (2009). Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell, 5(4): 434–441
|
| 54 |
Halbach M, Pfannkuche K, Pillekamp F, Ziomka A, Hannes T, Reppel M, Hescheler J, Müller-Ehmsen J (2007). Electrophysiological maturation and integration of murine fetal cardiomyocytes after transplantation. Circ Res, 101(5): 484–492
|
| 55 |
Han P, Li W, Lin C H, Yang J, Shang C, Nurnberg S T, Jin K K, Xu W, Lin C Y, Lin C J, Xiong Y, Chien H C, Zhou B, Ashley E, Bernstein D, Chen P S, Chen H S, Quertermous T, Chang C P (2014). A long noncoding RNA protects the heart from pathological hypertrophy. Nature, 514(7520): 102–106
|
| 56 |
Handy D E, Castro R, Loscalzo J (2011). Epigenetic modifications: basic mechanisms and role in cardiovascular disease. Circulation, 123(19): 2145–2156
|
| 57 |
Hang C T, Yang J, Han P, Cheng H L, Shang C, Ashley E, Zhou B, Chang C P (2010). Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature, 466(7302): 62–67
|
| 58 |
Hanna J, Cheng A W, Saha K, Kim J, Lengner C J, Soldner F, Cassady J P, Muffat J, Carey B W, Jaenisch R (2010). Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci U S A, 107(20): 9222–9227
|
| 59 |
Hansen T B, Jensen T I, Clausen B H, Bramsen J B, Finsen B, Damgaard C K, Kjems J (2013). Natural RNA circles function as efficient microRNA sponges. Nature, 495(7441): 384–388
|
| 60 |
Hattori F, Chen H, Yamashita H, Tohyama S, Satoh Y S, Yuasa S, Li W, Yamakawa H, Tanaka T, Onitsuka T, Shimoji K, Ohno Y, Egashira T, Kaneda R, Murata M, Hidaka K, Morisaki T, Sasaki E, Suzuki T, Sano M, Makino S, Oikawa S, Fukuda K (2010). Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat Methods, 7(1): 61–66
|
| 61 |
Henning R J (2011). Stem cells in cardiac repair. Future Cardiol, 7(1): 99–117
|
| 62 |
Hirt M N, Boeddinghaus J, Mitchell A, Schaaf S, Börnchen C, Müller C, Schulz H, Hubner N, Stenzig J, Stoehr A, Neuber C, Eder A, Luther P K, Hansen A, Eschenhagen T (2014). Functional improvement and maturation of rat and human engineered heart tissue by chronic electrical stimulation. J Mol Cell Cardiol, 74: 151–161
|
| 63 |
Ho L, Crabtree G R (2010). Chromatin remodelling during development. Nature, 463(7280): 474–484
|
| 64 |
Hoekstra M, van der Lans C A, Halvorsen B, Gullestad L, Kuiper J, Aukrust P, van Berkel T J C, Biessen E A L (2010). The peripheral blood mononuclear cell microRNA signature of coronary artery disease. Biochem Biophys Res Commun, 394(3): 792–797
|
| 65 |
Horrillo A, Pezzolla D, Fraga M F, Aguilera Y, Salguero-Aranda C, Tejedo J R, Martin F, Bedoya F J, Soria B, Hmadcha A (2013). Zebularine regulates early stages of mESC differentiation: effect on cardiac commitment. Cell Death Dis, 4(4): e570
|
| 66 |
Horton R E, Millman J R, Colton C K, Auguste D T (2009). Engineering microenvironments for embryonic stem cell differentiation to cardiomyocytes. Regen Med, 4(5): 721–732
|
| 67 |
Hough S R, Laslett A L, Grimmond S B, Kolle G, Pera M F (2009). A continuum of cell states spans pluripotency and lineage commitment in human embryonic stem cells. PLoS One, 4(11): e7708
|
| 68 |
Huang V, Li L C (2012). miRNA goes nuclear. RNA Biol, 9(3): 269–273
|
| 69 |
Huang Z P, Chen J, Seok H Y, Zhang Z, Kataoka M, Hu X, Wang D Z (2013). MicroRNA-22 regulates cardiac hypertrophy and remodeling in response to stress. Circ Res, 112(9): 1234–1243
|
| 70 |
Ikeda S, Kong S W, Lu J, Bisping E, Zhang H, Allen P D, Golub T R, Pieske B, Pu W T (2007). Altered microRNA expression in human heart disease. Physiol Genomics, 31(3): 367–373
