Cardiac regeneration using human embryonic stem cells: producing cells for future therapy

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Bibliography

• 1  Lloyd-Jones D, Adams R, Carnethon M et al.: Heart disease and stroke statistics – 2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation119(3),480–486 (2009).
  MedlineGoogle Scholar
• 2  Chien KR, Domian IJ, Parker KK: Cardiogenesis and the complex biology of regenerative cardiovascular medicine. Science322(5907),1494–1497 (2008).
  Medline CASGoogle Scholar
• 3  Kehat I, Kenyagin-Karsenti D, Snir M et al.: Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J. Clin. Invest.108(3),407–414 (2001).▪ First comprehensive characterization of human embryonic stem cell (hESC)-derived cardiomyocytes (CMs).
  Medline CASGoogle Scholar
• 4  Xu C, Police S, Rao N, Carpenter MK: Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ. Res.91(6),501–508 (2002).
  Medline CASGoogle Scholar
• 5  Itskovitz-Eldor J, Schuldiner M, Karsenti D et al.: Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol. Med.6(2),88–95 (2000).
  Medline CASGoogle Scholar
• 6  He JQ, Ma Y, Lee Y, Thomson JA, Kamp TJ: Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ. Res.93(1),32–39 (2003).▪ First characterization of electrophysiological heterogeneity among cultures of hESC-derived CMs.
  Medline CASGoogle Scholar
• 7  Beltrami CA, Finato N, Rocco M et al.: Structural basis of end-stage failure in ischemic cardiomyopathy in humans. Circulation89(1),151–163 (1994).
  Medline CASGoogle Scholar
• 8  Fukuda K: Development of regenerative cardiomyocytes from mesenchymal stem cells for cardiovascular tissue engineering. Artif. Organs25(3),187–193 (2001).
  Medline CASGoogle Scholar
• 9  Graichen R, Xu X, Braam SR et al.: Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK. Differentiation76(4),357–370 (2008).
  Medline CASGoogle Scholar
• 10  Gaur M, Ritner C, Sievers RE et al.: Timed inhibition of p38MAPK directs accelerated differentiation of human embryonic stem cells into cardiomyocytes. Cytotherapy (2010) (Epub ahead of print).
  MedlineGoogle Scholar
• 11  Mummery CL, van Achterberg TA, van den Eijnden-van Raaij AJ et al.: Visceral-endoderm-like cell lines induce differentiation of murine P19 embryonal carcinoma cells. Differentiation46(1),51–60 (1991).
  Medline CASGoogle Scholar
• 12  Mummery C, Ward-van Oostwaard D, Doevendans P et al.: Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation107(21),2733–2740 (2003).
  Medline CASGoogle Scholar
• 13  Xu XQ, Graichen R, Soo SY et al.: Chemically defined medium supporting cardiomyocyte differentiation of human embryonic stem cells. Differentiation76(9),958–970 (2008).
  Medline CASGoogle Scholar
• 14  Mummery CL, Feijen A, Moolenaar WH, van den Brink CE, de Laat SW: Establishment of a differentiated mesodermal line from P19 EC cells expressing functional PDGF and EGF receptors. Exp. Cell Res.165(1),229–242 (1986).
  Medline CASGoogle Scholar
• 15  Laflamme MA, Chen KY, Naumova AV et al.: Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol.25(9),1015–1024 (2007).
  Medline CASGoogle Scholar
• 16  Sugi Y, Lough J: Activin-A and FGF-2 mimic the inductive effects of anterior endoderm on terminal cardiac myogenesis in vitro. Dev. Biol.168(2),567–574 (1995).
  Medline CASGoogle Scholar
• 17  Smith JC, Price BM, Van Nimmen K, Huylebroeck D: Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature345(6277),729–731 (1990).
  Medline CASGoogle Scholar
• 18  Nakajima Y, Yamagishi T, Ando K, Nakamura H: Significance of bone morphogenetic protein-4 function in the initial myofibrillogenesis of chick cardiogenesis. Dev. Biol.245(2),291–303 (2002).
  Medline CASGoogle Scholar
• 19  Lough J, Barron M, Brogley M, Sugi Y, Bolender DL, Zhu X: Combined BMP-2 and FGF-4, but neither factor alone, induces cardiogenesis in non-precardiac embryonic mesoderm. Dev. Biol.178(1),198–202 (1996).