|
| 71 |
Ishii N, Ozaki K, Sato H, Mizuno H, Saito S, Takahashi A, Miyamoto Y, Ikegawa S, Kamatani N, Hori M, Saito S, Nakamura Y, Tanaka T (2006). Identification of a novel non-coding RNA, MIAT, that confers risk of myocardial infarction. J Hum Genet, 51(12): 1087–1099
|
| 72 |
Jaguszewski M, Osipova J, Ghadri J R, Napp L C, Widera C, Franke J, Fijalkowski M, Nowak R, Fijalkowska M, Volkmann I, Katus H A, Wollert K C, Bauersachs J, Erne P, Lüscher T F, Thum T, Templin C (2014). A signature of circulating microRNAs differentiates takotsubo cardiomyopathy from acute myocardial infarction. Eur Heart J, 35(15): 999–1006
|
| 73 |
Jenuwein T, Allis C D (2001). Translating the histone code. Science, 293(5532): 1074–1080
|
| 74 |
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna J A, Charpentier E (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337(6096): 816–821
|
| 75 |
Karamboulas C, Swedani A, Ward C, Al-Madhoun A S, Wilton S, Boisvenue S, Ridgeway A G, Skerjanc I S (2006). HDAC activity regulates entry of mesoderm cells into the cardiac muscle lineage. J Cell Sci, 119(Pt 20): 4305–4314
|
| 76 |
Kattman S J, Witty A D, Gagliardi M, Dubois N C, Niapour M, Hotta A, Ellis J, Keller G (2011). Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell, 8(2): 228–240
|
| 77 |
Kavi H H, Birchler J A (2009). Interaction of RNA polymerase II and the small RNA machinery affects heterochromatic silencing in Drosophila. Epigenetics Chromatin, 2(1): 15
|
| 78 |
Kawamura T, Ono K, Morimoto T, Wada H, Hirai M, Hidaka K, Morisaki T, Heike T, Nakahata T, Kita T, Hasegawa K (2005). Acetylation of GATA-4 is involved in the differentiation of embryonic stem cells into cardiac myocytes. J Biol Chem, 280(20): 19682–19688
|
| 79 |
Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A, Livne E, Binah O, Itskovitz-Eldor J, Gepstein L (2001). Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest, 108(3): 407–414
|
| 80 |
Kehat I, Molkentin J D (2010). Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation, 122(25): 2727–2735
|
| 81 |
Kim D H, Saetrom P, Snøve O Jr, Rossi J J (2008). MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci U S A, 105(42): 16230–16235
|
| 82 |
Kim D H, Villeneuve L M, Morris K V, Rossi J J (2006). Argonaute-1 directs siRNA-mediated transcriptional gene silencing in human cells. Nat Struct Mol Biol, 13(9): 793–797
|
| 83 |
Kim J K, Samaranayake M, Pradhan S (2009). Epigenetic mechanisms in mammals. Cell Mol Life Sci, 66(4): 596–612
|
| 84 |
Kim K, Doi A, Wen B, Ng K, Zhao R, Cahan P, Kim J, Aryee M J, Ji H, Ehrlich L I R, Yabuuchi A, Takeuchi A, Cunniff K C, Hongguang H, McKinney-Freeman S, Naveiras O, Yoon T J, Irizarry R A, Jung N, Seita J, Hanna J, Murakami P, Jaenisch R, Weissleder R, Orkin S H, Weissman I L, Feinberg A P, Daley G Q (2010). Epigenetic memory in induced pluripotent stem cells. Nature, 467(7313): 285–290
|
| 85 |
Klattenhoff C A, Scheuermann J C, Surface L E, Bradley R K, Fields P A, Steinhauser M L, Ding H, Butty V L, Torrey L, Haas S, Abo R, Tabebordbar M, Lee R T, Burge C B, Boyer L A (2013). Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell, 152(3): 570–583
|
| 86 |
Kohli R M, Zhang Y (2013). TET enzymes, TDG and the dynamics of DNA demethylation. Nature, 502(7472): 472–479
|
| 87 |
Koitabashi N, Kass D A (2012). Reverse remodeling in heart failure—mechanisms and therapeutic opportunities. Nat Rev Cardiol, 9(3): 147–157
|
| 88 |
Kolossov E, Lu Z, Drobinskaya I, Gassanov N, Duan Y, Sauer H, Manzke O, Bloch W, Bohlen H, Hescheler J, Fleischmann B K (2005). Identification and characterization of embryonic stem cell-derived pacemaker and atrial cardiomyocytes. FASEB J, 19(6): 577–579
|
| 89 |
Krenning G, Zeisberg E M, Kalluri R (2010). The origin of fibroblasts and mechanism of cardiac fibrosis. J Cell Physiol, 225(3): 631–637
|
| 90 |
Kreutziger K L, Muskheli V, Johnson P, Braun K, Wight T N, Murry C E (2011). Developing vasculature and stroma in engineered human myocardium. Tissue Eng Part A, 17(9-10): 1219–1228
|
| 91 |
Kumarswamy R, Bauters C, Volkmann I, Maury F, Fetisch J, Holzmann A, Lemesle G, de Groote P, Pinet F, Thum T (2014). Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure. Circ Res, 114(10): 1569–1575
|
| 92 |
Laflamme M A, Chen K Y, Naumova A V, Muskheli V, Fugate J A, Dupras S K, Reinecke H, Xu C, Hassanipour M, Police S, O’Sullivan C, Collins L, Chen Y, Minami E, Gill E A, Ueno S, Yuan C, Gold J, Murry C E (2007). Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol, 25(9): 1015–1024
|
| 93 |
Laflamme M A, Gold J, Xu C, Hassanipour M, Rosler E, Police S, Muskheli V, Murry C E (2005). Formation of human myocardium in the rat heart from human embryonic stem cells. Am J Pathol, 167(3): 663–671
|
| 94 |
Laflamme M A, Murry C E (2005). Regenerating the heart. Nat Biotechnol, 23(7): 845–856
|
| 95 |
Laflamme M A, Murry C E (2011). Heart regeneration. Nature, 473(7347): 326–335
|
| 96 |
Laurent L, Wong E, Li G, Huynh T, Tsirigos A, Ong C T, Low H M, Kin Sung K W, Rigoutsos I, Loring J, Wei C L (2010). Dynamic changes in the human methylome during differentiation. Genome Res, 20(3): 320–331
|
| 97 |
Leri A, Kajstura J, Anversa P (2011). Role of cardiac stem cells in cardiac pathophysiology: a paradigm shift in human myocardial biology. Circ Res, 109(8): 941–961
|
| 98 |
Lesman A, Habib M, Caspi O, Gepstein A, Arbel G, Levenberg S, Gepstein L (2010). Transplantation of a tissue-engineered human vascularized cardiac muscle. Tissue Eng Part A, 16(1): 115–125
|
| 99 |
Li X, Wang J, Jia Z, Cui Q, Zhang C, Wang W, Chen P, Ma K, Zhou C (2013). MiR-499 regulates cell proliferation and apoptosis during late-stage cardiac differentiation via Sox6 and cyclin D1. PLoS One, 8(9): e74504
|
| 100 |
Lian X, Zhang J, Azarin S M, Zhu K, Hazeltine L B, Bao X, Hsiao C, Kamp T J, Palecek S P (2013). Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat Protoc, 8(1): 162–175
|
| 101 |
Lin Z, Pu WT (2014). Strategies for cardiac regeneration and repair. Sci Transl Med, 6: 239rv231
|
| 102 |
Lindsley R C, Gill J G, Kyba M, Murphy T L, Murphy K M (2006). Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development, 133(19): 3787–3796
|
| 103 |
Lu T Y, Lin B, Kim J, Sullivan M, Tobita K, Salama G, Yang L (2013). Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells. Nat Commun, 4: 2307
|
| 104 |
Luco R F, Allo M, Schor I E, Kornblihtt A R, Misteli T (2011). Epigenetics in alternative pre-mRNA splicing. Cell, 144(1): 16–26
|
| 105 |
Luger K, Mäder A W, Richmond R K, Sargent D F, Richmond T J (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389(6648): 251–260
|
| 106 |
Majumdar G, Johnson I M, Kale S, Raghow R (2008). Epigenetic regulation of cardiac muscle-specific genes in H9c2 cells by Interleukin-18 and histone deacetylase inhibitor m-carboxycinnamic acid bis-hydroxamide. Mol Cell Biochem, 312(1-2): 47–60
|
| 107 |