  Medline CASGoogle Scholar
• 20  Ladd AN, Yatskievych TA, Antin PB: Regulation of avian cardiac myogenesis by activin/TGF-β and bone morphogenetic proteins. Dev. Biol.204(2),407–419 (1998).
  Medline CASGoogle Scholar
• 21  Barron M, Gao M, Lough J: Requirement for BMP and FGF signaling during cardiogenic induction in non-precardiac mesoderm is specific, transient, and cooperative. Dev. Dyn.218(2),383–393 (2000).
  Medline CASGoogle Scholar
• 22  Yao S, Chen S, Clark J et al.: Long-term self-renewal and directed differentiation of human embryonic stem cells in chemically defined conditions. Proc. Natl Acad. Sci. USA103(18),6907–6912 (2006).
  Medline CASGoogle Scholar
• 23  Yang L, Soonpaa MH, Adler ED et al.: Human cardiovascular progenitor cells develop from a KDR⁺ embryonic-stem-cell-derived population. Nature453(7194),524–528 (2008).▪ Identification of a human cardiac progenitor derived from hESCs.
  Medline CASGoogle Scholar
• 24  Schneider VA, Mercola M: Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev.15(3),304–315 (2001).
  Medline CASGoogle Scholar
• 25  Marvin MJ, Di Rocco G, Gardiner A, Bush SM, Lassar AB: Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes Dev.15(3),316–327 (2001).
  Medline CASGoogle Scholar
• 26  Sargent CY, Berguig GY, McDevitt TC: Cardiomyogenic differentiation of embryoid bodies is promoted by rotary orbital suspension culture. Tissue Eng. Part A15(2),331–342 (2009).
  Medline CASGoogle Scholar
• 27  Sargent CY, Berguig GY, Kinney MA et al.: Hydrodynamic modulation of embryonic stem cell differentiation by rotary orbital suspension culture. Biotechnol. Bioeng.105(3),611–626 (2010).
  Medline CASGoogle Scholar
• 28  Domian IJ, Chiravuri M, van der Meer P et al.: Generation of functional ventricular heart muscle from mouse ventricular progenitor cells. Science326(5951),426–429 (2009).
  Medline CASGoogle Scholar
• 29  Lim LP, Lau NC, Garrett-Engele P et al.: Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature433(7027),769–773 (2005).
  Medline CASGoogle Scholar
• 30  Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R: DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat. Genet.39(3),380–385 (2007).
  Medline CASGoogle Scholar
• 31  Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ: Characterization of Dicer-deficient murine embryonic stem cells. Proc. Natl Acad. Sci. USA102(34),12135–12140 (2005).
  Medline CASGoogle Scholar
• 32  Kanellopoulou C, Muljo SA, Kung AL et al.: Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev.19(4),489–501 (2005).
  Medline CASGoogle Scholar
• 33  Bernstein E, Kim SY, Carmell MA et al.: Dicer is essential for mouse development. Nat. Genet.35(3),215–217 (2003).
  Medline CASGoogle Scholar
• 34  Zhao Y, Samal E, Srivastava D: Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature436(7048),214–220 (2005).
  Medline CASGoogle Scholar
• 35  Zhao Y, Ransom JF, Li A et al.: Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1–2. Cell129(2),303–317 (2007).
  Medline CASGoogle Scholar
• 36  Sayed D, Hong C, Chen IY, Lypowy J, Abdellatif M: MicroRNAs play an essential role in the development of cardiac hypertrophy. Circ. Res.100(3),416–424 (2007).
  Medline CASGoogle Scholar
• 37  Care A, Catalucci D, Felicetti F et al.: MicroRNA-133 controls cardiac hypertrophy. Nat. Med.13(5),613–618 (2007).
  Medline CASGoogle Scholar
• 38  Ivey KN, Muth A, Arnold J et al.: MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell2(3),219–229 (2008).▪▪ First demonstration that miRNAs control hESC differentiation.
  Medline CASGoogle Scholar
• 39  Kawamura T, Ono K, Morimoto T et al.: Acetylation of GATA-4 is involved in the differentiation of embryonic stem cells into cardiac myocytes. J. Biol. Chem.280(20),19682–19688 (2005).
  Medline CASGoogle Scholar
• 40  Takeuchi JK, Bruneau BG: Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature459(7247),708–711 (2009).▪ Determined a role for chromatin remodeling in directing cardiac differentiation.