Marks H, Kalkan T, Menafra R, Denissov S, Jones K, Hofemeister H, Nichols J, Kranz A, Stewart A F, Smith A, Stunnenberg H G (2012). The transcriptional and epigenomic foundations of ground state pluripotency. Cell, 149(3): 590–604
|
| 108 |
Matkovich S J, Edwards J R, Grossenheider T C, de Guzman Strong C, Dorn G W 2nd (2014). Epigenetic coordination of embryonic heart transcription by dynamically regulated long noncoding RNAs. Proc Natl Acad Sci U S A, 111(33): 12264–12269
|
| 109 |
Nature Methods editorial (2012). Method of the Year 2011. Nat Methods, 9(1): 1
|
| 110 |
Miyamoto S, Kawamura T, Morimoto T, Ono K, Wada H, Kawase Y, Matsumori A, Nishio R, Kita T, Hasegawa K (2006). Histone acetyltransferase activity of p300 is required for the promotion of left ventricular remodeling after myocardial infarction in adult mice in vivo. Circulation, 113(5): 679–690
|
| 111 |
Movassagh M, Choy M K, Goddard M, Bennett M R, Down T A, Foo R S (2010). Differential DNA methylation correlates with differential expression of angiogenic factors in human heart failure. PLoS One, 5(1): e8564
|
| 112 |
Movassagh M, Choy M K, Knowles D A, Cordeddu L, Haider S, Down T, Siggens L, Vujic A, Simeoni I, Penkett C, Goddard M, Lio P, Bennett M R, Foo R S Y (2011). Distinct epigenomic features in end-stage failing human hearts. Circulation, 124(22): 2411–2422
|
| 113 |
Mujtaba S, Zeng L, Zhou M M (2007). Structure and acetyl-lysine recognition of the bromodomain. Oncogene, 26(37): 5521–5527
|
| 114 |
Mummery C, Ward-van Oostwaard D, Doevendans P, Spijker R, van den Brink S, Hassink R, van der Heyden M, Opthof T, Pera M, de la Riviere A B, Passier R, Tertoolen L (2003). Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation, 107(21): 2733–2740
|
| 115 |
Naito A T, Shiojima I, Akazawa H, Hidaka K, Morisaki T, Kikuchi A, Komuro I (2006). Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc Natl Acad Sci U S A, 103(52): 19812–19817
|
| 116 |
Narazaki G, Uosaki H, Teranishi M, Okita K, Kim B, Matsuoka S, Yamanaka S, Yamashita J K (2008). Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation, 118(5): 498–506
|
| 117 |
Ng S Y, Wong C K, Tsang S Y (2010). Differential gene expressions in atrial and ventricular myocytes: insights into the road of applying embryonic stem cell-derived cardiomyocytes for future therapies. Am J Physiol Cell Physiol, 299(6): C1234–C1249
|
| 118 |
Nie L, Wu H J, Hsu J M, Chang S S, Labaff A M, Li C W, Wang Y, Hsu J L, Hung M C (2012). Long non-coding RNAs: versatile master regulators of gene expression and crucial players in cancer. Am J Transl Res, 4(2): 127–150
|
| 119 |
Nissim L, Perli S D, Fridkin A, Perez-Pinera P, Lu T K (2014). Multiplexed and programmable regulation of gene networks with an integrated RNA and CRISPR/Cas toolkit in human cells. Mol Cell, 54(4): 698–710
|
| 120 |
Nunes S S, Miklas J W, Liu J, Aschar-Sobbi R, Xiao Y, Zhang B, Jiang J, Massé S, Gagliardi M, Hsieh A, Thavandiran N, Laflamme M A, Nanthakumar K, Gross G J, Backx P H, Keller G, Radisic M (2013). Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat Methods, 10(8): 781–787
|
| 121 |
Nussbaum J, Minami E, Laflamme M A, Virag J A, Ware C B, Masino A, Muskheli V, Pabon L, Reinecke H, Murry C E (2007). Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. FASEB J, 21(7): 1345–1357
|
| 122 |
Osafune K, Caron L, Borowiak M, Martinez R J, Fitz-Gerald C S, Sato Y, Cowan C A, Chien K R, Melton D A (2008). Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol, 26(3): 313–315
|
| 123 |
Paige S L, Thomas S, Stoick-Cooper C L, Wang H, Maves L, Sandstrom R, Pabon L, Reinecke H, Pratt G, Keller G, Moon R T, Stamatoyannopoulos J, Murry C E (2012). A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development. Cell, 151(1): 221–232
|
| 124 |
Papait R, Condorelli G (2010). Epigenetics in heart failure. Ann N Y Acad Sci, 1188(1): 159–164
|
| 125 |
Papait R, Kunderfranco P, Stirparo G G, Latronico M V, Condorelli G (2013). Long noncoding RNA: a new player of heart failure? J Cardiovasc Transl Res, 6(6): 876–883
|
| 126 |
Pascut F C, Goh H T, George V, Denning C, Notingher I (2011). Toward label-free Raman-activated cell sorting of cardiomyocytes derived from human embryonic stem cells. J Biomed Opt, 16(4): 045002
|
| 127 |
Passier R, van Laake L W, Mummery C L (2008). Stem-cell-based therapy and lessons from the heart. Nature, 453(7193): 322–329
|
| 128 |
Porrello E R, Mahmoud A I, Simpson E, Hill J A, Richardson J A, Olson E N, Sadek H A (2011). Transient regenerative potential of the neonatal mouse heart. Science, 331(6020): 1078–1080
|
| 129 |
Radisic M, Christman K L (2013). Materials science and tissue engineering: repairing the heart. Mayo Clin Proc, 88(8): 884–898
|
| 130 |
Rai M, Walthall J M, Hu J, Hatzopoulos A K (2012). Continuous antagonism by Dkk1 counter activates canonical Wnt signaling and promotes cardiomyocyte differentiation of embryonic stem cells. Stem Cells Dev, 21(1): 54–66
|
| 131 |
Rajala K, Pekkanen-Mattila M, Aalto-Setälä K (2011). Cardiac differentiation of pluripotent stem cells. Stem Cells Int, 2011: 383709
|
| 132 |
Reinecke H, Zhang M, Bartosek T, Murry C E (1999). Survival, integration, and differentiation of cardiomyocyte grafts: a study in normal and injured rat hearts. Circulation, 100(2): 193–202
|
| 133 |
Reisman D, Glaros S, Thompson E A (2009). The SWI/SNF complex and cancer. Oncogene, 28(14): 1653–1668
|
| 134 |
Reynolds N, Salmon-Divon M, Dvinge H, Hynes-Allen A, Balasooriya G, Leaford D, Behrens A, Bertone P, Hendrich B (2012). NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb Repressive Complex 2 to direct gene repression. EMBO J, 31(3): 593–605
|
| 135 |
Rizzi R, Di Pasquale E, Portararo P, Papait R, Cattaneo P, Latronico M V, Altomare C, Sala L, Zaza A, Hirsch E, Naldini L, Condorelli G, Bearzi C (2012). Post-natal cardiomyocytes can generate iPS cells with an enhanced capacity toward cardiomyogenic re-differentation. Cell Death Differ, 19(7): 1162–1174
|
| 136 |
Robertson K D (2005). DNA methylation and human disease. Nat Rev Genet, 6(8): 597–610
|
| 137 |
Robey T E, Saiget M K, Reinecke H, Murry C E (2008). Systems approaches to preventing transplanted cell death in cardiac repair. J Mol Cell Cardiol, 45(4): 567–581
|
| 138 |
Rubart M, Pasumarthi K B, Nakajima H, Soonpaa M H, Nakajima H O, Field L J (2003). Physiological coupling of donor and host cardiomyocytes after cellular transplantation. Circ Res, 92(11): 1217–1224
|
| 139 |
Salmanidis M, Pillman K, Goodall G, Bracken C (2014). Direct transcriptional regulation by nuclear microRNAs. Int J Biochem Cell Biol, 54: 304–311
|
| 140 |
Sanchez-Freire V, Lee A S, Hu S, Abilez O J, Liang P, Lan F, Huber B C, Ong S G, Hong W X, Huang M, Wu J C (2014). Effect of human donor cell source on differentiation and function of cardiac induced pluripotent stem cells. J Am Coll Cardiol, 64(5): 436–448
|
| 141 |
Santillan D A, Theisler C M, Ryan A S, Popovic R, Stuart T, Zhou M M, Alkan S, Zeleznik-Le N J (2006). Bromodomain and histone acetyltransferase domain specificities control mixed lineage leukemia phenotype. Cancer Res, 66(20): 10032–10039