  Medline CASGoogle Scholar
• 41  Xu C, Police S, Hassanipour M, Gold JD: Cardiac bodies: a novel culture method for enrichment of cardiomyocytes derived from human embryonic stem cells. Stem Cells Dev.15(5),631–639 (2006).
  Medline CASGoogle Scholar
• 42  Hattori F, Chen H, Yamashita H et al.: Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat. Methods7(1),61–66 (2010).
  Medline CASGoogle Scholar
• 43  Huber I, Itzhaki I, Caspi O et al.: Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. FASEB J.21(10),2551–2563 (2007).
  Medline CASGoogle Scholar
• 44  Xu XQ, Zweigerdt R, Soo SY et al.: Highly enriched cardiomyocytes from human embryonic stem cells. Cytotherapy10(4),376–389 (2008).
  MedlineGoogle Scholar
• 45  Kita-Matsuo H, Barcova M, Prigozhina N et al.: Lentiviral vectors and protocols for creation of stable hESC lines for fluorescent tracking and drug resistance selection of cardiomyocytes. PLoS ONE4(4),e5046 (2009).
  MedlineGoogle Scholar
• 46  Anderson D, Self T, Mellor IR, Goh G, Hill SJ, Denning C: Transgenic enrichment of cardiomyocytes from human embryonic stem cells. Mol. Ther.15(11),2027–2036 (2007).
  Medline CASGoogle Scholar
• 47  Santangelo P, Nitin N, Bao G: Nanostructured probes for RNA detection in living cells. Ann. Biomed. Eng.34(1),39–50 (2006).
  MedlineGoogle Scholar
• 48  Wu SM, Fujiwara Y, Cibulsky SM et al.: Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell127(6),1137–1150 (2006).
  Medline CASGoogle Scholar
• 49  Kouskoff V, Lacaud G, Schwantz S, Fehling HJ, Keller G: Sequential development of hematopoietic and cardiac mesoderm during embryonic stem cell differentiation. Proc. Natl Acad. Sci. USA102(37),13170–13175 (2005).
  Medline CASGoogle Scholar
• 50  Fehling HJ, Lacaud G, Kubo A et al.: Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development130(17),4217–4227 (2003).
  Medline CASGoogle Scholar
• 51  Kattman SJ, Huber TL, Keller GM: Multipotent flk-1⁺ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev. Cell11(5),723–732 (2006).▪ Among the first studies to demonstrate that major cardiac lineages may arise from a common progenitor.
  Medline CASGoogle Scholar
• 52  Moretti A, Caron L, Nakano A et al.: Multipotent embryonic Isl1⁺ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell127(6),1151–1165 (2006).▪ Among the first studies to demonstrate that major cardiac lineages may arise from a common progenitor.
  Medline CASGoogle Scholar
• 53  Bu L, Jiang X, Martin-Puig S et al.: Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature460(7251),113–117 (2009).▪ Identification of human cardiac progenitors derived from hESCs.
  Medline CASGoogle Scholar
• 54  Kitajima S, Takagi A, Inoue T, Saga Y: MesP1 and MesP2 are essential for the development of cardiac mesoderm. Development127(15),3215–3226 (2000).
  Medline CASGoogle Scholar
• 55  Saga Y, Hata N, Kobayashi S, Magnuson T, Seldin MF, Taketo MM: MesP1: a novel basic helix–loop–helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development122(9),2769–2778 (1996).
  Medline CASGoogle Scholar
• 56  Saga Y, Kitajima S, Miyagawa-Tomita S: Mesp1 expression is the earliest sign of cardiovascular development. Trends Cardiovasc. Med.10(8),345–352 (2000).
  Medline CASGoogle Scholar
• 57  Saga Y, Miyagawa-Tomita S, Takagi A, Kitajima S, Miyazaki J, Inoue T: MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development126(15),3437–3447 (1999).
  Medline CASGoogle Scholar
• 58  Bondue A, Lapouge G, Paulissen C et al.: Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell3(1),69–84 (2008).
  Medline CASGoogle Scholar
• 59  Lindsley RC, Gill JG, Murphy TL et al.: Mesp1 coordinately regulates cardiovascular fate restriction and epithelial-mesenchymal transition in differentiating ESCs. Cell Stem Cell3(1),55–68 (2008).