|
| 142 |
Santos-Rosa H, Schneider R, Bannister A J, Sherriff J, Bernstein B E, Emre N C, Schreiber S L, Mellor J, Kouzarides T (2002). Active genes are tri-methylated at K4 of histone H3. Nature, 419(6905): 407–411
|
| 143 |
Sarma K, Margueron R, Ivanov A, Pirrotta V, Reinberg D (2008). Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol Cell Biol, 28(8): 2718–2731
|
| 144 |
Sartiani L, Bettiol E, Stillitano F, Mugelli A, Cerbai E, Jaconi M E (2007). Developmental changes in cardiomyocytes differentiated from human embryonic stem cells: a molecular and electrophysiological approach. Stem Cells, 25(5): 1136–1144
|
| 145 |
Segers V F, Lee R T (2008). Stem-cell therapy for cardiac disease. Nature, 451(7181): 937–942
|
| 146 |
Senyo S E, Steinhauser M L, Pizzimenti C L, Yang V K, Cai L, Wang M, Wu T D, Guerquin-Kern J L, Lechene C P, Lee R T (2013). Mammalian heart renewal by pre-existing cardiomyocytes. Nature, 493(7432): 433–436
|
| 147 |
Sera T (2009). Zinc-finger-based artificial transcription factors and their applications. Adv Drug Deliv Rev, 61(7-8): 513–526
|
| 148 |
Shiba Y, Fernandes S, Zhu W Z, Filice D, Muskheli V, Kim J, Palpant N J, Gantz J, Moyes K W, Reinecke H, Van Biber B, Dardas T, Mignone J L, Izawa A, Hanna R, Viswanathan M, Gold J D, Kotlikoff M I, Sarvazyan N, Kay M W, Murry C E, Laflamme M A (2012). Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature, 489(7415): 322–325
|
| 149 |
Shiba Y, Hauch K D, Laflamme M A (2009). Cardiac applications for human pluripotent stem cells. Curr Pharm Des, 15(24): 2791–2806
|
| 150 |
Shilatifard A (2006). Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem, 75(1): 243–269
|
| 151 |
Snir M, Kehat I, Gepstein A, Coleman R, Itskovitz-Eldor J, Livne E, Gepstein L (2003). Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes. Am J Physiol Heart Circ Physiol, 285(6): H2355–H2363
|
| 152 |
Sondermeijer B M, Bakker A, Halliani A, de Ronde M W, Marquart A A, Tijsen A J, Mulders T A, Kok M G M, Battjes S, Maiwald S, Sivapalaratnam S, Trip M D, Moerland P D, Meijers J C M, Creemers E E, Pinto-Sietsma S J (2011). Platelets in patients with premature coronary artery disease exhibit upregulation of miRNA340* and miRNA624*. PLoS One, 6(10): e25946
|
| 153 |
Stein A B, Jones T A, Herron T J, Patel S R, Day S M, Noujaim S F, Milstein M L, Klos M, Furspan P B, Jalife J, Dressler G R (2011). Loss of H3K4 methylation destabilizes gene expression patterns and physiological functions in adult murine cardiomyocytes. J Clin Invest, 121(7): 2641–2650
|
| 154 |
Stevens K R, Kreutziger K L, Dupras S K, Korte F S, Regnier M, Muskheli V, Nourse M B, Bendixen K, Reinecke H, Murry C E (2009). Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc Natl Acad Sci U S A, 106(39): 16568–16573
|
| 155 |
Stroud H, Feng S, Morey Kinney S, Pradhan S, Jacobsen S E (2011). 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells. Genome Biol, 12(6): R54
|
| 156 |
Sucharov C, Bristow M R, Port J D (2008). miRNA expression in the failing human heart: functional correlates. J Mol Cell Cardiol, 45(2): 185–192
|
| 157 |
Sullivan G J, Bai Y, Fletcher J, Wilmut I (2010). Induced pluripotent stem cells: epigenetic memories and practical implications. Mol Hum Reprod, 16(12): 880–885
|
| 158 |
Takaya T, Ono K, Kawamura T, Takanabe R, Kaichi S, Morimoto T, Wada H, Kita T, Shimatsu A, Hasegawa K (2009). MicroRNA-1 and MicroRNA-133 in spontaneous myocardial differentiation of mouse embryonic stem cells. Circ J, 73(8): 1492–1497
|
| 159 |
Tanasijevic B, Dai B, Ezashi T, Livingston K, Roberts R M, Rasmussen T P (2009). Progressive accumulation of epigenetic heterogeneity during human ES cell culture. Epigenetics, 4(5): 330–338
|
| 160 |
Tohyama S, Hattori F, Sano M, Hishiki T, Nagahata Y, Matsuura T, Hashimoto H, Suzuki T, Yamashita H, Satoh Y, Egashira T, Seki T, Muraoka N, Yamakawa H, Ohgino Y, Tanaka T, Yoichi M, Yuasa S, Murata M, Suematsu M, Fukuda K (2013). Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell, 12(1): 127–137
|
| 161 |
Tompkins J D, Hall C, Chen V C, Li A X, Wu X, Hsu D, Couture L A, Riggs A D (2012). Epigenetic stability, adaptability, and reversibility in human embryonic stem cells. Proc Natl Acad Sci U S A, 109(31): 12544–12549
|
| 162 |
Trivedi C M, Luo Y, Yin Z, Zhang M, Zhu W, Wang T, Floss T, Goettlicher M, Noppinger P R, Wurst W, Ferrari V A, Abrams C S, Gruber P J, Epstein J A (2007). Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity. Nat Med, 13(3): 324–331
|
| 163 |
Tsai M C, Manor O, Wan Y, Mosammaparast N, Wang J K, Lan F, Shi Y, Segal E, Chang H Y (2010). Long noncoding RNA as modular scaffold of histone modification complexes. Science, 329(5992): 689–693
|
| 164 |
Tulloch N L, Muskheli V, Razumova M V, Korte F S, Regnier M, Hauch K D, Pabon L, Reinecke H, Murry C E (2011). Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res, 109(1): 47–59
|
| 165 |
Ueno S, Weidinger G, Osugi T, Kohn A D, Golob J L, Pabon L, Reinecke H, Moon R T, Murry C E (2007). Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc Natl Acad Sci U S A, 104(23): 9685–9690
|
| 166 |
Uosaki H, Fukushima H, Takeuchi A, Matsuoka S, Nakatsuji N, Yamanaka S, Yamashita J K (2011). Efficient and scalable purification of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression. PLoS One, 6(8): e23657
|
| 167 |
Van Hoof D, Dormeyer W, Braam S R, Passier R, Monshouwer-Kloots J, Ward-van Oostwaard D, Heck A J R, Krijgsveld J, Mummery C L (2010). Identification of cell surface proteins for antibody-based selection of human embryonic stem cell-derived cardiomyocytes. J Proteome Res, 9(3): 1610–1618
|
| 168 |
van Rooij E, Sutherland L B, Liu N, Williams A H, McAnally J, Gerard R D, Richardson J A, Olson E N (2006). A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci U S A, 103(48): 18255–18260
|
| 169 |
Verheugt C L, Uiterwaal C S, van der Velde E T, Meijboom F J, Pieper P G, van Dijk A P, Vliegen H W, Grobbee D E, Mulder B J M (2010). Mortality in adult congenital heart disease. Eur Heart J, 31(10): 1220–1229
|
| 170 |
Voigt P, LeRoy G, Drury W J 3rd, Zee B M, Son J, Beck D B, Young N L, Garcia B A, Reinberg D (2012). Asymmetrically modified nucleosomes. Cell, 151(1): 181–193
|
| 171 |
Wamstad J A, Alexander J M, Truty R M, Shrikumar A, Li F, Eilertson K E, Ding H, Wylie J N, Pico A R, Capra J A, Erwin G, Kattman S J, Keller G M, Srivastava D, Levine S S, Pollard K S, Holloway A K, Boyer L A, Bruneau B G (2012). Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell, 151(1): 206–220
|
| 172 |
Wang G K, Zhu J Q, Zhang J T, Li Q, Li Y, He J, Qin Y W, Jing Q (2010). Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J, 31(6): 659–666
|
| 173 |
Xu C, Police S, Rao N, Carpenter M K (2002). Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res, 91(6): 501–508
|
| 174 |