  Medline CASGoogle Scholar
• 60  David R, Brenner C, Stieber J et al.: MesP1 drives vertebrate cardiovascular differentiation through DKK-1-mediated blockade of Wnt-signalling. Nat. Cell Biol.10(3),338–345 (2008).
  Medline CASGoogle Scholar
• 61  Carpenter MK, Rosler ES, Fisk GJ et al.: Properties of four human embryonic stem cell lines maintained in a feeder-free culture system. Dev. Dyn.229(2),243–258 (2004).
  Medline CASGoogle Scholar
• 62  King FW, Ritner C, Liszewski W et al.: Subpopulations of human embryonic stem cells with distinct tissue-specific fates can be selected from pluripotent cultures. Stem Cells Dev.18(10),1441–1450 (2009).▪▪ Determined that undifferentiated hESC cultures contain stem cell populations with predetermined fates.
  Medline CASGoogle Scholar
• 63  Laflamme MA, Gold J, Xu C et al.: Formation of human myocardium in the rat heart from human embryonic stem cells. Am. J. Pathol.167(3),663–671 (2005).
  Medline CASGoogle Scholar
• 64  van Laake LW, Passier R, Monshouwer-Kloots J et al.: Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction. Stem Cell Res.1(1),9–24 (2007).
  MedlineGoogle Scholar
• 65  van Laake LW, Passier R, Monshouwer-Kloots J et al.: Monitoring of cell therapy and assessment of cardiac function using magnetic resonance imaging in a mouse model of myocardial infarction. Nat. Protoc.2(10),2551–2567 (2007).
  Medline CASGoogle Scholar
• 66  van Laake LW, Passier R, Doevendans PA, Mummery CL: Human embryonic stem cell-derived cardiomyocytes and cardiac repair in rodents. Circ. Res.102(9),1008–1010 (2008).▪ Extended the assessment of cardiac function in mice to 12 weeks following hESC-derived CM transplantation, underscoring the importance of long-term analysis and the challenges to using rodents as a preclinical model for myocardial therapy.
  Medline CASGoogle Scholar
• 67  Leor J, Gerecht S, Cohen S et al.: Human embryonic stem cell transplantation to repair the infarcted myocardium. Heart93(10),1278–1284 (2007).
  MedlineGoogle Scholar
• 68  Kofidis T, Lebl DR, Swijnenburg RJ, Greeve JM, Klima U, Robbins RC: Allopurinol/uricase and ibuprofen enhance engraftment of cardiomyocyte-enriched human embryonic stem cells and improve cardiac function following myocardial injury. Eur. J. Cardiothorac. Surg.29(1),50–55 (2006).
  MedlineGoogle Scholar
• 69  Caspi O, Huber I, Kehat I et al.: Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. J. Am. Coll. Cardiol.50(19),1884–1893 (2007).
  MedlineGoogle Scholar
• 70  Angeli FS, Shapiro M, Amabile N et al.: Left ventricular remodeling after myocardial infarction: characterization of a swine model on β-blocker therapy. Comp. Med.59(3),272–279 (2009).
  Medline CASGoogle Scholar
• 71  Everett TH 4th, Wilson EE, Foreman S, Olgin JE: Mechanisms of ventricular fibrillation in canine models of congestive heart failure and ischemia assessed by in vivo noncontact mapping. Circulation112(11),1532–1541 (2005).
  MedlineGoogle Scholar
• 72  Kehat I, Khimovich L, Caspi O et al.: Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat. Biotechnol.22(10),1282–1289 (2004).
  Medline CASGoogle Scholar
• 73  Drukker M, Katchman H, Katz G et al.: Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells24(2),221–229 (2006).
  MedlineGoogle Scholar
• 74  Foldes G, Harding SE, Ali NN: Cardiomyocytes from embryonic stem cells: towards human therapy. Expert Opin. Biol. Ther.8(10),1473–1483 (2008).
  MedlineGoogle Scholar
• 75  Martin-Puig S, Wang Z, Chien KR: Lives of a heart cell: tracing the origins of cardiac progenitors. Cell Stem Cell2(4),320–331 (2008).
  Medline CASGoogle Scholar
• 76  Murry CE, Keller G: Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell132(4),661–680 (2008).
  Medline CASGoogle Scholar