Xu H, Yi B A, Wu H, Bock C, Gu H, Lui K O, Park J H C, Shao Y, Riley A K, Domian I J, Hu E, Willette R, Lepore J, Meissner A, Wang Z, Chien K R (2012). Highly efficient derivation of ventricular cardiomyocytes from induced pluripotent stem cells with a distinct epigenetic signature. Cell Res, 22(1): 142–154
|
| 175 |
Xue T, Cho H C, Akar F G, Tsang S Y, Jones S P, Marbán E, Tomaselli G F, Li R A (2005). Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: insights into the development of cell-based pacemakers. Circulation, 111(1): 11–20
|
| 176 |
Yang L, Soonpaa M H, Adler E D, Roepke T K, Kattman S J, Kennedy M, Henckaerts E, Bonham K, Abbott G W, Linden R M, Field L J, Keller G M (2008). Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature, 453(7194): 524–528
|
| 177 |
Yang Y W, Flynn R A, Chen Y, Qu K, Wan B, Wang K C, Lei M, Chang H Y (2014). Essential role of lncRNA binding for WDR5 maintenance of active chromatin and embryonic stem cell pluripotency. Elife, 3: e02046
|
| 178 |
Yao C X, Wei Q X, Zhang Y Y, Wang W P, Xue L X, Yang F, Zhang S F, Xiong C J, Li W Y, Wei Z R, Zou Y, Zang M X (2013). miR-200b targets GATA-4 during cell growth and differentiation. RNA Biol, 10(4): 465–480
|
| 179 |
Yi F F, Yang L, Li Y H, Su P X, Cai J, Yang X C (2009). Electrophysiological development of transplanted embryonic stem cell-derived cardiomyocytes in the hearts of syngeneic mice. Arch Med Res, 40(5): 339–344
|
| 180 |
Yoon B S, Yoo S J, Lee J E, You S, Lee H T, Yoon H S (2006). Enhanced differentiation of human embryonic stem cells into cardiomyocytes by combining hanging drop culture and 5-azacytidine treatment. Differentiation, 74(4): 149–159
|
| 181 |
Zaratiegui M, Irvine D V, Martienssen R A (2007). Noncoding RNAs and gene silencing. Cell, 128(4): 763–776
|
| 182 |
Zhang C L, McKinsey T A, Chang S, Antos C L, Hill J A, Olson E N (2002a). Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell, 110(4): 479–488
|
| 183 |
Zhang J, Klos M, Wilson G F, Herman A M, Lian X, Raval K K, Barron M R, Hou L, Soerens A G, Yu J, Palecek S P, Lyons G E, Thomson J A, Herron T J, Jalife J, Kamp T J (2012a). Extracellular matrix promotes highly efficient cardiac differentiation of human pluripotent stem cells: the matrix sandwich method. Circ Res, 111(9): 1125–1136
|
| 184 |
Zhang L, Chen B, Zhao Y, Dubielecka P M, Wei L, Qin G J, Chin Y E, Wang Y, Zhao T C (2012b). Inhibition of histone deacetylase-induced myocardial repair is mediated by c-kit in infarcted hearts. J Biol Chem, 287(47): 39338–39348
|
| 185 |
Zhang L, Qin X, Zhao Y, Fast L, Zhuang S, Liu P, Cheng G, Zhao T C (2012c). Inhibition of histone deacetylases preserves myocardial performance and prevents cardiac remodeling through stimulation of endogenous angiomyogenesis. J Pharmacol Exp Ther, 341(1): 285–293
|
| 186 |
Zhang T, Kohlhaas M, Backs J, Mishra S, Phillips W, Dybkova N, Chang S, Ling H, Bers D M, Maier L S, Olson E N, Brown J H (2007). CaMKIIdelta isoforms differentially affect calcium handling but similarly regulate HDAC/MEF2 transcriptional responses. J Biol Chem, 282(48): 35078–35087
|
| 187 |
Zhang Y M, Hartzell C, Narlow M, Dudley S C Jr (2002). Stem cell-derived cardiomyocytes demonstrate arrhythmic potential. Circulation, 106(10): 1294–1299
|
| 188 |
Zhu S, Hu X, Han S, Yu Z, Peng Y, Zhu J, Liu X, Qian L, Zhu C, Li M, Song G, Guo X (2014). Differential expression profile of long non-coding RNAs during differentiation of cardiomyocytes. Int J Med Sci, 11(5): 500–507
|
| 189 |
Zwi-Dantsis L, Gepstein L (2012). Induced pluripotent stem cells for cardiac repair. Cell Mol Life Sci, 69(19): 3285–3299
|
/
| 〈 |
|
〉 |